{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:19:01Z","timestamp":1787026741479,"version":"build-2736575974"},"reference-count":129,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,11,9]],"date-time":"2023-11-09T00:00:00Z","timestamp":1699488000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>\n                    Understanding the relationships between social stress and the gastrointestinal microbiota, and how they influence host health and performance is expected to have many scientific and commercial implementations in different species, including identification and improvement of challenges to animal welfare and health. In particular, the study of the stress impact on the gastrointestinal microbiota of pigs may be of interest as a model for human health. A porcine stress model based on repeated regrouping and reduced space allowance during the last 4 weeks of the finishing period was developed to identify stress-induced changes in the gut microbiome composition. The application of the porcine stress model resulted in a significant increase in salivary cortisol concentration over the course of the trial and decreased growth performance and appetite. The applied social stress resulted in 32 bacteria being either enriched (13) or depleted (19) in the intestine and feces. Fecal samples showed a greater number of microbial genera influenced by stress than caecum or colon samples. Our trial revealed that the opportunistic pathogens\n                    <jats:italic>Treponema<\/jats:italic>\n                    and\n                    <jats:italic>Clostridium<\/jats:italic>\n                    were enriched in colonic and fecal samples from stressed pigs. Additionally, genera such as\n                    <jats:italic>Streptococcus<\/jats:italic>\n                    ,\n                    <jats:italic>Parabacteroides<\/jats:italic>\n                    ,\n                    <jats:italic>Desulfovibrio<\/jats:italic>\n                    ,\n                    <jats:italic>Terrisporobacter<\/jats:italic>\n                    ,\n                    <jats:italic>Marvinbryantia<\/jats:italic>\n                    , and\n                    <jats:italic>Romboutsia<\/jats:italic>\n                    were found to be enriched in response to social stress. In contrast, the genera\n                    <jats:italic>Prevotella<\/jats:italic>\n                    ,\n                    <jats:italic>Faecalibacterium<\/jats:italic>\n                    ,\n                    <jats:italic>Butyricicoccus<\/jats:italic>\n                    ,\n                    <jats:italic>Dialister<\/jats:italic>\n                    ,\n                    <jats:italic>Alloprevotella<\/jats:italic>\n                    ,\n                    <jats:italic>Megasphaera<\/jats:italic>\n                    , and\n                    <jats:italic>Mitsuokella<\/jats:italic>\n                    were depleted. These depleted bacteria are of great interest because they synthesize metabolites [e.g., short-chain fatty acids (SCFA), in particular, butyrate] showing beneficial health benefits due to inhibitory effects on pathogenic bacteria in different animal species. Of particular interest are\n                    <jats:italic>Dialister<\/jats:italic>\n                    and\n                    <jats:italic>Faecalibacterium<\/jats:italic>\n                    , as their depletion was identified in a human study to be associated with inferior quality of life and depression. We also revealed that some pigs were more susceptible to pathogens as indicated by large enrichments of opportunistic pathogens of\n                    <jats:italic>Clostridium, Treponema, Streptococcus<\/jats:italic>\n                    and\n                    <jats:italic>Campylobacter<\/jats:italic>\n                    . Generally, our results provide further evidence for the microbiota-gut-brain axis as indicated by an increase in cortisol concentration due to social stress regulated by the hypothalamic\u2013pituitary\u2013adrenal axis, and a change in microbiota composition, particularly of bacteria known to be associated with pathogenicity and mental health diseases.\n                  <\/jats:p>","DOI":"10.3389\/fmicb.2023.1197371","type":"journal-article","created":{"date-parts":[[2023,11,12]],"date-time":"2023-11-12T22:46:09Z","timestamp":1699829169000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":33,"title":["Identification of intestinal and fecal microbial biomarkers using a porcine social stress model"],"prefix":"10.3389","volume":"14","author":[{"given":"Tuan Q.","family":"Nguyen","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marina","family":"Mart\u00ednez-\u00c1lvaro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joana","family":"Lima","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marc D.","family":"Auffret","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenneth M. 