Isolation and complete genome sequence of Citrobacter bacteriophage Ursula

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Golomidova" }, { "@type": "Person", "name": "E.E. Kulikov" }, { "@type": "Person", "name": "A.D. Efimov" }, { "@type": "Person", "name": "I.S. Belalov" }, { "@type": "Person", "name": "A.S. Kuznetsov" }, { "@type": "Person", "name": "A.V. Letarov" }, { "@type": "Person", "name": "L.I. Popova" } ], "publisher": { "@type": "Organization", "name": "F1000Research", "logo": { "@type": "ImageObject", "url": "https://f1000research.com/img/AMP/F1000Research_image.png", "height": 480, "width": 60 } }, "image": { "@type": "ImageObject", "url": "https://f1000research.com/img/AMP/F1000Research_image.png", "height": 1200, "width": 150 }, "description": "The emergence of antibiotic resistance among bacterial pathogens poses a significant threat to aquaculture and public health. This study presents the characterization of a novel bacteriophage, designated as Ursula, specifically targeting Citrobacter, a prominent pathogen affecting fish populations. We isolated Ursula from aquatic environments during a search for novel phages active against fish pathogens, and conducted a comprehensive analysis of its morphological, genomic, and lytic properties. Transmission electron microscopy revealed that Ursula has a myovirus morphology, being a rather large T4-like phage. Genomic sequencing identified a double-stranded linear DNA genome of approximately 183 kb, containing unique genes associated with lytic activity and host recognition. This phage is related to other T4-like Citrobacter phages, being a new species." } { "@context": "http://schema.org", "@type": "BreadcrumbList", "itemListElement": [ { "@type": "ListItem", "position": "1", "item": { "@id": "https://f1000research.com/", "name": "Home" } }, { "@type": "ListItem", "position": "2", "item": { "@id": "https://f1000research.com/browse/articles", "name": "Browse" } }, { "@type": "ListItem", "position": "3", "item": { "@id": "https://f1000research.com/articles/14-86/v1", "name": "Isolation and complete genome sequence of Citrobacter bacteriophage..." } } ] } Home Browse Isolation and complete genome sequence of Citrobacter bacteriophage... ALL Metrics - Views Downloads Get PDF Get XML Cite How to cite this article Golomidova AK, Kulikov EE, Efimov AD et al. Isolation and complete genome sequence of Citrobacter bacteriophage Ursula [version 1; peer review: 1 approved, 1 approved with reservations] . F1000Research 2025, 14 :86 ( https://doi.org/10.12688/f1000research.159170.1 ) NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article. Close Copy Citation Details Export Export Citation Sciwheel EndNote Ref. Manager Bibtex ProCite Sente EXPORT Select a format first Track Share ▬ ✚ Genome Note Isolation and complete genome sequence of Citrobacter bacteriophage Ursula [version 1; peer review: 1 approved, 1 approved with reservations] A.K. Golomidova 1 , E.E. Kulikov https://orcid.org/0000-0002-9101-1543 1 , A.D. Efimov 1 , [...] I.S. Belalov 1 , A.S. Kuznetsov https://orcid.org/0000-0002-8016-3760 1 , A.V. Letarov 1 , L.I. Popova 2 A.K. Golomidova 1 , E.E. Kulikov https://orcid.org/0000-0002-9101-1543 1 , [...] A.D. Efimov 1 , I.S. Belalov 1 , A.S. Kuznetsov https://orcid.org/0000-0002-8016-3760 1 , A.V. Letarov 1 , L.I. Popova 2 PUBLISHED 15 Jan 2025 Author details Author details 1 Winogradsky Institute of Microbiology, Research Center “Fundamentals of Biotechnology” RAS, Moscow, Russian Federation 2 Department of Biology, Shenzhen MSU-BIT University, Shenzhen, Guangdong, China A.K. Golomidova Roles: Data Curation, Formal Analysis, Investigation, Methodology, Visualization, Writing – Original Draft Preparation E.E. Kulikov Roles: Data Curation, Formal Analysis, Investigation, Methodology, Visualization, Writing – Original Draft Preparation, Writing – Review & Editing A.D. Efimov Roles: Data Curation, Formal Analysis, Investigation, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing I.S. Belalov Roles: Data Curation, Formal Analysis, Writing – Original Draft Preparation, Writing – Review & Editing A.S. Kuznetsov Roles: Data Curation, Formal Analysis, Investigation, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing A.V. Letarov Roles: Conceptualization, Formal Analysis, Funding Acquisition, Project Administration, Resources, Supervision, Writing – Review & Editing L.I. Popova Roles: Writing – Review & Editing OPEN PEER REVIEW DETAILS REVIEWER STATUS This article is included in the Genomics and Genetics gateway. Abstract The emergence of antibiotic resistance among bacterial pathogens poses a significant threat to aquaculture and public health. This study presents the characterization of a novel bacteriophage, designated as Ursula, specifically targeting Citrobacter , a prominent pathogen affecting fish populations. We isolated Ursula from aquatic environments during a search for novel phages active against fish pathogens, and conducted a comprehensive analysis of its morphological, genomic, and lytic properties. Transmission electron microscopy revealed that Ursula has a myovirus morphology, being a rather large T4-like phage. Genomic sequencing identified a double-stranded linear DNA genome of approximately 183 kb, containing unique genes associated with lytic activity and host recognition. This phage is related to other T4-like Citrobacter phages, being a new species. READ ALL READ LESS Keywords bacteriophage, Citrobacter spp., T4-like bacteriophage, Claries gariepinus, aquaculture, phage therapy Corresponding Author(s) A.V. Letarov ( [email protected] ) L.I. Popova ( [email protected] ) Close Corresponding authors: A.V. Letarov, L.I. Popova Competing interests: No competing interests were disclosed. Grant information: This work was supported by the Ministry of Science and Higher Education of the Russian Federation in accordance with agreement #075-15-2022-318 dated April 20, 2022, on the provision of a grant in the form of subsidies from the federal budget of the Russian Federation for the implementation of the state support for the creation and development of a world-class scientific center “Agrotechnologies for the Future”. