Reproductive toxicities of tetradecyltrimethylammonium chloride and tetradecyltrimethylammonium bromide on Caenorhabditis elegans over four consecutive generations

Reproductive toxicities of tetradecyltrimethylammonium chloride and tetradecyltrimethylammonium bromide on Caenorhabditis elegans over four consecutive generations | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Reproductive toxicities of tetradecyltrimethylammonium chloride and tetradecyltrimethylammonium bromide on Caenorhabditis elegans over four consecutive generations Jing Zhang, Ruoqi Ding, Zhenyang Yu This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3528355/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Quaternary ammonium compounds (QACs) become emerging pollutants and their toxicities earn increasing attentions. So far, their reproductive toxicities were poorly investigated, and their effects over generations were even less explored. In the present study, reproductive toxicities of two QACs, i.e., tetradecyltrimethylammonium chloride (TTAC) and tetradecyltrimethylammonium bromide (TTAB) were studied on Caenorhabditis elegans with a consecutive exposure over four generations (from F1 to F4). The effects of TTAC on total reproduction showed stimulation and inhibition which oscillated from F1 to F4, and such oscillation was also observed in the effects on initial reproduction. The effects of TTAB on the total reproduction commonly showed stimulation over generations. The greatest stimulation was in F2, and it was accompanied with inhibition on the initial reproduction but stimulation on the reproduction duration. Further mechanisms exploration demonstrated that both TTAC and TTAB significantly disturbed the levels of SPE8, SPE9, Vg, MSP and VAB-1 and the expressions of vab-1 , ceh-18 , set-2 , met-2 and mes-4 over generations. Such disturbances demonstrated that both QACs impacted the reproductive processes in multiple aspects including oocyte meiosis, gonadal support and germline development. Further analysis also showed that the effects of both TTAC and TTAB in parents were connected with those in the offspring, which highlighted the conjunctive roles of reproduction in responses of adjacent generations. In addition, the differences the effects of TTAC and TTAB also demonstrated the anionic influences on the QACs’ toxicities. Multigenerational effect Oocyte meiosis Gonadal support Germline development Anionic influence Figures Figure 1 Figure 2 Figure 3 Figure 4 1. Introduction Quaternary ammonium compounds (QACs) have wide application in disinfectants, biocides, environmental remediation and even carbon capture (Abe and Kishimura 2022 , Roy and Ahmaruzzaman 2022 , Mai et al. 2023 ). Their discharge into the environment during application and through effluents and sludge earned increasing attentions on their toxicities (Jardak et al. 2016 , Mohapatra et al. 2023 ). It was reported that QACs showed mutagenic effects in bioluminescence assays (Dmochowska et al. 2016 ), growth inhibition and respiratory damage in beagles, mice and rats (Luz et al. 2020 , Park et al. 2023 ), and even promotion on resistance gene transfer (Han et al. 2019 , Liu et al. 2023 ). However, their toxicities still need more studies to fully demonstrate their environmental impacts on ecosystem and human health. The reproductive toxicities are very important in ecological risk and hazard evaluation. It was reported that QACs significantly decreased reproduction, caused birth defects and impacted the development of ovaries in mice and rats (Jiao et al. 2017 , Hrubec et al. 2021 , Matsumoto et al. 2021 ). In the yeast assays and in vitro cell line studies, QACs impacted hormones that are important in reproduction (Hrubec et al. 2021 , Liwarska-Bizukojc et al. 2021 ). Notably, the reproduction process connects adjacent generations and its changes by pollutants can represent intergenerational influences. As expected, QACs (e.g., didecyldimethyl ammonium chloride and alkyl dimethyl benzyl ammonium chloride) indeed impacted the body weight of the rat offspring in the exposure over generations (Luz et al. 2020 ). However, it remained poorly reported the reproductive toxicities of QACs over generations and also urged systematic exploration on the mechanisms. Reproduction involves a series of subtle processes with the various regulations. In Caenorhabditis elegans , the reproduction includes (1) spermiogenesis, which is triggered by spermatocyte protein 8 (SPE8) and promoted by vitellogenin (Vg) (Han et al. 2010 , Ellis and Stanfield 2014 ); (2) oogenesis, which includes mitogen-activated protein kinase (MAPK) activation, binding of major sperm protein (MSP) to VAB-1 Eph receptor protein-tyrosine kinase, POU-homeoprotein ( ceh-18 ) in gonadal sheath cells and also Gα o/i and Gα s signaling pathways (Govindan et al. 2006 , Yamamoto et al. 2006 ); and (3) the sperm-oocyte interactions and fertilization which are ensured with SPE9 (Marcello and Singson 2010 ). The process also requires epigenetic regulations by histone methylation at H3K4 ( set-2 ), H3K9 ( met-2 ) and H3K36 ( mes-4 ) sites (González-Aguilera et al. 2013 , Herbette et al. 2017 ). The reproduction of C. elegans was widely to employed to investigate toxicities of environmental pollutants, e.g., (Wang et al. 2018 , Huang et al. 2023 , Liu et al. 2024 ). Changes in aforementioned processes explained the reproductive toxicities of ionic liquids (ILs) (Yue et al. 2021 , Wang et al. 2023 ). Therefore, they are expected to explain the reproductive toxicities of QACs. The present study aimed to explore the reproductive toxicity of two representative QACs, i.e., tetradecyltrimethylammonium chloride (TTAC) and tetradecyltrimethylammonium bromide (TTAB) with an exposure over four consecutive generations. The toxicity mechanisms were explored changes in SPE8, Vg, vitellogenin (Vn), MAPK, MSP and VAB-1, and the expressions of genetic and epigenetic regulating genes. Further hierarchical cluster analysis (HCA) and correlation analysis were employed to explore the connections among indicators underlying the reproductive toxicities over generations. 2. Method and Materials 2.1. Chemicals Tetradecyltrimethylammonium chloride (TTAC, CAS No.: 4574-04-3, 99%) and tetradecyltrimethylammonium bromide (TTAB, CAS No.: 1119-97-7, 99%) were purchased from Adamas-beta. Stock solutions were prepared with sterile K-medium (0.051 M NaCl and 0.032 M KCl) and their nominal concentrations were arranged as 0.88 mg/L. 2.2. Preparation of organism Wild-type N2 C. elegans were cultured on nematode growth medium (NGM) agars at 20 ºC temperature with Escherichia coli OP50 as food (Yu et al. 2017 ). Gravid nematodes were lysed with fresh-made clorox solution (1% NaClO and 0.5 mol/L NaOH) to obtain age-synchronized eggs which were used in subsequent experiments (Yue et al. 2021 ). 2.3. Multi-generational reproduction For the exposure, 200.0 mL warm NGM containing 2.0 mL stock solutions or sterile K-medium solutions (served as the control) was aliquoted into 10 petri dishes as replicates in each group (Yu et al. 2017 , Yue et al. 2021 ). The exposure concentration was 0.0088 mg/L, at which TTAC and TTAB did not provoke significant lethality (less than 5%). The NGM agars further received same amounts of E. coli OP50 to form a bacterial lawn. At last, the NGM agars received same amounts of age-synchronization nematode eggs to start the F1 exposure. On the 3rd day in F1, adult nematodes were used for reproduction measurement, preparation for next generation exposure and sample collection. Briefly, 48 adult nematodes in every group were transferred daily onto 24 new NGM agars (i.e., two adults per agar) containing the same TTAC/TTAB or K-medium solutions to measure initial reproduction (offspring within the first 72 h), total reproduction and reproduction duration (Yu et al. 2017 , Liu et al. 2020 ). Another 100 adult nematodes in each group including the control were transferred onto ten replicate agars containing the same TTAC/TTAB or K-medium solutions. With the adults discarded after 24 h, the newly laid eggs started the F2 exposure (Yue et al. 2021 ). The rest nematodes were collected as samples for subsequent assays. Through the same way, the multi-generational exposure lasted for 4 consecutive generations (i.e., F1 to F4). 2.4. Biochemical assays Nematode samples were homogenized in ice bath and centrifuged at 4 ºC, and the supernatants were aliquoted into new centrifuge tubes for subsequent bioassays (Liu et al. 2020 , Yue et al. 2021 ). The contents or activities of MSP, VAB-1, SPE-9, SPE-8, Vg, vitellin (Vn) and MAPK were determined via microplate reader using the commercial enzyme-linked immune-sorbent assay (ELISA) kits (Shanghai Zhanshi Biotechnology Co. LTD). They were normalized as their portions against the total protein (TP, measured via BCA protein assay kits) in the same sample. 