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Biotechnol."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"965","DOI":"10.1016\/j.anbehav.2003.12.016","article-title":"Aggression and group size in domesticated pigs, Sus scrofa: When the winner takes it all and the loser is standing small","volume":"68","author":"Andersen","year":"2004","journal-title":"Anim. Behav."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"216","DOI":"10.3389\/fgene.2020.00216","article-title":"Exploring phenotypes for disease resilience in pigs using complete blood count data from a natural disease challenge model","volume":"11","author":"Bai","year":"2020","journal-title":"Front. Genet."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1016\/j.bbi.2010.10.023","article-title":"Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immunomodulation","volume":"25","author":"Bailey","year":"2011","journal-title":"Brain Behav. Immun."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"541","DOI":"10.3389\/fpsyt.2020.00541","article-title":"Altered composition of gut microbiota in depression: a systematic review","volume":"11","author":"Barandouzi","year":"2020","journal-title":"Front. Psych."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"1","DOI":"10.18637\/jss.v067.i01","article-title":"fitting linear mixed-effects models using lme4","volume":"67","author":"Bates","year":"2015","journal-title":"J. Stat. Softw."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1016\/j.nmni.2017.11.001","article-title":"Libanicoccus massiliensis gen. nov., sp. nov., a new bacterium isolated from human stool","volume":"21","author":"Bilen","year":"2018","journal-title":"New Microbes New Infect."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1016\/j.livsci.2014.04.034","article-title":"Genomics and disease resistance studies in livestock","volume":"166","author":"Bishop","year":"2014","journal-title":"Livest. Sci."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1111\/j.2041-1014.2009.00550.x","article-title":"Desulfovibrio spp. survive within KB cells and modulate inflammatory responses","volume":"25","author":"Bisson-Boutelliez","year":"2010","journal-title":"Mol Oral Microbiol"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"888","DOI":"10.1172\/JCI81121","article-title":"The gut connectome: Making sense of what you eat","volume":"125","author":"Boh\u00f3rquez","year":"2015","journal-title":"J. Clin. Invest."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"e89881","DOI":"10.1371\/journal.pone.0089881","article-title":"An enteroendocrine cell \u2013 enteric glia connection revealed by 3D electron microscopy","volume":"9","author":"Boh\u00f3rquez","year":"2014","journal-title":"PLoS One"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.18637\/JSS.V100.I05","article-title":"Bayesian item response modeling in R with brms and Stan","volume":"100","author":"B\u00fcrkner","year":"2021","journal-title":"J. Stat. Softw."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1177\/0300985816653795","article-title":"Swine dysentery","volume":"54","author":"Burrough","year":"2017","journal-title":"Vet. Pathol."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"581","DOI":"10.1038\/nmeth.3869","article-title":"DADA2: High-resolution sample inference from Illumina amplicon data","volume":"13","author":"Callahan","year":"2016","journal-title":"Nat. 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Behav."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"7931","DOI":"10.1128\/AEM.01784-10","article-title":"Influence of the composition of the cellulolytic flora on the development of hydrogenotrophic microorganisms, hydrogen utilization, and methane production in the rumens of gnotobiotically reared lambs","volume":"76","author":"Chaucheyras-Durand","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1016\/j.jad.2020.12.143","article-title":"Gut microbiota dysbiosis in depressed women: The association of symptom severity and microbiota function","volume":"282","author":"Chen","year":"2021","journal-title":"J. Affect. Disord."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1016\/j.jveb.2015.05.002","article-title":"Effects of stocking density and environmental enrichment on behavior and fecal corticosteroid levels of pigs under commercial farm conditions","volume":"10","author":"Cornale","year":"2015","journal-title":"J. Vet. Behav. Clin. Appl. Res."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1016\/j.applanim.2006.05.007","article-title":"Pig\u2019s responses to repeated social regrouping and relocation during the growing-finishing period","volume":"105","author":"Coutellier","year":"2007","journal-title":"Appl. Anim. Behav. Sci."