The gut microbiota of warm-blooded vertebrates consists of bacterial species belonging to two main phyla; Firmicutes and Bacteroidetes. However, does it mean that the same bacterial species are found in humans and chickens? Here we show that the ability to survive in an aerobic environment is central for host species adaptation. Known bacterial species commonly found in humans, pigs, chickens and Antarctic gentoo penguins are those capable of extended survival under aerobic conditions, i.e., either spore-forming, aerotolerant or facultatively anaerobic bacteria. Such bacteria are ubiquitously distributed in the environment, which acts as the source of infection with similar probability in humans, pigs, chickens, penguins and likely any other warm-blooded omnivorous hosts. On the other hand, gut anaerobes with no specific adaptation for survival in an aerobic environment exhibit host adaptation. This is associated with their vertical transmission from mothers to offspring and long-term colonisation after administration of a single dose. This knowledge influences the design of next-generation probiotics. The origin of aerotolerant or spore-forming probiotic strains may not be that important. On the other hand, if Bacteroidetes and other host-adapted species are used as future probiotics, host preference should be considered.

Department of Experimental Biology Czech Collection of Microorganisms Faculty of Science Masaryk University 625 00 Brno Czech Republic

Medi Pharma Vision Ltd 612 00 Brno Czech Republic

Veterinary Research Institute 621 00 Brno Czech Republic

See more in PubMed

Karasova D., Crhanova M., Babak V., Jerabek M., Brzobohaty L., Matesova Z., Rychlik I. Development of piglet gut microbiota at the time of weaning influences development of postweaning diarrhea—A field study. Res. Vet. Sci. 2020;135:59–65. doi: 10.1016/j.rvsc.2020.12.022. PubMed DOI

Dominguez-Bello M.G., Costello E.K., Contreras M., Magris M., Hidalgo G., Fierer N., Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA. 2010;107:11971–11975. doi: 10.1073/pnas.1002601107. PubMed DOI PMC

Jakobsson H.E., Abrahamsson T.R., Jenmalm M.C., Harris K., Quince C., Jernberg C., Bjorksten B., Engstrand L., Andersson A.F. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut. 2014;63:559–566. doi: 10.1136/gutjnl-2012-303249. PubMed DOI

Kubasova T., Kollarcikova M., Crhanova M., Karasova D., Cejkova D., Sebkova A., Matiasovicova J., Faldynova M., Pokorna A., Cizek A., et al. Contact with adult hen affects development of caecal microbiota in newly hatched chicks. PLoS ONE. 2019;14:e0212446. doi: 10.1371/journal.pone.0212446. PubMed DOI PMC

Nowrouzian F., Hesselmar B., Saalman R., Strannegard I.L., Aberg N., Wold A.E., Adlerberth I. Escherichia coli in infants’ intestinal microflora: Colonization rate, strain turnover, and virulence gene carriage. Pediatr. Res. 2003;54:8–14. doi: 10.1203/01.PDR.0000069843.20655.EE. PubMed DOI

Videnska P., Sedlar K., Lukac M., Faldynova M., Gerzova L., Cejkova D., Sisak F., Rychlik I. Succession and replacement of bacterial populations in the caecum of egg laying hens over their whole life. PLoS ONE. 2014;9:e115142. doi: 10.1371/journal.pone.0115142. PubMed DOI PMC

Kubasova T., Kollarcikova M., Crhanova M., Karasova D., Cejkova D., Sebkova A., Matiasovicova J., Faldynova M., Sisak F., Babak V., et al. Gut anaerobes capable of chicken caecum colonisation. Microorganisms. 2019;7:597. doi: 10.3390/microorganisms7120597. PubMed DOI PMC

Avershina E., Larsen M.G., Aspholm M., Lindback T., Storro O., Oien T., Johnsen R., Rudi K. Culture dependent and independent analyses suggest a low level of sharing of endospore-forming species between mothers and their children. Sci. Rep. 2020;10:1832. doi: 10.1038/s41598-020-58858-y. PubMed DOI PMC

Rothschild D., Weissbrod O., Barkan E., Kurilshikov A., Korem T., Zeevi D., Costea P.I., Godneva A., Kalka I.N., Bar N., et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;555:210–215. doi: 10.1038/nature25973. PubMed DOI

Kearney S.M., Gibbons S.M., Poyet M., Gurry T., Bullock K., Allegretti J.R., Clish C.B., Alm E.J. Endospores and other lysis-resistant bacteria comprise a widely shared core community within the human microbiota. ISME J. 2018;12:2403–2416. doi: 10.1038/s41396-018-0192-z. PubMed DOI PMC