2.5. Gene expression analysis The total RNA was isolated using TRIzol reagent and functioned as templates to synthesize cDNA according to the instruction of M-MLV, Promega (Li et al. 2020 ). Subsequent real-time polymerase chain reaction (RT-PCR) with SYBR Green Master Mix was performed on Applied Biosystems 7900HT Fast Real-Time PCR System (USA). The primers (Table S1 in Supporting information) were designed with Primer Premier (6.0, Premier Biosoft Inc., CA). The gene expressions were quantified using the 2 −ΔΔCT method with gpd-1 as the reference gene. 2.6. Data presentation and statistical analysis Data in each sample were presented as fold-change against those in the concurrent control in the same generation (Liu et al. 2020 , Yue et al. 2021 ). Significant differences between control and treatment and among generations were analyzed via two-way ANOVA with Tukey post hoc test at the level of 0.05 (p < 0.05). The hierarchical component analysis (HCA) and Pearson’s rank correlation statistics were performed to explore further connection among the indicators (Yu et al. 2019 , Yue et al. 2021 ). 3. Results 3.1. Multi-generational reproductive effects of TTAC and TTAB Results showed that TTAC caused significant stimulation on the total reproduction in F1, inhibition in F2, stimulation again in F3 and inhibition in F4 (Fig. 1 (A)). Moreover, the effects of TTAC on the initial reproduction were generally similar to those on the total reproduction. Notably, the effects of TTAC on the reproduction duration showed inhibition in F1 and stimulation in F2 to F4. The stimulation on the reproduction duration in F2 and F4 spared more time for reproduction but it was not enough to compensate the inhibition on initial reproduction, and therefore resulted in the inhibition in the total reproduction. Summing up, the multi-generational reproductive effects of TTAC showed oscillatory changes between stimulation and inhibition over generations. Moreover, the effects were mainly resulted from the influences on the initial reproduction which was not compensated by the prolonged reproduction duration. (Fig. 1 around here) In the aspect of TTAB, it showed stimulation on the total reproduction in all generations with the greatest stimulation in F2 (Fig. 1 (B)). It showed stimulation on the initial reproduction in F1, F3 and F4, but inhibition in F2. It also commonly stimulated the reproduction duration in all generations. In other words, the reproductive increases by TTAC in F1, F3 and F4 were resulted from both initial reproduction and reproduction duration. Meanwhile, the reproductive increases in F2 were mainly resulted from longer reproduction duration instead of the initial reproduction. The different results of TTAC and TTAB showed the influences of anions on the reproductive toxicities of QACs. 3.2. Multi-generational effects of TTAC and TTAB on essential reproduction proteins Multi-generational effects of TTAC on essential reproduction proteins are showed in Fig. 2 (A). In F1, TTAC inhibited MSP and Vg, and stimulated VAB-1, SPE9 and SPE8. In F2, it stimulated MSP and SPE8, and inhibited SPE9, Vg and MAPK. In F3, it inhibited MSP, VAB-1, SPE9 and Vn, and stimulated Vg and MAPK. In F4, it stimulated MSP and Vn, and inhibited VAB-1 and Vg. Summing up, effects of TTAC oscillated between stimulation and inhibition on all proteins over generations. Combining the biochemical effects, the IBR values were 2.21, 2.17, 2.10 and 2.34 in F1 to F4, respectively. Compared with the IBR value in the control (2.60), the overall effects of TTAC commonly showed inhibition Fig. 2 (C). Effects of TTAB on the proteins also showed oscillation between stimulation and inhibition over generations (Fig. 2 (B)). The IBR values were 2.43, 2.12, 2.18 and 2.34 in F1 to F4, respectively. The overall effects of TTAB also commonly inhibition. (Fig. 2 around here) 3.3. Multi-generational effects of TTAC and TTAB on genetic regulations In F1, TTAC upregulated all gene expressions (Fig. 3 (A)). In F2, it upregulated the expressions of set-2 , met-2 , mes-4 and vab-1 and downregulated those of ceh-18 . In F3, it upregulated the expressions of set-2 , mes-4 and vab-1 , and downregulated those of ceh-18 and gsa-1 . In F4, it upregulated expressions of set-2 , met-2 , mes-4 , vab-1 and gsa-1 , and downregulated those of ceh-18 . The IBR values were 13.4, 3.72, 2.43 and 2.60 in F1 to F4, respectively. Compared with the IBR value of the control (2.74), the overall effects of TTAC on gene expressions were stimulatory in F1 and F2, and inhibitory in F3 and F4 (Fig. 3 (C)). (Fig. 3 around here) In F1, TTAB did not show significant influences on all gene expressions (Fig. 3 (B)). In F2, it upregulated the expressions of set-2 , met-2 , mes-4 , vab-1 and gsa-1 , and downregulated those of ceh-18 . In F3, it upregulated the expressions of set-2 , mes-4 , vab-1 and gsa-1 , and downregulated those of ceh-18 . In F4, it upregulated expressions of set-2 , mes-4 , vab-1 and gsa-1 , and downregulated those of met-2 and ceh-18 . Collectively, the expression levels showed oscillation between upregulation and downregulation over generations. The IBR values were 2.33, 9.51, 2.86 and 2.60 in F1 to F4, respectively (Fig. 3 (C)). The overall effects of TTAB on gene expressions were inhibitory in F1 and F4 and stimulatory in F2 and F3. 3.4. Overall analysis on multi-generational effects of TTAC and TTAB In the HCA results, the effects of TTAC on reproduction (including initial reproduction, total reproduction and reproduction duration) and reproduction-related proteins (including MSP, VAB-1, SPE9, SPE8, Vg and Vn) in F1 were closed clustered showing close connection (Fig. 4 (A)). Interestingly, the effects of TTAC on the gene expressions in F1 were more closely connected with the effects on reproduction in F2. Moreover, the effects on expressions of vab-1 , ceh-18 and gsa-1 in F2 were also more closely connected with those on reproduction in F3. In addition, the effects on SPE-8, Vg, Vn and MAPK and those on the gene regulation in F3 were also more closely connected with the effects on reproduction in F4. Summing up, the effects of TTAC on parents were closely connected with those on the offspring. The effects of TTAB in parent generations were also closely related with those on the offspring (Fig. 4 B). Moreover, the effects of TTAC in F1 were even connected with those in F3 and F4, and the effects of TTAB in F1 and F2 also showed close connection with those in F4. That is to say, the close connection among indicators expanded over adjacent generations. (Fig. 4 around here) (Tables 1 & 2 around here) Table 1 Pearson’s correlation between reproduction and biochemicals, between reproduction and gene expressions, and between biochemicals and gene expressions in the toxicities of tetradecyltrimethylammonium chloride (TTAC). TTAC IR TR MSP VAB-1 SPE-9 SPE-8 Vg Vn MAPK set-2 met-2 mes-4 vab-1 ceh-18 gsa-1 IR - 1.000 0.612 0.733 0.741 0.740 0.758 0.651 0.813 0.695 0.701 0.751 0.756 0.836 0.718 TR - 0.618 0.739 0.746 0.747 0.763 0.656 0.815 0.698 0.704 0.756 0.762 0.838 0.721 MSP - 0.964* 0.948* 0.973* 0.976* 0.988* 0.941* 0.539 0.585 0.724 0.766 0.553 0.413 VAB-1 - 0.992* 0.998* 0.964* 0.980* 0.959* 0.737 0.770 0.876 0.907* 0.751 0.638 SPE-9 - 0.985* 0.949* 0.980* 0.969* 0.771 0.808 0.900* 0.918* 0.779 0.670 SPE-8 - 0.978* 0.981* 0.964* 0.699 0.733 0.849 0.884* 0.725 0.602 Vg - 0.968* 0.978* 0.567 0.608 0.744 0.783 0.627 0.471 Vn - 0.964* 0.636 0.683 0.800 0.828 0.640 0.512 MAPK - 0.660 0.704 0.810 0.828 0.715 0.570 set-2 - 0.997 0.971* 0.950* 0.973* 0.982* met-2 - 0.981* 0.959* 0.967* 0.966* mes-4 - 0.994* 0.956* 0.922* vab-1 - 0.940* 0.897* ceh-18 - 0.978* gsa-1 - *, at 0.05 level. Table 2 Pearson’s correlation between reproduction and biochemicals, between reproduction and gene expressions, and between biochemicals and gene expressions in the toxicities of tetradecyltrimethylammonium bromide (TTAB). TTAB IR TR MSP VAB-1 SPE-9 SPE-8 Vg Vn MAPK set-2 met-2 mes-4 vab-1 ceh-18 gsa-1 IR - 0.846 0.968* 0.990* 0.980* 0.972* 0.976* 0.983* 0.980* 0.635 0.628 0.431 0.801 0.929* 0.717 TR - 0.940* 0.895* 0.922* 0.945* 0.926* 0.926* 0.911* 0.931* 0.946* 0.836 0.980* 0.856 0.616 MSP - 0.990* 0.982* 0.998* 0.996* 0.996* 0.982* 0.806 0.780 0.637 0.925* 0.893* 0.774 VAB-1 - 0.990* 0.991* 0.996* 0.997* 0.994* 0.718 0.702 0.531 0.867 0.919* 0.756 SPE-9 - 0.992* 0.991* 0.994* 0.997* 0.735 0.753 0.565 0.875 0.960* 0.664 SPE-8 - 0.997* 0.998* 0.990* 0.796 0.788 0.630 0.918* 0.921* 0.730 Vg - 0.998* 0.994* 0.771 0.756 0.599 0.905* 0.913* 0.756 Vn - 0.994* 0.762 0.753 0.586 0.896* 0.927* 0.735 MAPK - 0.727 0.735 0.555 0.873 0.946* 0.697 set-2 - 0.966* 0.967* 0.968* 0.609 0.622 met-2 - 0.951* 0.937* 0.697 0.440 mes-4 - 0.881* 0.455 0.451 vab-1 - 0.758 0.717 ceh-18 - 0.436 gsa-1 - *, at 0.05 level. In the Pearson’s correlation results, the biochemical effects of TTAC (e.g., on MSP, VAB-1, SPE-9, SPE-8, Vg, Vn and MAPK) were well correlated with themselves and also occasionally with those on mes-4 and vab-1 expressions (Table 1 ). Meanwhile, the biochemical effects of TTAB showed correlations with themselves, but also with reproduction, and commonly with those on vab-1 and ceh-18 expressions (Table 2 ). The results demonstrated the connection among indicators and also the differences between TTAC and TTAB. 4. Discussion 4.1. Multi-generational reproductive effects