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1111\/j.1365-2982.2010.01664.x","article-title":"The microbiome-gut-brain axis: From bowel to behavior","volume":"23","author":"Cryan","year":"2011","journal-title":"Neurogastroenterol. Motil."},{"key":"ref23","first-page":"237","article-title":"Sow mortality associated with high ambient temperatures","volume":"37","author":"D\u2019Allaire","year":"1996","journal-title":"Can. Vet. J."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/S0168-1591(02)00077-1","article-title":"Individual aggressiveness measured in a resident-intruder test predicts the persistence of aggressive behaviour and weight gain of young pigs after mixing","volume":"77","author":"D\u2019Eath","year":"2002","journal-title":"Appl. Anim. Behav. Sci."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1016\/j.applanim.2015.02.015","article-title":"Analysis of the phenotypic link between behavioural traits at mixing and increased long-term social stability in group-housed pigs","volume":"166","author":"Desire","year":"","journal-title":"Appl. Anim. Behav. Sci."},{"key":"ref9002","doi-asserted-by":"publisher","first-page":"3303","DOI":"10.2527\/jas.2014-8823","article-title":"Genetic associations of short- and long-term aggressiveness identified by skin lesion with growth, feed efficiency, and carcass characteristics in growing pigs","volume":"93","author":"Desire","year":"","journal-title":"J. Anim. Sci."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"2039","DOI":"10.1038\/s41396-018-0148-3","article-title":"Fermentative Spirochaetes mediate necromass recycling in anoxic hydrocarbon-contaminated habitats","volume":"12","author":"Dong","year":"2018","journal-title":"ISME J."},{"key":"ref27","first-page":"1214","article-title":"Description of Alloprevotella rava gen. nov., sp. nov., isolated from the human oral cavity, and reclassification of Prevotella tannerae Moore et al. 1994 as Alloprevotella tannerae gen. nov., comb. nov","volume-title":"Int. J. Syst. Evol. Microbiol.","author":"Downes","year":"2013"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"5810","DOI":"10.1128\/AEM.70.10.5810","article-title":"Lactate-utilizing bacteria, isolated from human feces, that produce","volume":"70","author":"Duncan","year":"2004","journal-title":"Appl. Environ. Microbiol."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"2799","DOI":"10.1099\/ijs.0.65730-0","article-title":"Butyricicoccus pullicaecorum gen. nov., sp. nov., an anaerobic, butyrate-producing bacterium isolated from the caecal content of a broiler chicken","volume":"58","author":"Eeckhaut","year":"2008","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"e05500","DOI":"10.2903\/j.efsa.2018.5500","article-title":"The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017","volume":"16","year":"2018","journal-title":"EFSA J."},{"key":"ref31","first-page":"105","volume-title":"Analysis of the costs and benefits of setting certain control measures for reduction of Campylobacter in broiler meat at different stages of the food chain","author":"Elliott","year":"2012"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.rvsc.2015.07.013","article-title":"Changes in saliva biomarkers of stress and immunity in domestic pigs exposed to a psychosocial stressor","volume":"102","author":"Escribano","year":"2015","journal-title":"Res. Vet. Sci."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"239","DOI":"10.9758\/cpn.2015.13.3.239","article-title":"The gut-brain axis: The missing link in depression","volume":"13","author":"Evrensel","year":"2015","journal-title":"Clin. Psychopharmacol. Neurosci."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"e67019","DOI":"10.1371\/journal.pone.0067019","article-title":"ANOVA-like differential expression (ALDEx) analysis for mixed population RNA-Seq","volume":"8","author":"Fernandes","year":"2013","journal-title":"PLoS One"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1186\/2049-2618-2-15","article-title":"Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis","volume":"2","author":"Fernandes","year":"2014","journal-title":"Microbiome"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"e0205122","DOI":"10.1371\/journal.pone.0205122","article-title":"Social network properties predict chronic aggression in commercial pig systems","volume":"13","author":"Foister","year":"2018","journal-title":"PLoS One"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"429","DOI":"10.1111\/j.1863-2378.2008.01185.x","article-title":"Prevalence and risk factors for bacterial food-borne zoonotic hazards in slaughter pigs: a review","volume":"56","author":"Fosse","year":"2009","journal-title":"Zoonoses Public Health"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"2064","DOI":"10.1038\/s41564-019-0540-4","article-title":"Intestinal serotonin and fluoxetine exposure modulate bacterial colonization in the gut","volume":"4","author":"Fung","year":"2019","journal-title":"Nat. Microbiol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1016\/S0168-1591(98)00141-5","article-title":"How does former acquaintance affect aggressive behaviour in repeatedly mixed male and female pigs?","volume":"59","author":"Giersing","year":"1998","journal-title":"Appl. Anim. Behav. Sci."