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Copyright: © 2025 Golomidova AK et al . This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. How to cite: Golomidova AK, Kulikov EE, Efimov AD et al. Isolation and complete genome sequence of Citrobacter bacteriophage Ursula [version 1; peer review: 1 approved, 1 approved with reservations] . F1000Research 2025, 14 :86 ( https://doi.org/10.12688/f1000research.159170.1 ) First published: 15 Jan 2025, 14 :86 ( https://doi.org/10.12688/f1000research.159170.1 ) Latest published: 15 Jan 2025, 14 :86 ( https://doi.org/10.12688/f1000research.159170.1 ) Introduction Aquaculture gained popularity as a main production way of fish in many countries. 1 Citrobacter bacteria, particularly Citrobacter freundii , have emerged as significant pathogens in aquaculture, leading to a range of diseases that affect various fish species. 2 – 4 These opportunistic pathogens can cause infections characterized by symptoms such as hemorrhaging, ulcers, and systemic disease, which ultimately compromise fish health and survival. The presence of Citrobacter in aquaculture systems is often exacerbated by environmental stressors, poor water quality, and overcrowding, creating conditions conducive to outbreaks. 5 As these bacteria proliferate, they can lead to high mortality rates among infected fish, resulting in substantial economic losses for aquaculture operations. The costs associated with treatment, increased feed conversion ratios due to stress, and the loss of marketable fish can severely impact the profitability of fish farms. Furthermore, the rise of antibiotic resistance among Citrobacter strains complicates treatment options, necessitating a shift towards alternative management strategies. Consequently, addressing Citrobacter -induced diseases is crucial not only for maintaining fish health but also for ensuring the sustainability and economic viability of the aquaculture industry. New bacteriophages as economically viable tools for Citrobacter biocontrol are highly demanded by industry. Here, we present an isolation and genome analysis of a novel bacteriophage infecting ichtyopathogenic Citrobacter strains, potentially attractive for phage prophylaxis and therapy in aquaculture. Methods Phage isolation and cultivation The bacteriophage Ursula was isolated during efforts to sample diverse bacteriophages from aquatic environments, specifically targeting Citrobacter spp. strains known to cause infections in African sharptooth catfish ( Clarias gariepinus ) in Russian aquaculture facilities. On September 14, 2021, a water sample was collected from the Norishka Stream in Mikhailovsky Park, Moscow, Russia. To isolate the phage, the following enrichment process was used: Initial Preparation: 0.5 liters of unsterilized water were added to a 2-liter sterile plastic bottle. Medium Addition: 50 milliliters of sterile 10× LB medium were mixed into the water (the 1× medium contains: 10 g Bacto Tryptone (Amresco, Am-J859-0.25), 5 g yeast extract (Amresco, J850-500G), 10 g NaCl (Amresco, J869-500G), and distilled water up to 1 liter). Bacterial Culture Introduction: 0.5 milliliters of an overnight liquid culture of Citrobacter spp. CF69 strain were added to the enriched mixture. Incubation: The enriched culture was incubated at 37°C with shaking at 240 rpm. After incubation, 1 milliliter of the enriched culture was centrifuged at 12,000 rpm using a tabletop microcentrifuge. The resulting supernatant was filtered through a 0.22-micron syringe membrane filter (Millex-GP, Millipore) and then plated onto a lawn of Citrobacter spp. CF69 strain using the standard double-layer method. 6 Phage plaques were formed after an overnight incubation at 37 °C. The phage was purified using two consecutive single-plaque isolations. To obtain a high-titer lysate, five 90 mm Petri dishes were filled with solid LB medium (15 g of Bacto Agar (BD214030, BD Difco) per 1 l). Without drying the plates, they were overlaid with 5 ml of soft LB agar (6 g Bacto Agar (BD214030, BD Difco) per 1 l) per plate. Soft agar was inoculated with 300 μl of a 4h log-phase liquid culture of the host strain and approximately 1×10 5 PFU of the phage per plate. The plates were incubated overnight at 37 °C. To extract the phage, the soft agar layer was gently destroyed with a spreader, transferred into 50 ml plastic centrifuge tubes, and layered with 10 ml of LB medium. Chloroform (Fisher Scientific, C298-4) (100 μL) was added to each tube, followed by vigorous vortexing for 1 min, and allowed to stand at room temperature for 2 h. After incubation, the agar fragments and bacterial cells were pelleted by centrifugation at 10 000 g for 5 min, and the supernatant was collected and centrifuged again under the same conditions. The phage clarified stock was pelleted in Beckman Ti45 angle rotor (75 000 g, 1 h, 20 °C), resuspended in saline and layered on sucrose step gradient in 5 ml tubes (60%-50%-40%-30%-20% sucrose w/w, 800 μL each). Tubes were centrifuged in Beckman SW55Ti swing bucket rotor (75 000 g, 1 h, 20 °C) and a compact opalescent band between 40% and 50% layers was removed, corresponding to intact phage particles. 