The acquisition of the infant gut microbiota is key to establishing a host-microbiota symbiosis. Microbially produced metabolites tightly interact with the immune system, and the fermentation-derived short-chain fatty acid butyrate is considered an important mediator linked to chronic diseases later in life. The intestinal butyrate-forming bacterial population is taxonomically and functionally diverse and includes endospore formers with high transmission potential. Succession, and contribution of butyrate-producing taxa during infant gut microbiota development have been little investigated. We determined the abundance of major butyrate-forming groups and fermentation metabolites in faeces, isolated, cultivated and characterized the heat-resistant cell population, which included endospores, and compared butyrate formation efficiency of representative taxa in batch cultures. The endospore community contributed about 0.001% to total cells, and was mainly composed of the pioneer butyrate-producing Clostridium sensu stricto. We observed an increase in abundance of Faecalibacterium prausnitzii, butyrate-producing Lachnospiraceae and faecal butyrate levels with age that is likely explained by higher butyrate production capacity of contributing taxa compared with Clostridium sensu stricto. Our data suggest that a successional arrangement and an overall increase in abundance of butyrate forming populations occur during the first year of life, which is associated with an increase of intestinal butyrate formation capacity.

Children's Hospital St Gallen St Gallen Switzerland

Christine Kühne Center for Allergy Research and Education Davos Switzerland

Department of Microbiology Nutrition and Dietetics Czech University of Life Sciences Prague Czech Republic

Division of Biological and Chemical Engineering Aarhus University Aarhus Denmark

Division of Respiratory Medicine Department of Paediatrics Inselspital University of Bern Bern Switzerland

Laboratory of Food Biotechnology Institute of Food Nutrition and Health ETH Zürich Zürich Switzerland

Laboratory of Toxicology Institute of Food Nutrition and Health ETH Zürich Zürich Switzerland

Swiss Institute of Allergy and Asthma Research University of Zürich Davos Switzerland

University Children's Hospital Zürich Zürich Switzerland

Zobrazit více v PubMed

Al-Hinai, M.A., Jones, S.W., and Papoutsakis, T. (2015) The Clostridium sporulation programs: diversity and preservation of endospore differentiation. Microbiol Mol Biol Rev 79: 19-37.

Arrieta, M.C., Stiemsma, L.T., Amenyogbe, N., Brown, E.M., and Finlay, B. (2014) The intestinal microbiome in early life: health and disease. Front Immunol 5: 427.

Avershina, E., Gro Larsen, M., Aspholm, M., Lindback, T., Storrø, O., Øien, T., et al. (2020) Culture dependent and independent analyses suggest a low level of sharing of endospore-forming species between mothers and their children. Sci Rep 10: 1832.

Bäckhed, F., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kovatcheva-Datchary, P., et al. (2015) Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17: 690-703.

Bradley, C.R., and Fraise, A.P. (1996) Heat and chemical resistance of enterococci. J Hosp Infect 34: 191-196.

Browne, H.P., Forster, S.C., Anonye, B.O., Kumar, N., Neville, B.A., Stares, M.D., et al. (2016) Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation. Nature 533: 543-546.

Browne, H.P., Neville, B.A., Forster, S.C., and Lawley, T.D. (2017) Transmission of the gut microbiota: spreading of health. Nat Rev Microbiol 15: 531-543.

Bui, T.P., de Vos, W.M., and Plugge, C.M. (2014) Anaerostipes rhamnosivorans sp. nov., a human intestinal, butyrate-forming bacterium. Int J Syst Evol Microbiol 64: 787-793.

Cait, A., Cardenas, E., Dimitru, P.A., Amenyogbe, N., Dai, D., Cait, J., et al. (2019) Reduced genetic potential for butyrate fermentation in the gut microbiome of infants who develop allergic sensitization. J Allergy Clin Immunol 144: 1638-1647.

Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., and Holmes, S.P. (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13: 581-583.

Didion, J.P., Martin, M., and Collins, F.S. (2017) Atropos: specific, sensitive, and speedy trimming of sequencing reads. J PeerJ 5: e3720.

Duncan, S.H., Barcenilla, A., Stewart, C.S., Pryde, S.E., and Flint, H.J. (2002) Acetate utilization and butyryl coenzyme A (CoA):acetate-CoA transferase in butyrate-producing bacteria from the human intestine. Appl Environ Microbiol 68: 5186-5190.