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fnbeh.2018.00064","article-title":"Psychosocial stress and immunity\u2014what can we learn from pig studies?","volume":"12","author":"Gimsa","year":"2018","journal-title":"Front. Behav. Neurosci."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1016\/j.livsci.2017.03.021","article-title":"Influence of loading handling and facilities on the subsequent response to pre-slaughter stress in pigs","volume":"200","author":"Goumon","year":"2017","journal-title":"Livest. Sci."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"3699","DOI":"10.1093\/jas\/skz245","article-title":"Genotype by environment interactions for performance and thermoregulation responses in growing pigs","volume":"97","author":"Gourdine","year":"2019","journal-title":"J. Anim. Sci."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"55","DOI":"10.3109\/00365528709095851","article-title":"The pig as a model in dietary fibre digestion studies","volume":"22","author":"Graham","year":"1987","journal-title":"Scand. J. Gastroenterol."},{"key":"ref44","doi-asserted-by":"crossref","DOI":"10.1201\/9780429455537","volume-title":"Compositional Data Analysis in Practice","author":"Greenacre","year":"2018"},{"key":"ref45","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fphys.2011.00094","article-title":"Brain-gut-microbe communication in health and disease","author":"Grenham","year":"2011","journal-title":"Front. Physiol."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s40104-018-0269-6","article-title":"The dynamics of the piglet gut microbiome during the weaning transition in association with health and nutrition","volume":"9","author":"Guevarra","year":"2018","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1111\/j.1365-2036.2007.03562.x","article-title":"Review article: the role of butyrate on colonic function","volume":"27","author":"Hamer","year":"2007","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"e1001923","DOI":"10.1371\/journal.pmed.1001923","article-title":"World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010","volume":"12","author":"Havelaar","year":"2015","journal-title":"PLoS Med."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"350","DOI":"10.3109\/07853890109002089","article-title":"The RAND-36 measure of health-related quality of life","volume":"33","author":"Hays","year":"2001","journal-title":"Ann. Med."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1017\/S0954422413000152","article-title":"Use of pigs as a potential model for research into dietary modulation of the human gut microbiota","volume":"26","author":"Heinritz","year":"2013","journal-title":"Nutr. Res. Rev."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0154329","article-title":"Intestinal microbiota and microbial metabolites are changed in a pig model fed a high-fat\/low-fiber or a low-fat\/high-fiber diet","volume":"11","author":"Heinritz","year":"2016","journal-title":"PLoS One"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"474","DOI":"10.2527\/1998.762474x","article-title":"Behavioral, endocrine, immune, and performance measures for pigs exposed to acute stress","volume":"76","author":"Hicks","year":"1998","journal-title":"J. Anim. Sci."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"1706","DOI":"10.3389\/fmicb.2016.01706","article-title":"Mucosal prevalence and interactions with the epithelium indicate commensalism of Sutterella spp","volume":"7","author":"Hiippala","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1038\/s41575-019-0227-6","article-title":"Building community in the gut: a role for mucosal serotonin","volume":"17","author":"Hoffman","year":"2020","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"e00004","DOI":"10.1128\/mSystems.00004-17","article-title":"Meta-analysis to define a core microbiota in the swine gut","volume":"2","author":"Holman","year":"2017","journal-title":"mSystems"},{"key":"ref56","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1016\/j.anaerobe.2004.01.004","article-title":"Subdoligranulum variabile gen. nov., sp. nov. from human feces","volume":"10","author":"Holmstr\u00f8m","year":"2004","journal-title":"Anaerobe"},{"key":"ref57","doi-asserted-by":"publisher","first-page":"855","DOI":"10.3389\/fpsyt.2020.00855","article-title":"The gut microbiota and associated metabolites are altered in sleep disorder of children with autism spectrum disorders","volume":"11","author":"Hua","year":"2020","journal-title":"Front. Psych."