7 The purified phage sample was used for DNA extraction and transmission electron microscopy (TEM), as previously described. 8 Briefly, a drop of purified phage preparation was adsorbed on a carbon-coated TEM support grids, negatively contrasted with 1% uranyl acetate in methanol (Reachim, USSR), dried and studied in Jeol JEM-1400Flash electron microscope Jeol Ltd., Japan). DNA extraction, sequencing, assembly and annotation To extract phage DNA, the high-titer phage stock (about 10 11 pfu/ml) was incubated with DNase (Thermo Scientific, EN0521) at a concentration of 0.01 mg/ml for 30 minutes at room temperature to destroy extraneous DNA traces. Subsequently, the phage particles were collected via ultracentrifugation in an angle rotor at room temperature (Beckman 45Ti, 1 hour, 75,000 g). Genomic DNA was extracted from pelleted bacteriophage using CTAB (cetyltrimethylammonium bromide) extraction as previously described. 9 The quality and quantity of the DNA were assessed using agarose gel electrophoresis and a Qubit dsDNA HS fluorometric assay (Qubit, USA). Libraries of phage genomic DNA were prepared and sequenced using an Ion Proton sequencer (Applied Biosystems, Foster City, CA, USA) with standard reagents according to the manufacturer’s protocol. Raw sequencing reads were pooled and filtered using the error-correction tool Pollux (RRID:SCR_026200). Final contigs were assembled using Newbler version 3.0 (RRID:SCR_011916) (Roche Diagnostics, USA), yielding a single contig representing the phage genome, consisting of 183,411 base pairs with an average coverage of 200 bp. Annotation was performed using Prokka 10 (RRID:SCR_014732) and Pharokka 11 (RRID:SCR_026017)-Phold (RRID:SCR_026016)-Phynteny (RRID:SCR_026015) pipeline with subsequent manual curation. Potential open reading frames (ORFs) were initially detected using GeneMarkS ( https://genemark.bme.gatech.edu/genemarks.cgi ) (RRID:SCR_011930) and subsequently analyzed using HMMER 12 (RRID:SCR_005305), HHPRED 13 (RRID:SCR_010276) (MPI Bioinformatics Toolkit), NCBI BLAST 14 (RRID:SCR_004870), and tRNAscan-SE 15 (RRID:SCR_008637). Results The bacteriophage Ursula was found to be a relatively large myovirus with an elongated head, suggesting it belongs to T4 phage group ( Figure 1 ). The genome consisted of 183 411 b.p. and encoded 343 ORF. Figure 1. Morphology of the Ursula phage virion. Numerous proteins constituting a contractile phage tail were identified, consistent with the TEM examination results. The Ursula genome also contains genes for an efficient host defense overtake and metabolism switching, including highly cytotoxic Ndd-like nucleoid disruption protein (Ursula_0014), DenB-like DNA endonuclease IV capable of destroying host DNA replication on dC residues. (Ursula_ 0017), small protein inhibitor of MrcBC restriction participating in host takeover (Ursula_0004), duplicated cef modifier of suppressor tRNAs (Ursula_0033, Ursula_0044), a number of genes involved in DNA replication and modification (glucosyltransferases, thymidylate synthase, anaerobic NrdD-like ribonucleotide reductase, NUDIX hydrolase, 2-oxoglutarate-dependent oxygenase, rNDP reductase, DHFR etc.) as well as cytotoxic proteins and recombination mediators. Twelve tRNA genes were detected. Phage Ursula lacks any genomic indicators that could be linked to a lysogenic lifestyle or virulence factors of this phage. A BLASTN search against the NCBI Nucleotide collection produced a number of relevant hits with a good homology, suggesting placement of this phage to Merlin (NCBI NC_028857.1) and Moon (NCBI NC_027331.1), cluster of T4-like Citrobacter spp. bacteriophages, although their genomes are about 6-7% shorter, with gaps diffused along the entire genome. Therefore, we conclude that phage Ursula represents a novel species in T4-like group of Citrobacter spp. bacteriophages, and numerous enzymes and regulatory proteins encoded in its genome make it a good candidate for phage therapy applications. Ethical considerations No animal research was conducted in this work. Ethical approval and consent were not required. Data availability Underlying data NCBI GenBank: Genomic DNA sequence of Ursula bacteriophage. Accession number PQ589834; https://www.ncbi.nlm.nih.gov/nuccore/PQ589834 (nucleotide: PQ589834). Figshare: Morphology of the Ursula phage virion, Doi: https://doi.org/10.6084/m9.figshare.28092209.v1 . 16 This project contains the following underlying data: • Figure1.png (0070E4AF-3A7F-4BDE-B30A-428EF2BD17EB.png) Figshare: Ursula bacteriophage genome sequence in GenBank format, Doi: https://doi.org/10.6084/m9.figshare.28092218.v1 . 17 This project contains the following underlying data: • Ursula.gbk Data are available under the terms of the Creative Commons Attribution 4.0 International license (CC-BY 4.0). Software availability statement All software used in this work is freely available online using respective RRIDs supplied in text. References 1. Bondad-Reantaso MG, MacKinnon B, Karunasagar I, et al. : Review of alternatives to antibiotic use in aquaculture. Rev. Aquac. 2023; 15 (4): 1421–1451. Publisher Full Text 2. Chen A, Qian Q, Cai X, et al. : Pathogenicity of Citrobacter freundii Causing Mass Mortalities of Macrobrachium rosenbergii and Its Induced Host Immune Response. Microorganisms. 2024 Oct 17; 12 (10). Epub 2024/10/26. PubMed Abstract | Publisher Full Text | Free Full Text 3. Laltlanmawia C, Saha H, Ghosh L, et al. : Identification and analysis of pathogenic bacteria causing outbreaks in Indian major carp aquaculture of Tripura. J. Aquat. Anim. Health. 