{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,11]],"date-time":"2026-02-11T13:47:42Z","timestamp":1770817662433,"version":"3.50.1"},"reference-count":46,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2024,6,27]],"date-time":"2024-06-27T00:00:00Z","timestamp":1719446400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002923","name":"CONICET","doi-asserted-by":"crossref","award":["PIP 11220100102665CO"],"award-info":[{"award-number":["PIP 11220100102665CO"]}],"id":[{"id":"10.13039\/501100002923","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100003074","name":"Agencia Nacional de Promoci\u00f3n Cient\u00edfica y Tecnol\u00f3gica","doi-asserted-by":"publisher","award":["PICT 2020-0343"],"award-info":[{"award-number":["PICT 2020-0343"]}],"id":[{"id":"10.13039\/501100003074","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>The economic impact of gastrointestinal (GI) nematode infections on livestock production is well documented worldwide. Increasing evidence supports the hypothesis that parasite colonization induces significant changes in the GI tract environment and, therefore, in the landscape where the microbiota and parasites occur. Understanding the interactions between bacterial and parasite populations in the digestive tract of livestock may be useful to design parasite control strategies based on microbiota modification. The aims of this work were to investigate the impact of the oxytetracycline-mediated manipulation of the gut microbial community on the composition of GI nematode populations in naturally infected sheep and to explore changes in the GI microbial communities after nematode population treatment with the anthelmintic compound monepantel. Extensive manipulation of the GI microbiota with a therapeutic dose of the long-acting oxytetracycline formulation did not induce significant changes in the GI nematode burden. The gut microbiota of treated animals returned to control levels 17 days after treatment, suggesting strong resilience of the sheep microbial community to antibiotic-mediated microbiota perturbation. A significant decrease of the bacterial <jats:italic>Mycoplasmataceae<\/jats:italic> family (Log<jats:sub>2<\/jats:sub>FC = -4, P<jats:sub>adj<\/jats:sub> = 0.001) and a marked increase of the <jats:italic>Methanobacteriaceae<\/jats:italic> family (Log<jats:sub>2<\/jats:sub>FC = 2.9, P<jats:sub>adj<\/jats:sub> = 0.018) were observed in the abomasum of sheep receiving the monepantel treatment. While a comprehensive evaluation of the interactions among GI mycoplasma, methanobacteria and nematode populations deserves further assessment, the bacteria-nematode population interactions should be included in future control programs in livestock production. Understanding how bacteria and parasites may influence each other in the GI tract environment may substantially contribute to the knowledge of the role of microbiota composition in nematode parasite establishment and the role of the parasites in the microbiota composition.<\/jats:p>","DOI":"10.1371\/journal.pone.0306390","type":"journal-article","created":{"date-parts":[[2024,6,27]],"date-time":"2024-06-27T20:39:31Z","timestamp":1719520771000},"page":"e0306390","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":3,"title":["Interaction between bacterial microbiota and nematode parasite communities in sheep\u2019s gastrointestinal tract"],"prefix":"10.1371","volume":"19","author":[{"given":"Laura","family":"Mate","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Luis Ignacio","family":"Alvarez","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mercedes","family":"Lloberas","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fernanda","family":"Imperiale","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carlos Edmundo","family":"Lanusse","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1989-8733","authenticated-orcid":true,"given":"Juan Pedro","family":"Liron","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2024,6,27]]},"reference":[{"key":"pone.0306390.ref001","doi-asserted-by":"crossref","first-page":"1133","DOI":"10.1016\/j.ijpara.2021.10.007","article-title":"A journey through 50 years of research relevant to the control of gastrointestinal nematodes in ruminant livestock and thoughts on future directions","volume":"51","author":"JS Gilleard","year":"2021","journal-title":"Int J Parasitol"},{"key":"pone.0306390.ref002","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.vetpar.2011.11.048","article-title":"An inconvenient truth: global worming and anthelmintic resistance","volume":"186","author":"RM Kaplan","year":"2012","journal-title":"Vet Parasitol"},{"key":"pone.0306390.ref003","doi-asserted-by":"crossref","first-page":"e12955","DOI":"10.1111\/pim.12955","article-title":"Gastrointestinal worms and bacteria: From association to intervention","volume":"45","author":"J Rooney","year":"2023","journal-title":"Parasite Immunol"},{"key":"pone.0306390.ref004","doi-asserted-by":"crossref","first-page":"843","DOI":"10.3389\/fmicb.2018.00843","article-title":"Parasite-microbiota interactions with the vertebrate gut: synthesis through an ecological lens","volume":"9","author":"JM Leung","year":"2018","journal-title":"Front Microbiol"},{"key":"pone.0306390.ref005","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1016\/j.pt.2017.04.004","article-title":"This gut ain\u2019t big enough for both of us. 