Kubasova T., Seidlerova Z., Rychlik I. Ecological adaptations of gut microbiota members and their consequences for use as a new generation of probiotics. Int. J. Mol. Sci. 2021;22:5471. doi: 10.3390/ijms22115471. PubMed DOI PMC

Medvecky M., Cejkova D., Polansky O., Karasova D., Kubasova T., Cizek A., Rychlik I. Whole genome sequencing and function prediction of 133 gut anaerobes isolated from chicken caecum in pure cultures. BMC Genom. 2018;19:561. doi: 10.1186/s12864-018-4959-4. PubMed DOI PMC

Crhanova M., Karasova D., Juricova H., Matiasovicova J., Jahodarova E., Kubasova T., Seidlerova Z., Cizek A., Rychlik I. Systematic culturomics shows that half of chicken caecal microbiota members can be grown in vitro except for two lineages of Clostridiales and a single lineage of Bacteroidetes. Microorganisms. 2019;7:496. doi: 10.3390/microorganisms7110496. PubMed DOI PMC

Forster S.C., Kumar N., Anonye B.O., Almeida A., Viciani E., Stares M.D., Dunn M., Mkandawire T.T., Zhu A., Shao Y., et al. A human gut bacterial genome and culture collection for improved metagenomic analyses. Nat. Biotechnol. 2019;37:186–192. doi: 10.1038/s41587-018-0009-7. PubMed DOI PMC

Browne H.P., Forster S.C., Anonye B.O., Kumar N., Neville B.A., Stares M.D., Goulding D., Lawley T.D. Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation. Nature. 2016;533:543–546. doi: 10.1038/nature17645. PubMed DOI PMC

Browne H.P., Almeida A., Kumar N., Vervier K., Adoum A.T., Viciani E., Dawson N.J.R., Forster S.C., Cormie C., Goulding D., et al. Host adaptation in gut Firmicutes is associated with sporulation loss and altered colonisation patterns. Genome Biol. 2021;22:204. doi: 10.1186/s13059-021-02428-6. PubMed DOI PMC

Browne H.P., Neville B.A., Forster S.C., Lawley T.D. Transmission of the gut microbiota: Spreading of health. Nat. Rev. Microbiol. 2017;15:531–543. doi: 10.1038/nrmicro.2017.50. PubMed DOI PMC

Reid G., Gaudier E., Guarner F., Huffnagle G.B., Macklaim J.M., Munoz A.M., Martini M., Ringel-Kulka T., Sartor B., Unal R., et al. Responders and non-responders to probiotic interventions: How can we improve the odds? Gut Microbes. 2010;1:200–204. doi: 10.4161/gmic.1.3.12013. PubMed DOI PMC

Nayfach S., Rodriguez-Mueller B., Garud N., Pollard K.S. An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography. Genome Res. 2016;26:1612–1625. doi: 10.1101/gr.201863.115. PubMed DOI PMC

Kollarcikova M., Faldynova M., Matiasovicova J., Jahodarova E., Kubasova T., Seidlerova Z., Babak V., Videnska P., Cizek A., Rychlik I. Different Bacteroides species colonise human and chicken intestinal tract. Microorganisms. 2020;8:1483. doi: 10.3390/microorganisms8101483. PubMed DOI PMC

O’Toole P.W., Marchesi J.R., Hill C. Next-generation probiotics: The spectrum from probiotics to live biotherapeutics. Nat. Microbiol. 2017;2:17057. doi: 10.1038/nmicrobiol.2017.57. PubMed DOI

Seidlerova Z., Kubasova T., Faldynova M., Crhanova M., Karasova D., Babak V., Rychlik I. Environmental impact on differential composition of gut microbiota in indoor chickens in commercial production and outdoor, backyard chickens. Microorganisms. 2020;8:767. doi: 10.3390/microorganisms8050767. PubMed DOI PMC

Kubasova T., Davidova-Gerzova L., Merlot E., Medvecky M., Polansky O., Gardan-Salmon D., Quesnel H., Rychlik I. Housing systems influence gut microbiota composition of sows but not of their piglets. PLoS ONE. 2017;12:e0170051. doi: 10.1371/journal.pone.0170051. PubMed DOI PMC