2023 Dec; 35 (4): 263–279. PubMed Abstract | Publisher Full Text 4. Gong C, Guo M, Lou J, et al. : Identification and characterization of a highly virulent Citrobacter freundii isolate and its activation on immune responses in largemouth bass (Micropterus salmoides). Fish Shellfish Immunol. 2023 Dec; 143 : 109224. Epub 2023/11/14. PubMed Abstract | Publisher Full Text 5. Salgueiro V, Manageiro V, Rosado T, et al. : Snapshot of resistome, virulome and mobilome in aquaculture. Sci. Total Environ. 2023 Dec 20; 905 : 166351. Epub 2023/08/22. PubMed Abstract | Publisher Full Text 6. Letarov AV, Kulikov EE: Determination of the bacteriophage host range: culture-based approach. Methods Mol. Biol. 2018; 1693 : 75–84. PubMed Abstract | Publisher Full Text 7. Kornienko M, Kuptsov N, Gorodnichev R, et al. : Contribution of Podoviridae and Myoviridae bacteriophages to the effectiveness of anti-staphylococcal therapeutic cocktails. Sci. Rep. 2020 Oct 29; 10 (1): 18612. Epub 2020/10/31. PubMed Abstract | Publisher Full Text | Free Full Text 8. Efimov A, Kulikov E, Golomidova A, et al. : Isolation and sequencing of three RB49-like bacteriophages infecting O antigen-producing E. coli strains. F1000Res. 2021; 10 : 1113. Publisher Full Text 9. Kulikov E, Golomidova A, Babenko V, et al. : A simple method for extraction of the horse feces virome DNA, suitable for oxford nanopore sequencing. Microbiology. 2020; 89 : 246–249. Publisher Full Text 10. Seemann T: Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014 Jul 15; 30 (14): 2068–2069. PubMed Abstract | Publisher Full Text 11. Bouras G, Nepal R, Houtak G, et al. : Pharokka: a fast scalable bacteriophage annotation tool. Bioinformatics. 2023 Jan 1; 39 (1). Epub 2022/12/02. PubMed Abstract | Publisher Full Text | Free Full Text 12. Eddy SR: Accelerated Profile HMM Searches. PLoS Comput. Biol. 2011 Oct; 7 (10): e1002195. Epub 2011/11/01. PubMed Abstract | Publisher Full Text | Free Full Text 13. Soding J, Biegert A, Lupas AN: The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 2005 Jul 1; 33 (Web Server issue): W244–W248. PubMed Abstract | Publisher Full Text | Free Full Text 14. Altschul SF, Gish W, Miller W, et al. : Basic local alignment search tool. J. Mol. Biol. 1990 Oct 5; 215 (3): 403–410. PubMed Abstract | Publisher Full Text 15. Chan PP, Lin BY, Mak AJ, et al. : tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes. Nucleic Acids Res. 2021 Sep 20; 49 (16): 9077–9096. PubMed Abstract | Publisher Full Text | Free Full Text 16. Kulikov E: Morphology of the Ursula phage virion. figshare. 2024 [cited 2025 Jan 6]. Reference Source 17. Kulikov E: Ursula bacteriophage genome sequence in Genbank format. figshare. 2024 [cited 2025 Jan 6]. Reference Source Comments on this article Comments (0) Version 1 VERSION 1 PUBLISHED 15 Jan 2025 ADD YOUR COMMENT Comment Author details Author details 1 Winogradsky Institute of Microbiology, Research Center “Fundamentals of Biotechnology” RAS, Moscow, Russian Federation 2 Department of Biology, Shenzhen MSU-BIT University, Shenzhen, Guangdong, China A.K. Golomidova Roles: Data Curation, Formal Analysis, Investigation, Methodology, Visualization, Writing – Original Draft Preparation E.E. Kulikov Roles: Data Curation, Formal Analysis, Investigation, Methodology, Visualization, Writing – Original Draft Preparation, Writing – Review & Editing A.D. Efimov Roles: Data Curation, Formal Analysis, Investigation, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing I.S. Belalov Roles: Data Curation, Formal Analysis, Writing – Original Draft Preparation, Writing – Review & Editing A.S. Kuznetsov Roles: Data Curation, Formal Analysis, Investigation, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing A.V. Letarov Roles: Conceptualization, Formal Analysis, Funding Acquisition, Project Administration, Resources, Supervision, Writing – Review & Editing L.I. Popova Roles: Writing – Review & Editing Competing interests No competing interests were disclosed. Grant information This work was supported by the Ministry of Science and Higher Education of the Russian Federation in accordance with agreement #075-15-2022-318 dated April 20, 2022, on the provision of a grant in the form of subsidies from the federal budget of the Russian Federation for the implementation of the state support for the creation and development of a world-class scientific center “Agrotechnologies for the Future”. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Article Versions (1) version 1 Published: 15 Jan 2025, 14:86 https://doi.org/10.12688/f1000research.159170.1 Copyright © 2025 Golomidova AK et al . This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Download Export To Sciwheel Bibtex EndNote ProCite Ref. Manager (RIS) Sente metrics Views Downloads F1000Research - - PubMed Central info_outline Data from PMC are received and updated monthly. - - Citations open_in_new 0 open_in_new 0 open_in_new SEE MORE DETAILS CITE how to cite this article Golomidova AK, Kulikov EE, Efimov AD et al. Isolation and complete genome sequence of Citrobacter bacteriophage Ursula [version 1; peer review: 1 approved, 1 approved with reservations] . F1000Research 2025, 14 :86 ( https://doi.org/10.12688/f1000research.159170.1 ) NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS track receive updates on this article Track an article to receive email alerts on any updates to this article. TRACK THIS ARTICLE Share Open Peer Review Current Reviewer Status: ? Key to Reviewer Statuses VIEW HIDE Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions Version 1 VERSION 