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Yang","year":"2020","journal-title":"mSystems"},{"key":"pone.0306390.ref021","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.ijpddr.2012.11.001","article-title":"Comparative tissue pharmacokinetics and efficacy of moxidectin, abamectin and ivermectin in lambs infected with resistant nematodes: Impact of drug treatments on parasite P-glycoprotein expression","volume":"3","author":"M Lloberas","year":"2013","journal-title":"Int J Parasitol Drugs Drug Resist"},{"key":"pone.0306390.ref022","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.vetpar.2019.06.003","article-title":"Recovery of fenbendazole efficacy on resistant Haemonchus contortus by management of parasite refugia and population replacement","volume":"271","author":"SM Muchiut","year":"2019","journal-title":"Vet Parasitol"},{"key":"pone.0306390.ref023","doi-asserted-by":"crossref","first-page":"109121","DOI":"10.1016\/j.vetpar.2020.109121","article-title":"Combination of bioactive phytochemicals 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Resist"},{"key":"pone.0306390.ref026","doi-asserted-by":"crossref","first-page":"D590","DOI":"10.1093\/nar\/gks1219","article-title":"The SILVA ribosomal RNA gene database project: improved data processing and web-based tools","volume":"41","author":"C Quast","year":"2012","journal-title":"Nucleic Acids Res"},{"key":"pone.0306390.ref027","doi-asserted-by":"crossref","first-page":"e61217","DOI":"10.1371\/journal.pone.0061217","article-title":"phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data","volume":"8","author":"PJ McMurdie","year":"2013","journal-title":"PLoS One"},{"key":"pone.0306390.ref028","author":"L Lahti","year":"2017","journal-title":"microbiome R package"},{"key":"pone.0306390.ref029","first-page":"719","article-title":"The vegan package","volume":"10","author":"J Oksanen","year":"2007","journal-title":"Community ecology package"},{"key":"pone.0306390.ref030","first-page":"1","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"MI Love","year":"2014","journal-title":"Genome Biol"},{"key":"pone.0306390.ref031","first-page":"104","article-title":"Nutritional and biological control synergism against gastrointestinal nematodes in small ruminants","volume":"4","author":"A Sahoo","year":"2016","journal-title":"J Vet Sci Anim Husb"},{"key":"pone.0306390.ref032","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13071-016-1908-4","article-title":"Helminth infections and gut microbiota\u2013a feline perspective","volume":"9","author":"AM Duarte","year":"2016","journal-title":"Parasit Vectors"},{"key":"pone.0306390.ref033","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.vetpar.2008.10.006","article-title":"Efficacy of the amino-acetonitrile derivative, monepantel, against experimental and natural adult stage gastro-intestinal nematode infections in sheep","volume":"159","author":"H Sager","year":"2009","journal-title":"Vet Parasitol"},{"key":"pone.0306390.ref034","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/j.vetpar.2008.11.028","article-title":"Dose confirmation studies for monepantel, an amino-acetonitrile derivative, against fourth stage gastro-intestinal nematode larvae infecting sheep","volume":"160","author":"BC Hosking","year":"2009","journal-title":"Vet Parasitol"},{"key":"pone.0306390.ref035","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.vetpar.2014.02.049","article-title":"Accumulation of monepantel and its sulphone derivative in tissues of nematode location in sheep: pharmacokinetic support to its excellent nematodicidal activity","volume":"203","author":"A Lifschitz","year":"2014","journal-title":"Vet Parasitol"},{"key":"pone.0306390.ref036","first-page":"1","article-title":"Variation in gut bacterial composition is associated with Haemonchus contortus parasite infection of sheep","volume":"2","author":"MA Al Mamun","year":"2020","journal-title":"Anim Microbiome"},{"key":"pone.0306390.ref037","doi-asserted-by":"crossref","first-page":"1216","DOI":"10.3390\/antibiotics10101216","article-title":"Integrating the human and animal sides of mycoplasmas resistance to antimicrobials","volume":"10","author":"S Pereyre","year":"2021","journal-title":"Antibiotics"},{"key":"pone.0306390.ref038","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1186\/s42523-022-00172-1","article-title":"Bacterial communities in the gastrointestinal tract segments of helminth-resistant and helminth-susceptible sheep","volume":"4","author":"EA Paz","year":"2022","journal-title":"Anim Microbiome"},{"key":"pone.0306390.ref039","doi-asserted-by":"crossref","first-page":"15","DOI":"10.4141\/A97-021","article-title":"Current understanding of the role of the reticulum and reticulo-omasal orifice in the control of digesta passage from the ruminoreticulum of sheep and cattle","volume":"78","author":"EK Okine","year":"1998","journal-title":"Can J Anim Sci"},{"key":"pone.0306390.ref040","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/s11259-017-9698-5","article-title":"Microbial community and ovine host response varies with early and late stages of Haemonchus contortus infection","volume":"41","author":"S El-Ashram","year":"2017","journal-title":"Vet Res Commun"},{"key":"pone.0306390.ref041","article-title":"Stomach fluke (paramphistomes) in ruminants","author":"J Lloyd","year":"2000","journal-title":"NSW Agriculture"},{"key":"pone.0306390.ref042","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/j.tree.2018.01.013","article-title":"Towards a comparable quantification of resilience","volume":"33","author":"J Ingrisch","year":"2018","journal-title":"Trends Ecol Evol"},{"key":"pone.0306390.ref043","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1038\/nrmicro.2017.58","article-title":"The resilience of the intestinal microbiota influences health and disease","volume":"15","author":"F Sommer","year":"2017","journal-title":"Nat Rev Microbiol"},{"key":"pone.0306390.ref044","first-page":"e02141","article-title":"Diet influences early microbiota development in dairy calves without long-term impacts on milk production","volume":"85","author":"KA Dill-McFarland","year":"2019","journal-title":"Appl Environ Microbiol"},{"key":"pone.0306390.ref045","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s40168-019-0696-4","article-title":"Antibiotic treatment in feedlot cattle: a longitudinal study of the effect of oxytetracycline and tulathromycin on the fecal and nasopharyngeal microbiota","volume":"7","author":"DB Holman","year":"2019","journal-title":"Microbiome"},{"key":"pone.0306390.ref046","doi-asserted-by":"crossref","first-page":"650","DOI":"10.1016\/j.chom.2019.10.011","article-title":"Recovery of the gut microbiota after antibiotics depends on host diet, community context, and environmental 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