Kubasova T., Davidova-Gerzova L., Babak V., Cejkova D., Montagne L., Le-Floc’h N., Rychlik I. Effects of host genetics and environmental conditions on fecal microbiota composition of pigs. PLoS ONE. 2018;13:e0201901. doi: 10.1371/journal.pone.0201901. PubMed DOI PMC

Rychlik I. Composition and function of chicken gut microbiota. Animals. 2020;10:103. doi: 10.3390/ani10010103. PubMed DOI PMC

MM O.D., Harris H.M.B., Ross R.P., O’Toole P.W. Core fecal microbiota of domesticated herbivorous ruminant, hindgut fermenters, and monogastric animals. Microbiologyopen. 2017;6:e00509. doi: 10.1002/mbo3.509. PubMed DOI PMC

Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Pena A.G., Goodrich J.K., Gordon J.I., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods. 2010;7:335–336. doi: 10.1038/nmeth.f.303. PubMed DOI PMC

Dione N., Khelaifia S., La Scola B., Lagier J.C., Raoult D. A quasi-universal medium to break the aerobic/anaerobic bacterial culture dichotomy in clinical microbiology. Clin. Microbiol. Infect. 2016;22:53–58. doi: 10.1016/j.cmi.2015.10.032. PubMed DOI

Li S.S., Zhu A., Benes V., Costea P.I., Hercog R., Hildebrand F., Huerta-Cepas J., Nieuwdorp M., Salojarvi J., Voigt A.Y., et al. Durable coexistence of donor and recipient strains after fecal microbiota transplantation. Science. 2016;352:586–589. doi: 10.1126/science.aad8852. PubMed DOI

Li X., Liang S., Xia Z., Qu J., Liu H., Liu C., Yang H., Wang J., Madsen L., Hou Y., et al. Establishment of a Macaca fascicularis gut microbiome gene catalog and comparison with the human, pig, and mouse gut microbiomes. Gigascience. 2018;7:giy100. doi: 10.1093/gigascience/giy100. PubMed DOI PMC

Baquero F., Coque T.M., Galan J.C., Martinez J.L. The origin of niches and species in the bacterial world. Front. Microbiol. 2021;12:657986. doi: 10.3389/fmicb.2021.657986. PubMed DOI PMC

Tetz G., Tetz V. Introducing the sporobiota and sporobiome. Gut Pathog. 2017;9:38. doi: 10.1186/s13099-017-0187-8. PubMed DOI PMC

van Nood E., Vrieze A., Nieuwdorp M., Fuentes S., Zoetendal E.G., de Vos W.M., Visser C.E., Kuijper E.J., Bartelsman J.F., Tijssen J.G., et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med. 2013;368:407–415. doi: 10.1056/NEJMoa1205037. PubMed DOI

Khan M.T., Duncan S.H., Stams A.J., van Dijl J.M., Flint H.J., Harmsen H.J. The gut anaerobe Faecalibacterium prausnitzii uses an extracellular electron shuttle to grow at oxic-anoxic interphases. ISME J. 2012;6:1578–1585. doi: 10.1038/ismej.2012.5. PubMed DOI PMC

Tang Y.P., Dallas M.M., Malamy M.H. Characterization of the Batl (Bacteroides aerotolerance) operon in Bacteroides fragilis: Isolation of a B. fragilis mutant with reduced aerotolerance and impaired growth in in vivo model systems. Mol. Microbiol. 1999;32:139–149. doi: 10.1046/j.1365-2958.1999.01337.x. PubMed DOI

Volf J., Polansky O., Varmuzova K., Gerzova L., Sekelova Z., Faldynova M., Babak V., Medvecky M., Smith A.L., Kaspers B., et al. Transient and prolonged response of chicken cecum mucosa to colonization with different gut microbiota. PLoS ONE. 2016;11:e0163932. doi: 10.1371/journal.pone.0163932. PubMed DOI PMC

Probiotic Mixtures Consisting of Representatives of Bacteroidetes and Selenomonadales Increase Resistance of Newly Hatched Chicks to Salmonella Enteritidis Infection

Immunoglobulin secretion influences the composition of chicken caecal microbiota

In Vivo Expression of Chicken Gut Anaerobes Identifies Carbohydrate- or Amino Acid-Utilising, Motile or Type VI Secretion System-Expressing Bacteria

Research Note: A mixture of Bacteroides spp. and other probiotic intestinal anaerobes reduces colonization by pathogenic E. coli strain O78:H4-ST117 in newly hatched chickens