of TTAC and TTAB The multigenerational reproductive effects showed oscillation between stimulation and inhibition over generations. The similar oscillations were also observed in multigenerational effects of imidazole-based ILs (Yue et al. 2021 , Zhang and Feng 2022 , Wang et al. 2023 ), pyridine-based ILs (Shi et al. 2021 , Zhang et al. 2022 ), and antibiotics (e.g., sulfamethoxazole, enrofloxacin, ofloxacin and norfloxacin) (Li et al. 2020 , Zhang et al. 2022 , Zheng et al. 2022 ). Offspring in uterus prepared similar responses to their maternal experiences via fetal reprogramming for better adaptation to the environment (Li et al. 2020 ). However, such preparation does not guarantee the matching with the actual requirement of the offspring. Accordingly, the outcomes in the offspring can be stimulation, inhibition and even non-significant influences, therefore explaining the oscillatory changes over generations. More investigation is needed to establish models for predicting multigenerational effects in the future. Similar to the effects of TTAB, pyridine-based ILs and antibiotics also caused consistent effects on the initial and total reproduction of nematodes (Shi et al. 2021 , Zhang et al. 2022 , Zhang et al. 2022 ). Meanwhile, the effects of TTAC in F2 showed inconsistence between effects on the initial reproduction and those on the total reproduction with compensation from longer reproduction duration. Notably, animals in the actual environment would reproduce as early as possible to ensure the population growth (Yu et al. 2017 ), and delayed reproduction with longer reproduction duration would be unrealistic due to accidental death or predation. Therefore, with or without compensation by longer reproduction duration, the reproductive toxicities of TTAC and TTAB would significantly influence the population growth and their ecological risks should be seriously considered in their application. It was known that QACs are cationic surfactants, and therefore most investigations were studied on cationic toxicity on various organisms (Luz et al. 2020 , Suthar et al. 2022 ). The present study showed the different results of TTAC and TTAB, which showed the influences of anions on the reproductive toxicities. In future studies, the anionic influences should be considered in the QACs toxicities to more accurate evaluation on their ecological risks. 4.2. Mechanisms of the multi-generational reproductive effects In the reproductive processes, the spermiogenesis is triggered via SPE8 and the sperm movement is promoted by Vg (Han et al. 2010 , Ellis and Stanfield 2014 ), the oocyte meiotic maturation is regulated by MAPK activation and binding of MSP to VAB-1 (Govindan et al. 2006 , Yamamoto et al. 2006 ), and the sperm-oocyte interactions and fertilization are ensured with SPE9 (Marcello and Singson 2010 ). At the molecular level, the expressions of vab-1 , ceh-18 , set-2 , met-2 and mes-4 regulate the oocyte meiotic maturation, gonadal sheath cells and germline genome integrity (Govindan et al. 2006 , Yamamoto et al. 2006 , González-Aguilera et al. 2013 , Herbette et al. 2017 ). The effects of TTAB on the reproduction showed positive correlations with those on the aforementioned biochemicals and those on the expressions of the aforementioned genes. Moreover, the effects of TTAB on the gene expressions (e.g., vab-1 and ceh-18 ) were also positively correlated with those on the biochemicals including MSP, SPE-9, Vg and MAPK. The correlation demonstrated that the reproductive toxicities of TTAB were well related with its impacts on the whole reproductive processes including oocyte meiosis, gonadal support and germline development. However, the effects of TTAC did not show such correlations as those in the results of TTAB, and therefore the differences supported the anionic influences on QACs toxicities as well. Notably, the effects of both TTAC and TTAB in parents were connected with those in the offspring. The connection was also observed in the multi-generational effects of antibiotics and ILs (Zhang et al. 2022 , Wang et al. 2023 ). Such connection supported that reproductive processes provided one essential tie to combine health over generations. Especially, the expressions of set-2 , met-2 and mes-4 involved histone methylation (e.g., at H3K4, H3K9 and H3K36 sites) to preserve germline genome integrity and normal development (González-Aguilera et al. 2013 , Herbette et al. 2017 ). Therefore, the connection in the effects between generations also supported the involvement of epigenetic modulation on the responses of offspring to the maternal experience (Yue et al. 2021 ). Therefore, further studies are still needed to explore the epigenetic mechanisms underlying the multigenerational consequences of pollutants. 5. Conclusion Both TTAC and TTAB caused reproductive toxicities with changes over generations. The reproductive effects of TTAC showed oscillation between stimulation and inhibition over generations. The toxicities of TTAB on initial reproduction can be compensated by reproduction duration. Biochemical and gene expression results showed that TTAC and TTAB impacted oocyte meiosis, gonadal support and germline development. Moreover, the reproductive toxicities also involved epigenetic regulations on histone methylation. In addition, the results also demonstrated the anionic influences on the toxicities of QACs. Declarations Ethical Approval: Not applicable. Consent to Participate and Publish: All authors agreed with authorship and the content, and approved to submit the present version to be published. Authors Contributions Formal analysis, investigation and writing original draft were performed by Jing Zhang. Experiment performance and data curation were performed by Ruoqi Ding. Supervision, project administration and funding acquisition were performed by Zhenyang Yu. Funding This work was supported by National Key Research and Development Program of China (2021YFC3200803). The authors are sincerely grateful for their financial support. Competing Interests The authors have no relevant financial interests to disclose. References Abe H, Kishimura H (2022) CO 2 -driven surface reconstruction in quaternary ammonium ionic liquid-propanol solutions. J Ionic Liquids 2:100018 Dmochowska B, Sikora K, Woziwodzka A, Piosik J, Podgórska B (2016) Mutagenic activity of quaternary ammonium salt derivatives of carbohydrates. Beilstein J Org Chem 12:1434–1439 Ellis RE, Stanfield GM (2014) The regulation of spermatogenesis and sperm function in nematodes. 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Sci Total Environ 778:146371 Suthar A, Gopalakkrishnan A, Maji C, Dahiya RK, Kumar R, Kumar S (2022) Evaluation of the inhibitory efficacy of quaternary ammonium compounds on in vitro growth of Theileria equi parasite in MASP culture. Int J Parasitol-Drug 20:11–16 Wang L, Wu D, Yu Z, Huang S, Zhang J (2023) Hormone-mediated multi- and trans-generational reproductive toxicities of 1-ethyl-3-methylimidazolium hexafluorophosphate on Caenorhabditis elegans . Sci Total Environ 863:160958 Wang S, Chu Z, Zhang K, Miao G (2018) Cadmium-induced serotonergic neuron and reproduction damages conferred lethality in the nematode Caenorhabditis elegans . Chemosphere 213:11–18 Yamamoto I, Kosinski ME, Greenstein D (2006) Start me up: Cell signaling and the journey from oocyte to embryo in C. elegans . Dev Dynam 235:571–585 Yu Z, Sun G, Liu Y, Yin D, Zhang J (2017) Trans-generational influences of sulfamethoxazole on lifespan, reproduction and population growth of Caenorhabditis elegans . Ecotoxicol Environ Safe 135:312–318 Yu ZY, Yin DQ, Zhang J (2019) Sex-dependent effects of sulfamethoxazole exposure on pro-/anti-oxidant status with stimulation on growth, behavior and reproduction in the amphipod Hyalella azteca . Environ Pollut 244:398–404 Yue WY, Mo LY, Zhang J (2021) Reproductive toxicities of 1-ethyl-3-methylimidazolium bromide on Caenorhabditis elegans with oscillation between inhibition and stimulation over generations. Sci Total Environ 765:144334 Zhang J, Feng L (2022) Intermittent multi-generational effects of 1-hexyl-3-methylimidazolium nitrate on Caenorhabditis elegans mediated by lipid metabolism. Sci Total Environ 812:152479 Zhang J, Shi Y, Yu Z (2022) Balances among reproduction, antioxidant responses and lipid metabolism underlying the multi-generational effects of N-butylpyridinium bromide on Caenorhabditis elegans . Sci Total Environ 846:157468 Zhang J, Zheng Y, Yu Z (2022) Reproductive toxicities of ofloxacin and norfloxacin on Caenorhabditis elegans with multi-generational oscillatory effects and trans-generational residual influences. Environ Toxicol Pharm 95:103962 Zheng YG, Yu ZY, Zhang J (2022) Multi-generational effects of enrofloxacin on lifespan and reproduction of Caenorhabditis elegans with SKN-1-mediated antioxidant responses and lipid metabolism disturbances. Sci Total Environ 804:150250 Supplementary Files 20231030TableS1.docx Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. 