1 PUBLISHED 15 Jan 2025 Views 0 Cite How to cite this report: Chitboonthavisuk C. Reviewer Report For: Isolation and complete genome sequence of Citrobacter bacteriophage Ursula [version 1; peer review: 1 approved, 1 approved with reservations] . F1000Research 2025, 14 :86 ( https://doi.org/10.5256/f1000research.174859.r433417 ) The direct URL for this report is: https://f1000research.com/articles/14-86/v1#referee-response-433417 NOTE: it is important to ensure the information in square brackets after the title is included in this citation. Close Copy Citation Details Reviewer Report 30 Dec 2025 Chutikarn Chitboonthavisuk , University of Wisconsin-Madison, Madison, Wisconsin, USA Approved with Reservations VIEWS 0 https://doi.org/10.5256/f1000research.174859.r433417 Summary The manuscript describes the isolation and characterization of “Ursula” phage, a novel phage targeting Citrobacter strains, isolated from an aquatic environment. Given the rising of antibiotic resistance in pathogens, including Citrobacter freundii , emerged in aquaculture industry and the ... Continue reading READ ALL Summary The manuscript describes the isolation and characterization of “Ursula” phage, a novel phage targeting Citrobacter strains, isolated from an aquatic environment. Given the rising of antibiotic resistance in pathogens, including Citrobacter freundii , emerged in aquaculture industry and the high cost in disease treatment, the isolation of new phage holds potential economic value for the industry. Overall, the authors presented their works on isolating a novel bacteriophage, genome sequencing, and morphology characterization. While the characterization and sequencing are described, this manuscript needs additional information to support their classification and their statement of this phage for further application in an aquaculture system. Here are several major and minor points that need clarification. The major points that may help the authors improve their work. 1. Genomic analysis and novelty of the phage discovery The statement “BLASTn search against the NCBI Nucleotide collection produced a number of relevant hits with a good homology” is vague. The authors should provide quantitative metrics, such as average nucleotide identity (ANI) or total similarity, to clearly define the relationship and similarity between Ursula and the other phages, Merlin and Moon. Schematic of genomic comparison can be provided. The current name used, Ursula, was previously named for actinophage, although that actinophage has been renamed to Trident. It might be confusing to readers. Authors could perform phylogenetic analyses using conserved markers may help improving the classification. 2. Authors claim the discovery of a novel phage and characterization of this phage. In addition, authors suggest this phage as a candidate for biocontrol; however, the authors did not provide a thorough characterization and their capability of the phage as a biocontrol candidate. The authors did not provide a basic growth characterization, including plaque morphology, stability, host range determination, and the burst size of this novel phage. A complete basic characterization may help improve the report and can be informative for further study. The figure of phage morphology is low in quality, obstructed by other components/debris. 3. The authors stated that this new phage is an economically viable tool for Citrobacter biocontrol and is highly demanded by the industry in their introduction; however, the authors did not provide reference information about the phages or antibiotic treatments currently used, the demand of acquiring new phages, and the comparison across these methods to better claim that this phage tool is economically efficient. The authors did not provide a host range of this novel phage, especially Citrobacter strains that cause diseases or are found in outbreaks in the aquaculture industry, which could help support the economic aspects and applications of this phage. However, this point regarding the economic aspects of this discovery might be out of the scope of this manuscript. Here are minor points. This includes clarifications, formatting, and consistency. In the method section, italicize Citrobacter spp., provide a reference or resource of Citrobacter strain used in this study. Italicize in the paragraph “After incubation,…. A lawn of Citrobacter spp. CF69 strain In the incubation step, authors stated “enriched culture was centrifuged at 12,000 rpm using a tabletop microcentrifuge”, without providing the model and diameter of the microcentrifuge. Additionally, authors use xg across the paper; ensure to keep the units consistent. During the extraction step, the soft agar layer and chloroform mix were pelleted at 10,000 xg for 5 min. Is this amount of time enough with this volume to completely separate the mixtures? Authors used both “h” and “hour”, both “µl” and “µL”, both “ml” and “mL”, both “pfu” and “PFU”, “min” and “minutes” please keep it consistent. Typo of parentheses in “…. dried and studied in Jeol JEM-1400Flash electron microscope Jeol Ltd., Japan).” Reference of chemicals is inconsistent, authors used (“ID number”, “brand”) and (“brand”, “ID number”). Space in the result section, (Ursula_ 0017), can be removed. Authors stated at the end of result section that “ numerous enzymes and regulatory proteins encoded in its genome make it a good candidate for phage therapy applications” may need more support information. Regarding the details of the sequencing and extraction, software used, and materials provided for the reproducibility, additional detail would