Ferraris, L., Butel, M.J., Campeotto, F., Vodovar, M., Rozé, J.C., and Aires, J. (2012) Clostridia in premature neonates' gut: incidence, antibiotic susceptibility, and perinatal determinants influencing colonization. PLoS One 7: e30594.

Ferretti, P., Pasolli, E., Tett, A., Asnicar, F., Gorfer, V., Fedi, S., et al. (2018) Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe 11: 133-145.

Flint, H.J., Scott, K.P., Duncan, S.H., Louis, P., and Forano, E. (2012) Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3: 289-306.

Galperin, M.Y. (2013) Genome diversity of spore-forming Firmicutes. Microbiol Spec 1: TBS-0015-2012.

Ghoddusi, H.B., and Sherburn, R. (2010) Preliminary study on the isolation of Clostridium butyricum strains from natural sources in the UKand screening the isolates for presence of the type E botulinal toxin gene. Int J Food Microbiol 142: 202-206.

Glöckner, F.O., Yilmaz, P., Quast, C., Gerken, J., Beccati, A., Ciuprona, A., et al. (2017) 25 years of serving the community with ribosomal RNA gene reference databases and tool. J Biotechnol 261: 169-176.

Harmon, S.M., Kautter, D.A., and Hatheway, C.L. (1986) Enumeration and characterization of Clostridium perfringens spores in the feces of food poisoning patients and normal controls. J Food Protect 49: 23-28.

Jian, C., Luukkonen, P., Yki-Järvinen, H., Salonen, A., and Korpela, K. (2020) Quantitative PCR provides a simple and accessible method for quantitative microbiota profiling. PLoS One 15: e0227285.

Jost, T., Lacroix, C., Braegger, C.P., and Chassard, C. (2012) New insights in gut microbiota establishment in healthy breast fed neonates. PLoS One 7: e4495.

Jost, T., Lacroix, C., Braegger, C.P., Rochat, F., and Chassard, C. (2014) Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ Microbiol 6: 2891-2904.

Kearney, S.M., Gibbons, S.M., Poyet, M., Gurry, T., Bullock, K., Allegretti, J.R., et al. (2018) Endospores and other lysis-resistant bacteria comprise a widely shared core community within the human microbiota. ISME J 12: 2403-2416.

Korpela, K., Costea, P., Coelho, L.P., Kandels-Lewis, S., Willemsen, G., Boomsma, D.I., et al. (2018) Selective maternal seeding and environment shape the human gut microbiome. Genome Res 28: 561-568.

Lawson, M.A.E., O'Neill, I.J., Kujawska, M., Javvadi, S.G., Wijeyesekera, A., Flegg, Z., et al. (2020) Breast milk-derived human milk oligosaccharides promote Bifidobacterium interactions within a single ecosystem. ISME J 14: 635-648.

Li, H., and Gänzle, M.G. (2016) Some like it hot: resistance of Escherichia coli in food. Front Microbiol 7: 1763.

Lister, M., Stevenson, E., Heeg, D., Minton, N.P., and Kuehne, S.A. (2014) Comparison of culture based methods for the isolation of Clostridium difficile from stool samples in a research setting. Anaerobe 28: 226-229.

Lopez-Siles, M., Khan, T.M., Duncan, S.H., Harmsen, H.J., Garcia-Gil, L.J., and Flint, H.J. (2012) Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrates for growth. Appl Environ Microbiol 78: 420-428.

Louis, P., Duncan, S.H., McCrae, S.I., Millar, J., Jackson, M.S., and Flint, H.J. (2004) Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J Bacteriol 186: 2099-2106.

Louis, P., and Flint, H.J. (2017) Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol 19: 29-41.

Modrackova, N., Makovska, M., Mekadim, C., Vlkova, E., Tejnecky, V., Bolechova, P., and Bunesova, V. (2019) Prebiotic potential of natural gums and starch for bifidobacteria of variable origins. Bioact Carbohydr Diet Fibre 20: 100199.

Mountzouris, K.C., McCartney, A.L., and Gibson, G.R. (2002) Intestinal microflora of human infants and current trends for nutritional modulation. Br J Nutr 87: 405-420.