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Also discoverable on Platform About In Review Editorial Policies Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3528355","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":244580624,"identity":"a22fc2ee-252a-40ae-9dd7-2f8c025d30bd","order_by":0,"name":"Jing Zhang","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAuklEQVRIie3PsQrCMBCA4QuBulzImlKhr9BNhKKvclDo1MXFOVDIM7ToczinuNcHcPQFWro6GN/gugnmn264D+4AYrFfzABJgBK1tutIvU07zycQyL0sLDFFfrGv5eQeWIAX09wwiLj6OuvdE3fSyrS/MYg0VEsVyN76RCoOSQxVi3IjFp6YBA1RppxfQUw4LMOxwrQbWt4veddUC54PR63bYZo5JJxGIJLvICxrP7TxAG/uciwWi/1lH7/iMnxeho/3AAAAAElFTkSuQmCC","orcid":"","institution":"Shanghai Institute of Technology","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Jing","middleName":"","lastName":"Zhang","suffix":""},{"id":244580625,"identity":"4c28d1c9-e973-4724-8899-0fb4f9c29e3b","order_by":1,"name":"Ruoqi Ding","email":"","orcid":"","institution":"Shanghai Institute of Technology","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Ruoqi","middleName":"","lastName":"Ding","suffix":""},{"id":244580626,"identity":"2b996a44-5781-4a95-abce-d63af7f1d8fd","order_by":2,"name":"Zhenyang Yu","email":"","orcid":"","institution":"Jiaxing Tongji Institute for Environment","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Zhenyang","middleName":"","lastName":"Yu","suffix":""}],"badges":[],"createdAt":"2023-10-31 20:00:34","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3528355/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3528355/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":45764974,"identity":"05c3d5a5-dc06-462d-bc4b-26a1c1650e95","added_by":"auto","created_at":"2023-11-02 19:32:25","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":72710,"visible":true,"origin":"","legend":"\u003cp\u003eEffects of tetradecyltrimethylammonium chloride (TTAC) and tetradecyltrimethylammonium bromide (TTAB) on reproduction of \u003cem\u003eC. elegans\u003c/em\u003e via multi-generational exposure from F1 to F4. *, significantly different from control group (1.0) at 0.05 level by ANOVA; +, significantly different from the earlier generation at the same concentration 0.05 level. The data in the figure were represented as mean ± standard deviation.\u003c/p\u003e","description":"","filename":"1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-3528355/v1/30fe4b20cab324ad7ef786f8.jpg"},{"id":45764973,"identity":"7e1d7b31-1f86-45e5-a25f-36783b3347c5","added_by":"auto","created_at":"2023-11-02 19:32:25","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":62694,"visible":true,"origin":"","legend":"\u003cp\u003eMulti-generational effects of TTAC and TTAB on major sperm protein (MSP), ephrin receptor protein tyrosine kinase (VAB-1), spermatocyte protein 8 (SPE8), sperm transmembrane protein 9 (SPE9), vitellogenin (Vg), vitellin (Vn) and mitogen-activated protein kinase (MAPK) of\u003cem\u003e C. elegans. \u003c/em\u003e*, significantly different from control group (2.60) at 0.05 level by ANOVA; +, significantly different from the earlier generation at the same concentration 0.05 level. The data in the figure were represented as mean ± standard deviation.\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-3528355/v1/b63fc29d680080c55368f8dc.png"},{"id":45764972,"identity":"73b85bf5-6057-4439-8da5-33e808819b86","added_by":"auto","created_at":"2023-11-02 19:32:25","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":46538,"visible":true,"origin":"","legend":"\u003cp\u003eMulti-generational effects of TTAC and TTAB on expressions of \u003cem\u003eset-2, met-2, mes-4, vab-1, ceh-18, gsa-1 \u003c/em\u003ein\u003cem\u003e C. elegans\u003c/em\u003e. *, significantly different from control group (2.74) at 0.05 level by ANOVA; #, significantly different between low and high concentrations in the generation at 0.05 level; +, significantly different from the earlier generation at the same concentration 0.05 level. The data in the figure were represented as mean ± standard deviation.\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-3528355/v1/8debfe595596ee6c91f092d3.png"},{"id":45764975,"identity":"a8088d8a-e00c-44c2-b093-cda681f801d4","added_by":"auto","created_at":"2023-11-02 19:32:25","extension":"jpeg","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":463035,"visible":true,"origin":"","legend":"\u003cp\u003eHierarchical cluster analysis on the multi-generational effects of TTAC and TTAB on initial reproduction (Initial Rep.), total reproduction (Total Rep.), reproduction duration (Rep. duration), essential reproduction proteins including spermatocyte protein 8 (SPE8), sperm transmembrane protein 9 (SPE9), major sperm protein (MSP), ephrin receptor protein tyrosine kinase (VAB-1), vitellogenin (Vg), vitellin (Vn), and mitogen-activated protein kinase (MPK-1) and gene expressions of \u003cem\u003eset-2\u003c/em\u003e, \u003cem\u003emet-2\u003c/em\u003e, \u003cem\u003emes-4\u003c/em\u003e, \u003cem\u003evab-1\u003c/em\u003e, \u003cem\u003eceh-18\u003c/em\u003e, \u003cem\u003egsa-1\u003c/em\u003e in \u003cem\u003eC. elegans\u003c/em\u003e.\u003c/p\u003e","description":"","filename":"floatimage4.jpeg","url":"https://assets-eu.researchsquare.com/files/rs-3528355/v1/18405494fc08972672de306c.jpeg"},{"id":47045365,"identity":"4acd3794-09bb-4dca-9976-72ad390f3ca5","added_by":"auto","created_at":"2023-11-24 21:30:07","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":736866,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3528355/v1/e5e69c43-c351-4577-ae47-9b293611605f.pdf"},{"id":45764976,"identity":"b73fe427-1f42-4843-b987-ea5bf69152e5","added_by":"auto","created_at":"2023-11-02 19:32:25","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":17901,"visible":true,"origin":"","legend":"","description":"","filename":"20231030TableS1.docx","url":"https://assets-eu.researchsquare.com/files/rs-3528355/v1/dcff92cffae96f275196eaf3.docx"}],"financialInterests":"","formattedTitle":"Reproductive toxicities of tetradecyltrimethylammonium chloride and tetradecyltrimethylammonium bromide on Caenorhabditis elegans over four consecutive generations","fulltext":[{"header":"1. Introduction","content":"\u003cp\u003eQuaternary ammonium compounds (QACs) have wide application in disinfectants, biocides, environmental remediation and even carbon capture (Abe and Kishimura \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2022\u003c/span\u003e, Roy and Ahmaruzzaman \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2022\u003c/span\u003e, Mai et al. \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Their discharge into the environment during application and through effluents and sludge earned increasing attentions on their toxicities (Jardak et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, Mohapatra et al. \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). It was reported that QACs showed mutagenic effects in bioluminescence assays (Dmochowska et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2016\u003c/span\u003e), growth inhibition and respiratory damage in beagles, mice and rats (Luz et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2020\u003c/span\u003e, Park et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2023\u003c/span\u003e), and even promotion on resistance gene transfer (Han et al. \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2019\u003c/span\u003e, Liu et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). However, their toxicities still need more studies to fully demonstrate their environmental impacts on ecosystem and human health.\u003c/p\u003e \u003cp\u003eThe reproductive toxicities are very important in ecological risk and hazard evaluation. It was reported that QACs significantly decreased reproduction, caused birth defects and impacted the development of ovaries in mice and rats (Jiao et al. \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2017\u003c/span\u003e, Hrubec et al. \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2021\u003c/span\u003e, Matsumoto et al. \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). In the yeast assays and \u003cem\u003ein vitro\u003c/em\u003e cell line studies, QACs impacted hormones that are important in reproduction (Hrubec et al. \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2021\u003c/span\u003e, Liwarska-Bizukojc et al. \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Notably, the reproduction process connects adjacent generations and its changes by pollutants can represent intergenerational influences. As expected, QACs (e.g., didecyldimethyl ammonium chloride and alkyl dimethyl benzyl ammonium chloride) indeed impacted the body weight of the rat offspring in the exposure over generations (Luz et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). However, it remained poorly reported the reproductive toxicities of QACs over generations and also urged systematic exploration on the mechanisms.