help improve the reproducibility of these processes. This includes small detail, such as the volume of phage used, modification needed for this particular types of samples, details to expand more on the standard reagent/manufacturer’s protocol, and the availability of scripts used for sequencing analyses. This manuscript is suitable for Genome Note. Major points, including a thorough characterization of the phage, both phenotype and physiochemistry, and host range determination, could help improve this discovery for further application, and genomic comparison would clarify the novelty of this phage discovery. Minor points, including formatting and consistency, should be clarified. Are the rationale for sequencing the genome and the species significance clearly described? Yes Are the protocols appropriate and is the work technically sound? Yes Are sufficient details of the sequencing and extraction, software used, and materials provided to allow replication by others? Partly Are the datasets clearly presented in a usable and accessible format, and the assembly and annotation available in an appropriate subject-specific repository? Yes Competing Interests: No competing interests were disclosed. Reviewer Expertise: Microbiology, Molecular biology, Phage engineering, High-throughput functional genomics I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above. Close READ LESS CITE CITE HOW TO CITE THIS REPORT Chitboonthavisuk C. Reviewer Report For: Isolation and complete genome sequence of Citrobacter bacteriophage Ursula [version 1; peer review: 1 approved, 1 approved with reservations] . F1000Research 2025, 14 :86 ( https://doi.org/10.5256/f1000research.174859.r433417 ) The direct URL for this report is: https://f1000research.com/articles/14-86/v1#referee-response-433417 NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS Report a concern Respond or Comment COMMENT ON THIS REPORT Views 0 Cite How to cite this report: Gencer D. Reviewer Report For: Isolation and complete genome sequence of Citrobacter bacteriophage Ursula [version 1; peer review: 1 approved, 1 approved with reservations] . F1000Research 2025, 14 :86 ( https://doi.org/10.5256/f1000research.174859.r418202 ) The direct URL for this report is: https://f1000research.com/articles/14-86/v1#referee-response-418202 NOTE: it is important to ensure the information in square brackets after the title is included in this citation. Close Copy Citation Details Reviewer Report 25 Nov 2025 Donus Gencer , Trabzon University, Trabzon, Turkey Approved VIEWS 0 https://doi.org/10.5256/f1000research.174859.r418202 The manuscript reports the isolation and complete genome sequencing of a novel Citrobacter-infecting bacteriophage, named Ursula, isolated from aquatic environments associated with fish pathogens. The study provides detailed experimental methods, electron microscopy evidence, and full genomic data of a 183,411 ... Continue reading READ ALL The manuscript reports the isolation and complete genome sequencing of a novel Citrobacter-infecting bacteriophage, named Ursula, isolated from aquatic environments associated with fish pathogens. The study provides detailed experimental methods, electron microscopy evidence, and full genomic data of a 183,411 bp T4-like myovirus containing 343 ORFs and 12 tRNA genes. The genome has been deposited in GenBank (PQ589834) and supplementary data are publicly available on Figshare. This Genome Note fulfills the expectations for this article type. The rationale for sequencing is clearly linked to the growing impact of Citrobacter infections and antibiotic resistance in aquaculture. Experimental protocols are standard, technically sound, and adequately described for replication. Data presentation and repository submission meet F1000Research’s open-science criteria. However, the section discussing novelty as a “new species” could be strengthened. While the genome differs by ~6–7% from the closest Citrobacter phages (Merlin and Moon), quantitative genomic similarity metrics (ANI or BLASTN %) and phylogenetic visualization are not shown. These additions would substantiate the claim of Ursula representing a novel species. If such analysis cannot be added, the statement should be softened to “likely represents a novel species”. Please provide numerical ANI or BLASTN similarity values versus Merlin and Moon phages to support the new species designation. Include GC content, genome termini type, and packaging mechanism if available. Minor formatting corrections (e.g., spacing in gene identifiers “Ursula_0017”). This work is technically robust, transparent, and suitable for indexing as a Genome Note. Minor revisions are recommended to clarify comparative genomic evidence and minor formatting. Are the rationale for sequencing the genome and the species significance clearly described? Yes Are the protocols appropriate and is the work technically sound? Yes Are sufficient details of the sequencing and extraction, software used, and materials provided to allow replication by others? Partly Are the datasets clearly presented in a usable and accessible format, and the assembly and annotation available in an appropriate subject-specific repository? Yes Competing Interests: No competing interests were disclosed. Reviewer Expertise: Molecular Virology, Insect Microbiology, Viral Genomics, Biocontrol and Phage Therapy. I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard. Close READ LESS CITE CITE HOW TO CITE THIS REPORT Gencer D. Reviewer Report For: Isolation and complete genome sequence of Citrobacter bacteriophage Ursula [version 1; peer review: 1 approved, 1 approved