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"3329","DOI":"10.2147\/NDT.S188340","article-title":"Possible association of firmicutes in the gut microbiota of patients with major depressive disorder","volume":"14","author":"Huang","year":"2018","journal-title":"Neuropsychiatr. Dis. Treat."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"2771","DOI":"10.2527\/1998.76112771x","article-title":"Effects of feeder type, space allowance, and mixing on the growth performance and feed intake pattern of growing pigs","volume":"76","author":"Hyun","year":"1998","journal-title":"J. Anim. Sci."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1016\/j.applanim.2010.02.001","article-title":"\u201cSubordination style\u201d in pigs? The response of pregnant sows to mixing stress affects their offspring\u2019s behaviour and stress reactivity","volume":"124","author":"Ison","year":"2010","journal-title":"Appl. Anim. Behav. Sci."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-018-05184-7","article-title":"Gut microbiota associations with common diseases and prescription medications in a population-based cohort","volume":"9","author":"Jackson","year":"2018","journal-title":"Nat. Commun."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/j.yhbeh.2005.05.004","article-title":"Programming the offspring of the pig by prenatal social stress: Neuroendocrine activity and behaviour","volume":"49","author":"Jarvis","year":"2006","journal-title":"Horm. Behav."},{"key":"ref63","doi-asserted-by":"publisher","first-page":"186","DOI":"10.1016\/j.bbi.2015.03.016","article-title":"Altered fecal microbiota composition in patients with major depressive disorder","volume":"48","author":"Jiang","year":"2015","journal-title":"Brain Behav. Immun."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fnins.2019.01184","article-title":"Analysis of the gut microflora in patients with Parkinson\u2019s disease","volume":"13","author":"Jin","year":"2019","journal-title":"Front. Neurosci."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1016\/j.jpsychires.2016.07.019","article-title":"Transferring the blues: Depression-associated gut microbiota induces neurobehavioural changes in the rat","volume":"82","author":"Kelly","year":"2016","journal-title":"J. Psychiatr. Res."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"375","DOI":"10.1146\/annurev.med.49.1.375","article-title":"Clostridium difficile infection","volume":"49","author":"Kelly","year":"1998","journal-title":"Annu. Rev. 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Nutr."},{"key":"ref88","doi-asserted-by":"publisher","first-page":"109951","DOI":"10.1016\/j.pnpbp.2020.109951","article-title":"The HPA axis dysregulation in severe mental illness: Can we shift the blame to gut microbiota?","volume":"102","author":"Misiak","year":"2020","journal-title":"Prog. Neuro-Psychopharmacol. Biol. Psychiatry"},{"key":"ref89","doi-asserted-by":"publisher","first-page":"4147","DOI":"10.1099\/ijs.0.068148-0","article-title":"Sphaerochaeta multiformis sp. nov., an anaerobic, psychrophilic bacterium isolated from subseafloor sediment, and emended description of the genus Sphaerochaeta","volume":"64","author":"Miyazaki","year":"2014","journal-title":"Int. J. Syst. Evol. 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Stat."},{"key":"ref93","doi-asserted-by":"publisher","first-page":"277","DOI":"10.3389\/fimmu.2019.00277","article-title":"Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases","volume":"10","author":"Parada Venegas","year":"2019","journal-title":"Front. Immunol."},{"key":"ref94","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/j.livprodsci.2005.01.012","article-title":"Nutritional and physiological responses of growing pigs exposed to a diurnal pattern of heat stress","volume":"96","author":"Patience","year":"2005","journal-title":"Livest. Prod. Sci."},{"key":"ref95","doi-asserted-by":"publisher","first-page":"216","DOI":"10.2527\/2005.831216x","article-title":"Effects of castration, tooth resection, or tail docking on plasma metabolites and stress hormones in young pigs","volume":"83","author":"Prunier","year":"2005","journal-title":"J. Anim. Sci."},{"key":"ref96","doi-asserted-by":"publisher","first-page":"922","DOI":"10.2527\/jas1981.534922x","article-title":"Effects of group size and space allowance on performance and behavior of swine","volume":"53","author":"Randolph","year":"1981","journal-title":"J. Anim. Sci."},{"key":"ref97","doi-asserted-by":"publisher","first-page":"210","DOI":"10.1099\/ijs.0.023986-0","article-title":"Sphaerochaeta globosa gen. nov., sp. nov. and sphaerochaeta pleomorpha sp. nov., free-living, spherical spirochaetes","volume":"62","author":"Ritalahti","year":"2011","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref98","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1111\/1755-0998.13116","article-title":"pime: A package for discovery of novel differences among microbial communities","volume":"20","author":"Roesch","year":"2020","journal-title":"Mol. Ecol. Resour."