\u003c/p\u003e \u003cp\u003eReproduction involves a series of subtle processes with the various regulations. In \u003cem\u003eCaenorhabditis elegans\u003c/em\u003e, the reproduction includes (1) spermiogenesis, which is triggered by spermatocyte protein 8 (SPE8) and promoted by vitellogenin (Vg) (Han et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2010\u003c/span\u003e, Ellis and Stanfield \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2014\u003c/span\u003e); (2) oogenesis, which includes mitogen-activated protein kinase (MAPK) activation, binding of major sperm protein (MSP) to VAB-1 Eph receptor protein-tyrosine kinase, POU-homeoprotein (\u003cem\u003eceh-18\u003c/em\u003e) in gonadal sheath cells and also Gα\u003csub\u003eo/i\u003c/sub\u003e and Gα\u003csub\u003es\u003c/sub\u003e signaling pathways (Govindan et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2006\u003c/span\u003e, Yamamoto et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2006\u003c/span\u003e); and (3) the sperm-oocyte interactions and fertilization which are ensured with SPE9 (Marcello and Singson \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). The process also requires epigenetic regulations by histone methylation at H3K4 (\u003cem\u003eset-2\u003c/em\u003e), H3K9 (\u003cem\u003emet-2\u003c/em\u003e) and H3K36 (\u003cem\u003emes-4\u003c/em\u003e) sites (Gonz\u0026aacute;lez-Aguilera et al. \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2013\u003c/span\u003e, Herbette et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). The reproduction of \u003cem\u003eC. elegans\u003c/em\u003e was widely to employed to investigate toxicities of environmental pollutants, e.g., (Wang et al. \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2018\u003c/span\u003e, Huang et al. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2023\u003c/span\u003e, Liu et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). Changes in aforementioned processes explained the reproductive toxicities of ionic liquids (ILs) (Yue et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2021\u003c/span\u003e, Wang et al. \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Therefore, they are expected to explain the reproductive toxicities of QACs.\u003c/p\u003e \u003cp\u003eThe present study aimed to explore the reproductive toxicity of two representative QACs, i.e., tetradecyltrimethylammonium chloride (TTAC) and tetradecyltrimethylammonium bromide (TTAB) with an exposure over four consecutive generations. The toxicity mechanisms were explored changes in SPE8, Vg, vitellogenin (Vn), MAPK, MSP and VAB-1, and the expressions of genetic and epigenetic regulating genes. Further hierarchical cluster analysis (HCA) and correlation analysis were employed to explore the connections among indicators underlying the reproductive toxicities over generations.\u003c/p\u003e"},{"header":"2. Method and Materials","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003e2.1. Chemicals\u003c/h2\u003e \u003cp\u003eTetradecyltrimethylammonium chloride (TTAC, CAS No.: 4574-04-3, 99%) and tetradecyltrimethylammonium bromide (TTAB, CAS No.: 1119-97-7, 99%) were purchased from Adamas-beta. Stock solutions were prepared with sterile K-medium (0.051 M NaCl and 0.032 M KCl) and their nominal concentrations were arranged as 0.88 mg/L.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003e2.2. Preparation of organism\u003c/h2\u003e \u003cp\u003eWild-type N2 \u003cem\u003eC. elegans\u003c/em\u003e were cultured on nematode growth medium (NGM) agars at 20 \u0026ordm;C temperature with \u003cem\u003eEscherichia coli\u003c/em\u003e OP50 as food (Yu et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Gravid nematodes were lysed with fresh-made clorox solution (1% NaClO and 0.5 mol/L NaOH) to obtain age-synchronized eggs which were used in subsequent experiments (Yue et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2021\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003e2.3. Multi-generational reproduction\u003c/h2\u003e \u003cp\u003eFor the exposure, 200.0 mL warm NGM containing 2.0 mL stock solutions or sterile K-medium solutions (served as the control) was aliquoted into 10 petri dishes as replicates in each group (Yu et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2017\u003c/span\u003e, Yue et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The exposure concentration was 0.0088 mg/L, at which TTAC and TTAB did not provoke significant lethality (less than 5%). The NGM agars further received same amounts of \u003cem\u003eE. coli\u003c/em\u003e OP50 to form a bacterial lawn. At last, the NGM agars received same amounts of age-synchronization nematode eggs to start the F1 exposure.\u003c/p\u003e \u003cp\u003eOn the 3rd day in F1, adult nematodes were used for reproduction measurement, preparation for next generation exposure and sample collection. Briefly, 48 adult nematodes in every group were transferred daily onto 24 new NGM agars (i.e., two adults per agar) containing the same TTAC/TTAB or K-medium solutions to measure initial reproduction (offspring within the first 72 h), total reproduction and reproduction duration (Yu et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2017\u003c/span\u003e, Liu et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Another 100 adult nematodes in each group including the control were transferred onto ten replicate agars containing the same TTAC/TTAB or K-medium solutions. With the adults discarded after 24 h, the newly laid eggs started the F2 exposure (Yue et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The rest nematodes were collected as samples for subsequent assays. Through the same way, the multi-generational exposure lasted for 4 consecutive generations (i.e., F1 to F4).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003e2.4. Biochemical assays\u003c/h2\u003e \u003cp\u003eNematode samples were homogenized in ice bath and centrifuged at 4 \u0026ordm;C, and the supernatants were aliquoted into new centrifuge tubes for subsequent bioassays (Liu et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2020\u003c/span\u003e, Yue et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The contents or activities of MSP, VAB-1, SPE-9, SPE-8, Vg, vitellin (Vn) and MAPK were determined via microplate reader using the commercial enzyme-linked immune-sorbent assay (ELISA) kits (Shanghai Zhanshi Biotechnology Co. LTD). They were normalized as their portions against the total protein (TP, measured via BCA protein assay kits) in the same sample.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003e2.5. Gene expression analysis\u003c/h2\u003e \u003cp\u003eThe total RNA was isolated using TRIzol reagent and functioned as templates to synthesize cDNA according to the instruction of M-MLV, Promega (Li et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Subsequent real-time polymerase chain reaction (RT-PCR) with SYBR Green Master Mix was performed on Applied Biosystems 7900HT Fast Real-Time PCR System (USA). The primers (Table \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e in Supporting information) were designed with Primer Premier (6.0, Premier Biosoft Inc., CA). The gene expressions were quantified using the 2\u003csup\u003e\u0026minus;ΔΔCT\u003c/sup\u003e method with \u003cem\u003egpd-1\u003c/em\u003e as the reference gene.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003e2.6. Data presentation and statistical analysis\u003c/h2\u003e \u003cp\u003eData in each sample were presented as fold-change against those in the concurrent control in the same generation (Liu et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2020\u003c/span\u003e, Yue et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Significant differences between control and treatment and among generations were analyzed via two-way ANOVA with Tukey \u003cem\u003epost hoc\u003c/em\u003e test at the level of 0.05 (p\u0026thinsp;\u0026lt;\u0026thinsp;0.05). The hierarchical component analysis (HCA) and Pearson\u0026rsquo;s rank correlation statistics were performed to explore further connection among the indicators (Yu et al. \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2019\u003c/span\u003e, Yue et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2021\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e"},{"header":"3. Results","content":"\u003cdiv id=\"Sec10\" class=\"Section2\"\u003e \u003ch2\u003e3.1. Multi-generational reproductive effects of TTAC and TTAB\u003c/h2\u003e \u003cp\u003eResults showed that TTAC caused significant stimulation on the total reproduction in F1, inhibition in F2, stimulation again in F3 and inhibition in F4 (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e(A)). Moreover, the effects of TTAC on the initial reproduction were generally similar to those on the total reproduction. Notably, the effects of TTAC on the reproduction duration showed inhibition in F1 and stimulation in F2 to F4. The stimulation on the reproduction duration in F2 and F4 spared more time for reproduction but it was not enough to compensate the inhibition on initial reproduction, and therefore resulted in the inhibition in the total reproduction. Summing up, the multi-generational reproductive effects of TTAC showed oscillatory changes between stimulation and inhibition over generations. Moreover, the effects were mainly resulted from the influences on the initial reproduction which was not compensated by the prolonged reproduction duration.