with reservations] . F1000Research 2025, 14 :86 ( https://doi.org/10.5256/f1000research.174859.r418202 ) The direct URL for this report is: https://f1000research.com/articles/14-86/v1#referee-response-418202 NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS Report a concern Respond or Comment COMMENT ON THIS REPORT Comments on this article Comments (0) Version 1 VERSION 1 PUBLISHED 15 Jan 2025 ADD YOUR COMMENT Comment keyboard_arrow_left keyboard_arrow_right Open Peer Review Reviewer Status info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions Reviewer Reports Invited Reviewers 1 2 Version 1 15 Jan 25 read read Donus Gencer , Trabzon University, Trabzon, Turkey Chutikarn Chitboonthavisuk , University of Wisconsin-Madison, Madison, USA Comments on this article All Comments (0) Add a comment Sign up for content alerts Sign Up You are now signed up to receive this alert Browse by related subjects keyboard_arrow_left Back to all reports Reviewer Report 0 Views copyright © 2026 Chitboonthavisuk C. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 30 Dec 2025 | for Version 1 Chutikarn Chitboonthavisuk , University of Wisconsin-Madison, Madison, Wisconsin, USA 0 Views copyright © 2026 Chitboonthavisuk C. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. format_quote Cite this report speaker_notes Responses (0) Approved With Reservations info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions Summary The manuscript describes the isolation and characterization of “Ursula” phage, a novel phage targeting Citrobacter strains, isolated from an aquatic environment. Given the rising of antibiotic resistance in pathogens, including Citrobacter freundii , emerged in aquaculture industry and the high cost in disease treatment, the isolation of new phage holds potential economic value for the industry. Overall, the authors presented their works on isolating a novel bacteriophage, genome sequencing, and morphology characterization. While the characterization and sequencing are described, this manuscript needs additional information to support their classification and their statement of this phage for further application in an aquaculture system. Here are several major and minor points that need clarification. The major points that may help the authors improve their work. 1. Genomic analysis and novelty of the phage discovery The statement “BLASTn search against the NCBI Nucleotide collection produced a number of relevant hits with a good homology” is vague. The authors should provide quantitative metrics, such as average nucleotide identity (ANI) or total similarity, to clearly define the relationship and similarity between Ursula and the other phages, Merlin and Moon. Schematic of genomic comparison can be provided. The current name used, Ursula, was previously named for actinophage, although that actinophage has been renamed to Trident. It might be confusing to readers. Authors could perform phylogenetic analyses using conserved markers may help improving the classification. 2. Authors claim the discovery of a novel phage and characterization of this phage. In addition, authors suggest this phage as a candidate for biocontrol; however, the authors did not provide a thorough characterization and their capability of the phage as a biocontrol candidate. The authors did not provide a basic growth characterization, including plaque morphology, stability, host range determination, and the burst size of this novel phage. A complete basic characterization may help improve the report and can be informative for further study. The figure of phage morphology is low in quality, obstructed by other components/debris. 3. The authors stated that this new phage is an economically viable tool for Citrobacter biocontrol and is highly demanded by the industry in their introduction; however, the authors did not provide reference information about the phages or antibiotic treatments currently used, the demand of acquiring new phages, and the comparison across these methods to better claim that this phage tool is economically efficient. The authors did not provide a host range of this novel phage, especially Citrobacter strains that cause diseases or are found in outbreaks in the aquaculture industry, which could help support the economic aspects and applications of this phage. However, this point regarding the economic aspects of this discovery might be out of the scope of this manuscript. Here are minor points. This includes clarifications, formatting, and consistency. In the method section, italicize Citrobacter spp., provide a reference or resource of Citrobacter strain used in this study. Italicize in the paragraph “After incubation,…. A lawn of Citrobacter spp. CF69 strain In the incubation step, authors stated “enriched culture was centrifuged at 12,000 rpm using a tabletop microcentrifuge”, without providing the model and diameter of the microcentrifuge. Additionally, authors use xg across the paper; ensure to keep the units consistent. During the extraction step, the soft agar layer and chloroform mix were pelleted at 10,000 xg for 5 min. Is this amount of time enough with this volume to completely separate the mixtures? Authors used both “h” and “hour”, both “µl” and “µL”, both “ml” and “mL”, both “pfu” and “PFU”, “min” and “minutes” please keep it consistent. Typo of parentheses in “…. dried and studied in Jeol JEM-1400Flash electron microscope Jeol Ltd., Japan).” Reference of chemicals is inconsistent, authors used (“ID number”, “brand”) and (“brand”, “ID number”). Space in the result section, (Ursula_ 0017), can be removed. Authors stated