},{"key":"ref99","doi-asserted-by":"publisher","first-page":"e1005752","DOI":"10.1371\/journal.pcbi.1005752","article-title":"mixOmics: An R package for \u2018omics feature selection and multiple data integration","volume":"13","author":"Rohart","year":"2017","journal-title":"PLoS Comput. Biol."},{"key":"ref100","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fvets.2022.834598","article-title":"Porcine models of the intestinal microbiota: the translational key to understanding how gut commensals contribute to gastrointestinal disease","volume":"9","author":"Rose","year":"2022","journal-title":"Front. Vet. Sci."},{"key":"ref101","doi-asserted-by":"publisher","first-page":"768","DOI":"10.1099\/ijsem.0.000788","article-title":"Reclassification of Eubacterium rectale (Hauduroy et al. 1937) pr\u00e9vot 1938 in a new genus agathobacter gen. nov. as Agathobacter rectalis comb. nov., and description of Agathobacter ruminis sp. nov., isolated from the rumen contents of sheep and cows","volume":"66","author":"Rosero","year":"2016","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref102","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1017\/S0954422416000020","article-title":"Critical review evaluating the pig as a model for human nutritional physiology","volume":"29","author":"Roura","year":"2016","journal-title":"Nutr. Res. 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Neurosci."},{"key":"ref109","doi-asserted-by":"publisher","first-page":"528","DOI":"10.1177\/104063870501700602","article-title":"Clostridial enteric infections in pigs","volume":"17","author":"Songer","year":"2005","journal-title":"J. Vet. Diagnostic Investig."},{"key":"ref110","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.fgb.2019.04.007","article-title":"The role of fungi in C. difficile infection: An underappreciated transkingdom interaction","volume":"129","author":"Stewart","year":"2019","journal-title":"Fungal Genet. Biol."},{"key":"ref111","doi-asserted-by":"publisher","first-page":"1260","DOI":"10.7150\/ijms.37322","article-title":"Fluoxetine ameliorates dysbiosis in a depression model induced by chronic unpredicted mild stress in mice","volume":"16","author":"Sun","year":"2019","journal-title":"Int. J. Med. Sci."},{"key":"ref112","doi-asserted-by":"crossref","DOI":"10.1002\/9781118960608.gbm01639","article-title":"Fusicatenibacter","volume-title":"Bergeys Manual of Systematics of Archaea and Bacteria","author":"Takada","year":"2019"},{"key":"ref113","doi-asserted-by":"publisher","first-page":"742","DOI":"10.1038\/s41437-018-0176-9","article-title":"Enhancing genetic disease control by selecting for lower host infectivity and susceptibility","volume":"122","author":"Tsairidou","year":"2019","journal-title":"Heredity (Edinb)."},{"key":"ref114","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3205\/000090","article-title":"Human intestinal spirochetosis-a review","volume":"8","author":"Tsinganou","year":"2010","journal-title":"Ger. Med. Sci."},{"key":"ref115","doi-asserted-by":"publisher","first-page":"454","DOI":"10.1111\/j.1740-0929.2006.00372.x","article-title":"Stimulation of butyrate production through the metabolic interaction among lactic acid bacteria, Lactobacillus acidophilus, and lactic acid-utilizing bacteria, Megasphaera elsdenii, in porcine cecal digesta","volume":"77","author":"Tsukahara","year":"2006","journal-title":"Anim. Sci. J."},{"key":"ref116","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1016\/S0168-1591(01)00168-X","article-title":"Effect of social group size on aggressive behaviour between unacquainted domestic pigs","volume":"74","author":"Turner","year":"2001","journal-title":"Appl. Anim. Behav. Sci."},{"key":"ref117","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1079\/ASC200678","article-title":"Heritability of post-mixing aggressiveness in grower-stage pigs and its relationship with production traits","volume":"82","author":"Turner","year":"2006","journal-title":"Anim. Sci."},{"key":"ref118","doi-asserted-by":"publisher","first-page":"623","DOI":"10.1038\/s41564-018-0337-x","article-title":"The neuroactive potential of the human gut microbiota in quality of life and depression","volume":"4","author":"Valles-Colomer","year":"2019","journal-title":"Nat. Microbiol."},{"key":"ref119","doi-asserted-by":"publisher","first-page":"286","DOI":"10.1093\/nutrit\/nuw067","article-title":"Role of short-chain fatty acids in colonic inflammation, carcinogenesis, and mucosal protection and healing","volume":"75","author":"van der Beek","year":"2017","journal-title":"Nutr. 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