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003e(Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e around here)\u003c/p\u003e \u003cp\u003eIn the aspect of TTAB, it showed stimulation on the total reproduction in all generations with the greatest stimulation in F2 (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e(B)). It showed stimulation on the initial reproduction in F1, F3 and F4, but inhibition in F2. It also commonly stimulated the reproduction duration in all generations. In other words, the reproductive increases by TTAC in F1, F3 and F4 were resulted from both initial reproduction and reproduction duration. Meanwhile, the reproductive increases in F2 were mainly resulted from longer reproduction duration instead of the initial reproduction. The different results of TTAC and TTAB showed the influences of anions on the reproductive toxicities of QACs.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003e3.2. Multi-generational effects of TTAC and TTAB on essential reproduction proteins\u003c/h2\u003e \u003cp\u003eMulti-generational effects of TTAC on essential reproduction proteins are showed in Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e(A). In F1, TTAC inhibited MSP and Vg, and stimulated VAB-1, SPE9 and SPE8. In F2, it stimulated MSP and SPE8, and inhibited SPE9, Vg and MAPK. In F3, it inhibited MSP, VAB-1, SPE9 and Vn, and stimulated Vg and MAPK. In F4, it stimulated MSP and Vn, and inhibited VAB-1 and Vg. Summing up, effects of TTAC oscillated between stimulation and inhibition on all proteins over generations. Combining the biochemical effects, the IBR values were 2.21, 2.17, 2.10 and 2.34 in F1 to F4, respectively. Compared with the IBR value in the control (2.60), the overall effects of TTAC commonly showed inhibition Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e(C).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eEffects of TTAB on the proteins also showed oscillation between stimulation and inhibition over generations (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e(B)). The IBR values were 2.43, 2.12, 2.18 and 2.34 in F1 to F4, respectively. The overall effects of TTAB also commonly inhibition.\u003c/p\u003e \u003cp\u003e(Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e around here)\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003e3.3. Multi-generational effects of TTAC and TTAB on genetic regulations\u003c/h2\u003e \u003cp\u003eIn F1, TTAC upregulated all gene expressions (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e(A)). In F2, it upregulated the expressions of \u003cem\u003eset-2\u003c/em\u003e, \u003cem\u003emet-2\u003c/em\u003e, \u003cem\u003emes-4\u003c/em\u003e and \u003cem\u003evab-1\u003c/em\u003e and downregulated those of \u003cem\u003eceh-18\u003c/em\u003e. In F3, it upregulated the expressions of \u003cem\u003eset-2\u003c/em\u003e, \u003cem\u003emes-4\u003c/em\u003e and \u003cem\u003evab-1\u003c/em\u003e, and downregulated those of \u003cem\u003eceh-18\u003c/em\u003e and \u003cem\u003egsa-1\u003c/em\u003e. In F4, it upregulated expressions of \u003cem\u003eset-2\u003c/em\u003e, \u003cem\u003emet-2\u003c/em\u003e, \u003cem\u003emes-4\u003c/em\u003e, \u003cem\u003evab-1\u003c/em\u003e and \u003cem\u003egsa-1\u003c/em\u003e, and downregulated those of \u003cem\u003eceh-18\u003c/em\u003e. The IBR values were 13.4, 3.72, 2.43 and 2.60 in F1 to F4, respectively. Compared with the IBR value of the control (2.74), the overall effects of TTAC on gene expressions were stimulatory in F1 and F2, and inhibitory in F3 and F4 (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e(C)).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003e(Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e around here)\u003c/p\u003e \u003cp\u003eIn F1, TTAB did not show significant influences on all gene expressions (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e(B)). In F2, it upregulated the expressions of \u003cem\u003eset-2\u003c/em\u003e, \u003cem\u003emet-2\u003c/em\u003e, \u003cem\u003emes-4\u003c/em\u003e, \u003cem\u003evab-1\u003c/em\u003e and \u003cem\u003egsa-1\u003c/em\u003e, and downregulated those of \u003cem\u003eceh-18\u003c/em\u003e. In F3, it upregulated the expressions of \u003cem\u003eset-2\u003c/em\u003e, \u003cem\u003emes-4\u003c/em\u003e, \u003cem\u003evab-1\u003c/em\u003e and \u003cem\u003egsa-1\u003c/em\u003e, and downregulated those of \u003cem\u003eceh-18\u003c/em\u003e. In F4, it upregulated expressions of \u003cem\u003eset-2\u003c/em\u003e, \u003cem\u003emes-4\u003c/em\u003e, \u003cem\u003evab-1\u003c/em\u003e and \u003cem\u003egsa-1\u003c/em\u003e, and downregulated those of \u003cem\u003emet-2\u003c/em\u003e and \u003cem\u003eceh-18\u003c/em\u003e. Collectively, the expression levels showed oscillation between upregulation and downregulation over generations. The IBR values were 2.33, 9.51, 2.86 and 2.60 in F1 to F4, respectively (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e(C)). The overall effects of TTAB on gene expressions were inhibitory in F1 and F4 and stimulatory in F2 and F3.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec13\" class=\"Section2\"\u003e \u003ch2\u003e3.4. Overall analysis on multi-generational effects of TTAC and TTAB\u003c/h2\u003e \u003cp\u003eIn the HCA results, the effects of TTAC on reproduction (including initial reproduction, total reproduction and reproduction duration) and reproduction-related proteins (including MSP, VAB-1, SPE9, SPE8, Vg and Vn) in F1 were closed clustered showing close connection (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003e(A)). Interestingly, the effects of TTAC on the gene expressions in F1 were more closely connected with the effects on reproduction in F2. Moreover, the effects on expressions of \u003cem\u003evab-1\u003c/em\u003e, \u003cem\u003eceh-18\u003c/em\u003e and \u003cem\u003egsa-1\u003c/em\u003e in F2 were also more closely connected with those on reproduction in F3. In addition, the effects on SPE-8, Vg, Vn and MAPK and those on the gene regulation in F3 were also more closely connected with the effects on reproduction in F4. Summing up, the effects of TTAC on parents were closely connected with those on the offspring. The effects of TTAB in parent generations were also closely related with those on the offspring (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003eB). Moreover, the effects of TTAC in F1 were even connected with those in F3 and F4, and the effects of TTAB in F1 and F2 also showed close connection with those in F4. That is to say, the close connection among indicators expanded over adjacent generations.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003e(Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003e around here)\u003c/p\u003e \u003cp\u003e(Tables\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e \u0026amp; \u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e around here)\u003c/p\u003e \u003cp style=\"margin:0in;text-align:justify;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-family:\"Times New Roman\",serif;color:blue;'\u003eTable 1\u003c/span\u003e\u003cspan style='font-family:\"Times New Roman\",serif;'\u003e\u0026nbsp;Pearson\u0026rsquo;s correlation between reproduction and biochemicals, between reproduction and gene expressions, and between biochemicals and gene expressions in the toxicities of tetradecyltrimethylammonium chloride (TTAC).\u003c/span\u003e\u003c/p\u003e\n\u003ctable style=\"width:100.0%;border-collapse:collapse;border:none;\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd style=\"width:6.6%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eTTAC\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.86%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eIR\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.9%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eTR\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.94%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eMSP\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.6%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eVAB-1\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eSPE-9\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eSPE-8\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eVg\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eVn\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.52%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eMAPK\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.96%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eset-2\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.96%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003emet-2\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003emes-4\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003evab-1\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eceh-18\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003egsa-1\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd style=\"width:6.6%;border:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:left;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eIR\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.86%;border:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e-\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.9%;border:none;padding:0in 5.4pt 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\u003c/td\u003e\n \u003ctd style=\"width:6.52%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.96%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.96%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.32%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e-\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e\n\u003cp style=\"margin:0in;text-align:left;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-family:\"Times New Roman\",serif;color:white;'\u003e*,\u003c/span\u003e\u003cspan style='font-family:\"Times New Roman\",serif;'\u003e\u0026nbsp;at 0.05 level.