at the end of result section that “ numerous enzymes and regulatory proteins encoded in its genome make it a good candidate for phage therapy applications” may need more support information. Regarding the details of the sequencing and extraction, software used, and materials provided for the reproducibility, additional detail would help improve the reproducibility of these processes. This includes small detail, such as the volume of phage used, modification needed for this particular types of samples, details to expand more on the standard reagent/manufacturer’s protocol, and the availability of scripts used for sequencing analyses. This manuscript is suitable for Genome Note. Major points, including a thorough characterization of the phage, both phenotype and physiochemistry, and host range determination, could help improve this discovery for further application, and genomic comparison would clarify the novelty of this phage discovery. Minor points, including formatting and consistency, should be clarified. Are the rationale for sequencing the genome and the species significance clearly described? Yes Are the protocols appropriate and is the work technically sound? Yes Are sufficient details of the sequencing and extraction, software used, and materials provided to allow replication by others? Partly Are the datasets clearly presented in a usable and accessible format, and the assembly and annotation available in an appropriate subject-specific repository? Yes Competing Interests No competing interests were disclosed. Reviewer Expertise Microbiology, Molecular biology, Phage engineering, High-throughput functional genomics I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above. reply Respond to this report Responses (0) Chitboonthavisuk C. Peer Review Report For: Isolation and complete genome sequence of Citrobacter bacteriophage Ursula [version 1; peer review: 1 approved, 1 approved with reservations] . F1000Research 2025, 14 :86 ( https://doi.org/10.5256/f1000research.174859.r433417) NOTE: it is important to ensure the information in square brackets after the title is included in this citation. The direct URL for this report is: https://f1000research.com/articles/14-86/v1#referee-response-433417 keyboard_arrow_left Back to all reports Reviewer Report 0 Views copyright © 2025 Gencer D. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 25 Nov 2025 | for Version 1 Donus Gencer , Trabzon University, Trabzon, Turkey 0 Views copyright © 2025 Gencer D. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. format_quote Cite this report speaker_notes Responses (0) Approved info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions The manuscript reports the isolation and complete genome sequencing of a novel Citrobacter-infecting bacteriophage, named Ursula, isolated from aquatic environments associated with fish pathogens. The study provides detailed experimental methods, electron microscopy evidence, and full genomic data of a 183,411 bp T4-like myovirus containing 343 ORFs and 12 tRNA genes. The genome has been deposited in GenBank (PQ589834) and supplementary data are publicly available on Figshare. This Genome Note fulfills the expectations for this article type. The rationale for sequencing is clearly linked to the growing impact of Citrobacter infections and antibiotic resistance in aquaculture. Experimental protocols are standard, technically sound, and adequately described for replication. Data presentation and repository submission meet F1000Research’s open-science criteria. However, the section discussing novelty as a “new species” could be strengthened. While the genome differs by ~6–7% from the closest Citrobacter phages (Merlin and Moon), quantitative genomic similarity metrics (ANI or BLASTN %) and phylogenetic visualization are not shown. These additions would substantiate the claim of Ursula representing a novel species. If such analysis cannot be added, the statement should be softened to “likely represents a novel species”. Please provide numerical ANI or BLASTN similarity values versus Merlin and Moon phages to support the new species designation. Include GC content, genome termini type, and packaging mechanism if available. Minor formatting corrections (e.g., spacing in gene identifiers “Ursula_0017”). This work is technically robust, transparent, and suitable for indexing as a Genome Note. Minor revisions are recommended to clarify comparative genomic evidence and minor formatting. Are the rationale for sequencing the genome and the species significance clearly described? Yes Are the protocols appropriate and is the work technically sound? Yes Are sufficient details of the sequencing and extraction, software used, and materials provided to allow replication by others? Partly Are the datasets clearly presented in a usable and accessible format, and the assembly and annotation available in an appropriate subject-specific repository? Yes Competing Interests No competing interests were disclosed. Reviewer Expertise Molecular Virology, Insect Microbiology, Viral Genomics, Biocontrol and Phage Therapy. I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard. reply Respond to this report Responses (0) Gencer D. Peer Review Report For: Isolation and complete genome sequence of Citrobacter bacteriophage Ursula [version 1; peer review: 1 approved, 1 approved with reservations] . F1000Research 2025, 14 :86 ( https://doi.org/10.5256/f1000research.174859.r418202) NOTE: it is important to ensure the information in square brackets after the title is included in this citation. 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