Mukhopadhya, I., Moraïs, S., Laverde-Gomez, J., Sheridan, P.O., Walker, A.W., Kelly, W., et al. (2018) Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch-degrader Ruminococcus bromii. Environ Microbiol 20: 324-336.

Nayfach, S., Rodriquez-Mueller, B., Garud, B., and Pollard, K.S. (2016) An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography. Genome Res 26: 1-14.

Pham, V.T., Lacroix, C., Braegger, C.P., and Chassard, C. (2016) Early colonization of functional groups of microbes in the infant gut. Environ Microbiol 18: 2246-2258.

Raveh-Sedka, T., Firek, B., Sharon, I., Baker, R., Brown, C.T., Thomas, B.C., et al. (2016) Evidence for persistent and shared bacterial strains against a background of largely unique gut colonization in hospitalized premature infants. ISME J 10: 2817-2830.

Roduit, C., Frei, R., Ferstl, R., Loeliger, S., Westermann, P., Rhyner, C., et al. (2019) High levels of butyrate and propionate in early life are associated with protection against atopy. Allergy 74: 799-809.

Rooks, M.G., and Garrett, W.S. (2016) Gut microbiota, metabolites and host immunity. Nat Rev Immunol 16: 341-352.

Sandin, A., Braback, L., Norin, E., and Bjorksten, B. (2009) Faecal short chain fatty acid pattern and allergy in early childhood. Acta Paediatr 98: 823-827.

Schwab, C., Ruscheweyh, H.-J., Bunesova, V., Pham, V.T., Beerenwinkel, N., and Lacroix, C. (2017) Trophic interactions of infant bifidobacteria and Eubacterium hallii during L-fucose and fucosyllactose degradation. Front Microbiol 8: 95.

Scott, K.P., Martin, J.C., Duncan, S.H., and Flint, H.J. (2014) Prebiotic stimulation of human colonic butyrate-producing bacteria and bifidobacteria in vitro. FEMS Microbiol Ecol 87: 30-40.

Slobodkin, A. (2014) The family Peptostreptococcaceae. In The Prokaryotes: Firmicutes and Tenericutes, Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., and Thompson, F. (eds). Switzerland: Springer Nature, pp. 291-302.

Stoddard, S.F., Smith, B.J., Hein, R., Roller, B.R.K., and Schmidt, T.M. (2015) rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acid Res 43: D593-D598.

Trompette, A., Gollwitzer, E.S., Yadava, K., Sichelstiel, A.K., Sprenger, N., Ngom-Bru, C., et al. (2014) Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 20: 159-166.

Vital, M., Howe, A.C., and Tiedje, J.M. (2014) Revealing the bacterial butyrate synthesis pathways by analyzing (meta) genomic data. MBio 5: e00889-00814.

Vital, M., Karch, A., and Pieper, D.H. (2017) Colonic butyrate-producing communities in humans: an overview using omics data. mSystems 2: e00130-00117.

Vital, M., Penton, C.R., Wang, Q., Young, V.B., Antonopoulos, D.A., Sogin, M.L., et al. (2013) A gene-targeted approach to investigate the intestinal butyrate-producing bacterial community. Microbiome 1: 8.

Vlkova, E., Nevoral, J., Jencikova, B., Kopecny, J., Godefrooij, J., Trojanová, I., and Rada, V. (2005) Detection of infant faecal bifidobacterial by enzymatic methods. J Microbiol Methods 60: 365-373.

Wiegel, J., Tanner, R., and Rainey, F.A. (2006) An introduction to the family Clostridiaceae. In The Prokaryotes, Falkow, S., Rosenberg, E., Schleifer, K.-H., and Stackebrandt, E. (eds). New York, USA: Springer, pp. 654-678.

Zhang, J., Lacroix, C., and Wortmann, E. (2019). Gut microbial beta-glucuronidase and glycerol/diol dehydratase activity contribute to dietary heterocyclic amine biotransformation. BMC Microbiol 19: 99. https://doi.org/10.1186/s12866-019-1483-x.

Culture-dependent screening of endospore-forming clostridia in infant feces

Breastfeeding and the major fermentation metabolite lactate determine occurrence of Peptostreptococcaceae in infant feces