\u003c/span\u003e\u003c/p\u003e\n\u003cp style=\"margin:0in;text-align:left;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-family:\"Times New Roman\",serif;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n\u003cp style=\"margin:0in;text-align:justify;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-family:\"Times New Roman\",serif;color:blue;'\u003eTable 2\u003c/span\u003e\u003cspan style='font-family:\"Times New Roman\",serif;'\u003e\u0026nbsp;Pearson\u0026rsquo;s correlation between reproduction and biochemicals, between reproduction and gene expressions, and between biochemicals and gene expressions in the toxicities of tetradecyltrimethylammonium bromide (TTAB).\u003c/span\u003e\u003c/p\u003e\n\u003cdiv align=\"center\" style=\"margin:0in;text-align:justify;font-size:14px;font-family:DengXian;\"\u003e\n \u003ctable style=\"width:100.0%;border-collapse:collapse;border:none;\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd style=\"width:6.74%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eTTAB\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:3.84%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eIR\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.7%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eTR\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.44%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eMSP\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.74%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eVAB-1\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eSPE-9\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eSPE-8\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eVg\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eVn\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.66%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eMAPK\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eset-2\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003emet-2\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003emes-4\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003evab-1\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eceh-18\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.72%;border-top:solid windowtext 1.0pt;border-left:none;border-bottom:solid windowtext 1.0pt;border-right:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:center;font-size:14px;font-family:DengXian;\"\u003e\u003cem\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003egsa-1\u003c/span\u003e\u003c/em\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd style=\"width:6.74%;border:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:left;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003eIR\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:3.84%;border:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e-\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.7%;border:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e0.846\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.44%;border:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:red;'\u003e0.968*\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.74%;border:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:red;'\u003e0.990*\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:red;'\u003e0.980*\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:red;'\u003e0.972*\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border:none;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:red;'\u003e0.976*\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border:none;padding:0in 5.4pt 0in 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style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:6.46%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e\u0026nbsp;\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width:5.72%;border:none;border-bottom:solid windowtext 1.0pt;padding:0in 5.4pt 0in 5.4pt;height:15.45pt;\"\u003e\n \u003cp style=\"margin:0in;text-align:right;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-size:9px;font-family:\"Times New Roman\",serif;color:black;'\u003e-\u003c/span\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n \u003c/table\u003e\n\u003c/div\u003e\n\u003cp style=\"margin:0in;text-align:left;font-size:14px;font-family:DengXian;\"\u003e\u003cspan style='font-family:\"Times New Roman\",serif;color:white;'\u003e*,\u003c/span\u003e\u003cspan style='font-family:\"Times New Roman\",serif;'\u003e\u0026nbsp;at 0.05 level.\u003c/span\u003e\u003c/p\u003e \u003cp\u003eIn the Pearson\u0026rsquo;s correlation results, the biochemical effects of TTAC (e.g., on MSP, VAB-1, SPE-9, SPE-8, Vg, Vn and MAPK) were well correlated with themselves and also occasionally with those on \u003cem\u003emes-4\u003c/em\u003e and \u003cem\u003evab-1\u003c/em\u003e expressions (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Meanwhile, the biochemical effects of TTAB showed correlations with themselves, but also with reproduction, and commonly with those on \u003cem\u003evab-1\u003c/em\u003e and \u003cem\u003eceh-18\u003c/em\u003e expressions (Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). The results demonstrated the connection among indicators and also the differences between TTAC and TTAB.\u003c/p\u003e \u003c/div\u003e"},{"header":"4. Discussion","content":"\u003cdiv id=\"Sec15\" class=\"Section2\"\u003e \u003ch2\u003e4.1. Multi-generational reproductive effects of TTAC and TTAB\u003c/h2\u003e \u003cp\u003eThe multigenerational reproductive effects showed oscillation between stimulation and inhibition over generations. The similar oscillations were also observed in multigenerational effects of imidazole-based ILs (Yue et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2021\u003c/span\u003e, Zhang and Feng \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2022\u003c/span\u003e, Wang et al. \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2023\u003c/span\u003e), pyridine-based ILs (Shi et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2021\u003c/span\u003e, Zhang et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2022\u003c/span\u003e), and antibiotics (e.g., sulfamethoxazole, enrofloxacin, ofloxacin and norfloxacin) (Li et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2020\u003c/span\u003e, Zhang et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2022\u003c/span\u003e, Zheng et al. \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Offspring in uterus prepared similar responses to their maternal experiences via fetal reprogramming for better adaptation to the environment (Li et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). However, such preparation does not guarantee the matching with the actual requirement of the offspring. Accordingly, the outcomes in the offspring can be stimulation, inhibition and even non-significant influences, therefore explaining the oscillatory changes over generations. More investigation is needed to establish models for predicting multigenerational effects in the future.\u003c/p\u003e \u003cp\u003eSimilar to the effects of TTAB, pyridine-based ILs and antibiotics also caused consistent effects on the initial and total reproduction of nematodes (Shi et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2021\u003c/span\u003e, Zhang et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2022\u003c/span\u003e, Zhang et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Meanwhile, the effects of TTAC in F2 showed inconsistence between effects on the initial reproduction and those on the total reproduction with compensation from longer reproduction duration. Notably, animals in the actual environment would reproduce as early as possible to ensure the population growth (Yu et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), and delayed reproduction with longer reproduction duration would be unrealistic due to accidental death or predation. Therefore, with or without compensation by longer reproduction duration, the reproductive toxicities of TTAC and TTAB would significantly influence the population growth and their ecological risks should be seriously considered in their application.