Host genetics shape productive lifespan in dairy cattle by sculpting rumen microbial metabolic functions

Host genetics shape productive lifespan in dairy cattle by sculpting rumen microbial metabolic functions | 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 Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Host genetics shape productive lifespan in dairy cattle by sculpting rumen microbial metabolic functions Panping Yang, Zhuoxuan Wu, Zhuang Cao, Yujia Li, Lei Yan, Yuefei Yan, and 15 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-9101224/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted 9 You are reading this latest preprint version Abstract Background Rumen microbiota constitutes key determinants of productive lifespan in dairy cattle, a trait that lies at the heart of breeding program profitability. However, whether host genetic variation influences productive lifespan through its effects on the rumen microbiota remains largely unexplored. To address this, we generated and analyzed host genomic data, 16S rRNA sequences, metagenomic profiles, and longitudinal productive lifespan records from 333 dairy cows with divergent longevity. Results Rumen microbial community composition shifted significantly with increasing productive lifespan, characterized by a decline in firmicutes and an increase in proteobacteria , alongside reduced microbial diversity. We identified 28 core genera universally present across individuals and 113 keystone taxa through co-occurrence network analysis, which collectively represent functional hubs that may mediate host productive lifespan. Variance component analysis revealed substantial heritability in the rumen microbiome, with 82% of core genera and 87% of keystone taxa showing significant heritable signals. At the functional level, glycolysis/gluconeogenesis, quorum sensing, and the TCA cycle emerged as highly heritable pathways and exhibited strong genetic correlations with productive lifespan (|r_g| = 0.32–0.80). Productive lifespan itself was lowly heritable, yet the rumen microbiome explained 36.2% of its phenotypic variance-pointing to a major microbial contribution. Integrated microbiome-wide and genome-wide association studies identified four microbial genera and three host genetic variants significantly associated with productive lifespan. Multi-omics integration, combined with microbial genome assembly, further revealed that host genotypes influence productive lifespan indirectly through modulation of microbial metabolic pathways. Conclusions Integrating longitudinal multi-omics analyses, we uncovered a coordinated role for host genetics and rumen microbiota in regulating productive lifespan of dairy cattle, which lays the groundwork for genomically-informed, microbiome-targeted breeding strategies to enhance longevity, improve farm profitability, and support sustainable dairy production. Rumen microbiota Productive lifespan Host genetics Dairy cattle Heritability Microbiability Full Text Additional Declarations No competing interests reported. Supplementary Files Fig.S1PCAResultsAfterBatchCorrection.docx Fig.S2DifferencesinRumenCommunityStructureBetweenDairyCowswithDivergentProductiveLifespans.docx Fig.S3CorrelationAnalysisBetweenSpeciesPrevalenceandRelativeAbundance.docx Fig.S4Heritabledistributionofrumenmicrobialgenera.docx TableS2Detectionratesofrumenmicrobiotaatgenuslevelinacohortof340Holsteincattle.xlsx TableS3Heritabilityofrumenmicrobiota.csv Table.S4mbGWASresultsdata.xlsx Table.S6GWASfordairycowproductionlifespan.xlsx Table.S5MWASPval.xlsx TableS1.PLSDABatchEffect.xlsx Table.S7FunctionalannotationofgErysipelotrichaceaeUCG002fromassociatedmicrobes.xlsx Cite Share Download PDF Status: Under Review Version 1 posted Reviews received at journal 01 May, 2026 Reviewers agreed at journal 30 Apr, 2026 Reviewers agreed at journal 27 Apr, 2026 Reviewers agreed at journal 24 Apr, 2026 Reviewers agreed at journal 24 Apr, 2026 Reviewers invited by journal 22 Apr, 2026 Editor assigned by journal 14 Apr, 2026 Submission checks completed at journal 09 Apr, 2026 First submitted to journal 06 Apr, 2026 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. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board 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-9101224","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":632994437,"identity":"3ca3e17a-24a5-40e2-904c-a4a1da5000a5","order_by":0,"name":"Panping 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functions","fulltext":[],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":false,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":true,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":true,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"microbiome","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"mbio","sideBox":"Learn more about [Microbiome](http://microbiomejournal.biomedcentral.com/)","snPcode":"40168","submissionUrl":"https://submission.nature.com/new-submission/40168/3","title":"Microbiome","twitterHandle":"@MicrobiomeJ","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"BMC/SO AJ","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Rumen microbiota, Productive lifespan, Host genetics, Dairy cattle Heritability, Microbiability","lastPublishedDoi":"10.21203/rs.3.rs-9101224/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-9101224/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cb\u003eBackground\u003c/b\u003e\u003c/p\u003e \u003cp\u003eRumen microbiota constitutes key determinants of productive lifespan in dairy cattle, a trait that lies at the heart of breeding program profitability. However, whether host genetic variation influences productive lifespan through its effects on the rumen microbiota remains largely unexplored. To address this, we generated and analyzed host genomic data, 16S rRNA sequences, metagenomic profiles, and longitudinal productive lifespan records from 333 dairy cows with divergent longevity.