\u003c/p\u003e \u003cp\u003eIt was known that QACs are cationic surfactants, and therefore most investigations were studied on cationic toxicity on various organisms (Luz et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2020\u003c/span\u003e, Suthar et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). The present study showed the different results of TTAC and TTAB, which showed the influences of anions on the reproductive toxicities. In future studies, the anionic influences should be considered in the QACs toxicities to more accurate evaluation on their ecological risks.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec16\" class=\"Section2\"\u003e \u003ch2\u003e4.2. Mechanisms of the multi-generational reproductive effects\u003c/h2\u003e \u003cp\u003eIn the reproductive processes, the spermiogenesis is triggered via SPE8 and the sperm movement is promoted by Vg (Han et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2010\u003c/span\u003e, Ellis and Stanfield \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2014\u003c/span\u003e), the oocyte meiotic maturation is regulated by MAPK activation and binding of MSP to VAB-1 (Govindan et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2006\u003c/span\u003e, Yamamoto et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2006\u003c/span\u003e), and the sperm-oocyte interactions and fertilization are ensured with SPE9 (Marcello and Singson \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). At the molecular level, the expressions of \u003cem\u003evab-1\u003c/em\u003e, \u003cem\u003eceh-18\u003c/em\u003e, \u003cem\u003eset-2\u003c/em\u003e, \u003cem\u003emet-2\u003c/em\u003e and \u003cem\u003emes-4\u003c/em\u003e regulate the oocyte meiotic maturation, gonadal sheath cells and germline genome integrity (Govindan et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2006\u003c/span\u003e, Yamamoto et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2006\u003c/span\u003e, Gonz\u0026aacute;lez-Aguilera et al. \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2013\u003c/span\u003e, Herbette et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). The effects of TTAB on the reproduction showed positive correlations with those on the aforementioned biochemicals and those on the expressions of the aforementioned genes. Moreover, the effects of TTAB on the gene expressions (e.g., \u003cem\u003evab-1\u003c/em\u003e and \u003cem\u003eceh-18\u003c/em\u003e) were also positively correlated with those on the biochemicals including MSP, SPE-9, Vg and MAPK. The correlation demonstrated that the reproductive toxicities of TTAB were well related with its impacts on the whole reproductive processes including oocyte meiosis, gonadal support and germline development. However, the effects of TTAC did not show such correlations as those in the results of TTAB, and therefore the differences supported the anionic influences on QACs toxicities as well.\u003c/p\u003e \u003cp\u003eNotably, the effects of both TTAC and TTAB in parents were connected with those in the offspring. The connection was also observed in the multi-generational effects of antibiotics and ILs (Zhang et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2022\u003c/span\u003e, Wang et al. \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Such connection supported that reproductive processes provided one essential tie to combine health over generations. Especially, the expressions of \u003cem\u003eset-2\u003c/em\u003e, \u003cem\u003emet-2\u003c/em\u003e and \u003cem\u003emes-4\u003c/em\u003e involved histone methylation (e.g., at H3K4, H3K9 and H3K36 sites) to preserve germline genome integrity and normal development (Gonz\u0026aacute;lez-Aguilera et al. \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2013\u003c/span\u003e, Herbette et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Therefore, the connection in the effects between generations also supported the involvement of epigenetic modulation on the responses of offspring to the maternal experience (Yue et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Therefore, further studies are still needed to explore the epigenetic mechanisms underlying the multigenerational consequences of pollutants.\u003c/p\u003e \u003c/div\u003e"},{"header":"5. Conclusion","content":"\u003cp\u003eBoth TTAC and TTAB caused reproductive toxicities with changes over generations. The reproductive effects of TTAC showed oscillation between stimulation and inhibition over generations. The toxicities of TTAB on initial reproduction can be compensated by reproduction duration. Biochemical and gene expression results showed that TTAC and TTAB impacted oocyte meiosis, gonadal support and germline development. Moreover, the reproductive toxicities also involved epigenetic regulations on histone methylation. In addition, the results also demonstrated the anionic influences on the toxicities of QACs.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eEthical Approval:\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent to Participate and Publish:\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll authors agreed with authorship and the content, and approved to submit the present version to be published.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthors Contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eFormal analysis, investigation and writing original draft were performed by Jing Zhang. Experiment performance and data curation were performed by Ruoqi Ding. Supervision, project administration and funding acquisition were performed by Zhenyang Yu.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis work was supported by National Key Research and Development Program of China (2021YFC3200803). The authors are sincerely grateful for their financial support.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting Interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors have no relevant financial interests to disclose.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eAbe H, Kishimura H (2022) CO\u003csub\u003e2\u003c/sub\u003e-driven surface reconstruction in quaternary ammonium ionic liquid-propanol solutions. 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Sci Total Environ 804:150250\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Multigenerational effect, Oocyte meiosis, Gonadal support, Germline development, Anionic influence","lastPublishedDoi":"10.21203/rs.3.rs-3528355/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3528355/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eQuaternary ammonium compounds (QACs) become emerging pollutants and their toxicities earn increasing attentions. So far, their reproductive toxicities were poorly investigated, and their effects over generations were even less explored. In the present study, reproductive toxicities of two QACs, i.e., tetradecyltrimethylammonium chloride (TTAC) and tetradecyltrimethylammonium bromide (TTAB) were studied on \u003cem\u003eCaenorhabditis elegans\u003c/em\u003e with a consecutive exposure over four generations (from F1 to F4). The effects of TTAC on total reproduction showed stimulation and inhibition which oscillated from F1 to F4, and such oscillation was also observed in the effects on initial reproduction. The effects of TTAB on the total reproduction commonly showed stimulation over generations. The greatest stimulation was in F2, and it was accompanied with inhibition on the initial reproduction but stimulation on the reproduction duration. Further mechanisms exploration demonstrated that both TTAC and TTAB significantly disturbed the levels of SPE8, SPE9, Vg, MSP and VAB-1 and the expressions of \u003cem\u003evab-1\u003c/em\u003e, \u003cem\u003eceh-18\u003c/em\u003e, \u003cem\u003eset-2\u003c/em\u003e, \u003cem\u003emet-2\u003c/em\u003e and \u003cem\u003emes-4\u003c/em\u003e over generations. Such disturbances demonstrated that both QACs impacted the reproductive processes in multiple aspects including oocyte meiosis, gonadal support and germline development. Further analysis also showed that the effects of both TTAC and TTAB in parents were connected with those in the offspring, which highlighted the conjunctive roles of reproduction in responses of adjacent generations. In addition, the differences the effects of TTAC and TTAB also demonstrated the anionic influences on the QACs\u0026rsquo; toxicities.\u003c/p\u003e","manuscriptTitle":"Reproductive toxicities of tetradecyltrimethylammonium chloride and tetradecyltrimethylammonium bromide on Caenorhabditis elegans over four consecutive generations","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2023-11-02 19:32:20","doi":"10.21203/rs.3.rs-3528355/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"b0c52126-784a-4261-a8ea-a5b79e1768bd","owner":[],"postedDate":"November 2nd, 2023","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2023-11-24T21:22:00+00:00","versionOfRecord":[],"versionCreatedAt":"2023-11-02 19:32:20","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-3528355","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3528355","identity":"rs-3528355","version":["v1"]},"buildId":"pf3fE39SIOqb-0xH_OWvX","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}