\u003c/p\u003e\u003cp\u003e\u003cb\u003eResults\u003c/b\u003e\u003c/p\u003e \u003cp\u003eRumen microbial community composition shifted significantly with increasing productive lifespan, characterized by a decline in \u003cem\u003efirmicutes\u003c/em\u003e and an increase in \u003cem\u003eproteobacteria\u003c/em\u003e, alongside reduced microbial diversity. We identified 28 core genera universally present across individuals and 113 keystone taxa through co-occurrence network analysis, which collectively represent functional hubs that may mediate host productive lifespan. Variance component analysis revealed substantial heritability in the rumen microbiome, with 82% of core genera and 87% of keystone taxa showing significant heritable signals. At the functional level, glycolysis/gluconeogenesis, quorum sensing, and the TCA cycle emerged as highly heritable pathways and exhibited strong genetic correlations with productive lifespan (|r_g| = 0.32\u0026ndash;0.80). Productive lifespan itself was lowly heritable, yet the rumen microbiome explained 36.2% of its phenotypic variance-pointing to a major microbial contribution. Integrated microbiome-wide and genome-wide association studies identified four microbial genera and three host genetic variants significantly associated with productive lifespan. Multi-omics integration, combined with microbial genome assembly, further revealed that host genotypes influence productive lifespan indirectly through modulation of microbial metabolic pathways.\u003c/p\u003e\u003cp\u003e\u003cb\u003eConclusions\u003c/b\u003e\u003c/p\u003e \u003cp\u003eIntegrating longitudinal multi-omics analyses, we uncovered a coordinated role for host genetics and rumen microbiota in regulating productive lifespan of dairy cattle, which lays the groundwork for genomically-informed, microbiome-targeted breeding strategies to enhance longevity, improve farm profitability, and support sustainable dairy production.\u003c/p\u003e","manuscriptTitle":"Host genetics shape productive lifespan in dairy cattle by sculpting rumen microbial metabolic functions","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2026-05-04 22:35:19","doi":"10.21203/rs.3.rs-9101224/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"editorInvitedReview","content":"","date":"2026-05-01T13:52:47+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"138890706451954881619263081158256833401","date":"2026-04-30T11:39:42+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"198564896001090375087732474130888274301","date":"2026-04-27T17:10:58+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"266787227460390683443102043205814746209","date":"2026-04-24T18:00:55+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"184552768839395628514492350263801370420","date":"2026-04-24T15:49:43+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2026-04-22T15:03:32+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2026-04-14T23:05:34+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2026-04-09T10:59:44+00:00","index":"","fulltext":""},{"type":"submitted","content":"Microbiome","date":"2026-04-07T02:05:38+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"microbiome","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"mbio","sideBox":"Learn more about [Microbiome](http://microbiomejournal.biomedcentral.com/)","snPcode":"40168","submissionUrl":"https://submission.nature.com/new-submission/40168/3","title":"Microbiome","twitterHandle":"@MicrobiomeJ","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"BMC/SO AJ","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"a81899bb-ad01-435f-a101-16226580d947","owner":[],"postedDate":"May 4th, 2026","published":true,"recentEditorialEvents":[{"type":"editorInvitedReview","content":"","date":"2026-05-01T13:52:47+00:00","index":37,"fulltext":""},{"type":"reviewerAgreed","content":"138890706451954881619263081158256833401","date":"2026-04-30T11:39:42+00:00","index":36,"fulltext":""}],"rejectedJournal":[],"revision":"","amendment":"","status":"under-review","subjectAreas":[],"tags":[],"updatedAt":"2026-05-04T22:35:20+00:00","versionOfRecord":[],"versionCreatedAt":"2026-05-04 22:35:19","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-9101224","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-9101224","identity":"rs-9101224","version":["v1"]},"buildId":"XKTyCvWXoU3ODBz1xrDgd","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}