Exploring Bifidobacterium species community and functional variations with human gut microbiome structure and health beyond infancy

Ruben Ladeira , Julien Tap , Muriel Derrien

Microbiome Research Reports ›› 2023, Vol. 2 ›› Issue (2) : 9

PDF
Microbiome Research Reports ›› 2023, Vol. 2 ›› Issue (2) :9 DOI: 10.20517/mrr.2023.01
Original Article

Exploring Bifidobacterium species community and functional variations with human gut microbiome structure and health beyond infancy

Author information +
History +
PDF

Abstract

Aim: The human gut Bifidobacterium community has been studied in detail in infants and following dietary interventions in adults. However, the variability of the distribution of Bifidobacterium species and intra-species functions have been little studied, particularly beyond infancy. Here, we explore the ecology of Bifidobacterium communities in a large public dataset of human gut metagenomes, mostly corresponding to adults.

Methods: We selected 9.515 unique gut metagenomes from curatedMetagenomicData. Samples were partitioned by applying Dirichlet’s multinomial mixture to Bifidobacterium species. A functional analysis was performed on > 2.000 human-associated Bifidobacterium metagenome-assembled genomes (MAGs) paired with participant gut microbiome and health features.

Results: We identified several Bifidobacterium-based partitions in the human gut microbiome differing in terms of the presence and abundance of Bifidobacterium species. The partitions enriched in both B. longum and B. adolescentis were associated with gut microbiome diversity and a higher abundance of butyrate producers and were more prevalent in healthy individuals. B. bifidum MAGs harboring a set of genes potentially related to phages were more prevalent in partitions associated with a lower gut microbiome diversity and were genetically more closely related.

Conclusion: This study expands our knowledge of the ecology and variability of the Bifidobacterium community, particularly in adults, and its specific association with the gut microbiota and health. Its findings may guide the rational selection of Bifidobacterium strains for gut microbiome complementation according to the individual’s endogenous Bifidobacterium community. Our results also suggest that gut microbiome stratification for particular genera may be relevant for studies of variations of species and associations with the gut microbiome and health.

Keywords

Human gut microbiome / Bifidobacterium longum / Bifidobacterium adolescentis / partitions / function / MAGs / health

Cite this article

Download citation ▾
Ruben Ladeira, Julien Tap, Muriel Derrien. Exploring Bifidobacterium species community and functional variations with human gut microbiome structure and health beyond infancy. Microbiome Research Reports, 2023, 2(2): 9 DOI:10.20517/mrr.2023.01

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

O'Neill I,Hall LJ.Exploring the role of the microbiota member Bifidobacterium in modulating immune-linked diseases.Emerg Top Life Sci2017;1:333-49 PMCID:PMC7288987

[2]

Pokusaeva K,van Sinderen D.Carbohydrate metabolism in Bifidobacteria.Genes Nutr2011;6:285-306 PMCID:PMC3145055

[3]

Rossi M,Raimondi S.Folate production by probiotic bacteria.Nutrients2011;3:118-34 PMCID:PMC3257725

[4]

Sakurai T,Xiao JZ.Production of indole-3-lactic acid by bifidobacterium strains isolated fromhuman infants.Microorganisms2019;7:340 PMCID:PMC6780619

[5]

Duranti S,Lugli GA.Bifidobacterium adolescentis as a key member of the human gut microbiota in the production of GABA.Sci Rep2020;10:14112 PMCID:PMC7445748

[6]

Zeng S,Almeida A.A compendium of 32,277 metagenome-assembled genomes and over 80 million genes from the early-life human gut microbiome.Nat Commun2022;13:5139 PMCID:PMC9437082

[7]

Derrien M,de Vos WM.The gut microbiota in the first decade of life.Trends Microbiol2019;27:997-1010

[8]

Derrien M,Uyoga MA.Gut microbiome function and composition in infants from rural Kenya and association with human milk oligosaccharides.Gut Microbes2023;15:2178793 PMCID:PMC9980514

[9]

Matsuki T,Tanaka R,Oyaizu H.Distribution of bifidobacterial species in human intestinal microflora examined with 16S rRNA-gene-targeted species-specific primers.Appl Environ Microbiol1999;65:4506-12 PMCID:PMC91600

[10]

Derrien M,Ventura M.Insights into endogenous Bifidobacterium species in the human gut microbiota during adulthood.Trends Microbiol2022;30:940-7

[11]

Bolte LA,Imhann F.Long-term dietary patterns are associated with pro-inflammatory and anti-inflammatory features of the gut microbiome.Gut2021;70:1287-98 PMCID:PMC8223641

[12]

Asnicar F,Valdes AM.Microbiome connections with host metabolism and habitual diet from 1,098 deeply phenotyped individuals.Nat Med2021;27:321-32 PMCID:PMC8353542

[13]

Nayfach S,Seshadri R,Kyrpides NC.New insights from uncultivated genomes of the global human gut microbiome.Nature2019;568:505-10 PMCID:PMC6784871

[14]

Parks DH,Chuvochina M.Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life.Nat Microbiol2017;2:1533-42

[15]

Almeida A,Boland M.A new genomic blueprint of the human gut microbiota.Nature2019;568:499-504 PMCID:PMC6784870

[16]

Pasolli E,Manara S.Extensive unexplored human microbiome diversity revealed by over 150,000 genomes from metagenomes spanning age, geography, and lifestyle.Cell2019;176:649-662.e20 PMCID:PMC6349461

[17]

Leviatan S,Rothschild D,Segal E.An expanded reference map of the human gut microbiome reveals hundreds of previously unknown species.Nat Commun2022;13:3863 PMCID:PMC9256738

[18]

Zhernakova A,Bonder MJ.Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity.Science2016;352:565-9 PMCID:PMC5240844

[19]

Filippis F, Pasolli E, Ercolini D. Newly explored faecalibacterium diversity is connected to age, lifestyle, geography, and disease.Curr Biol2020;30:4932-4943.e4

[20]

Karcher N,Punčochář M.Genomic diversity and ecology of human-associated Akkermansia species in the gut microbiome revealed by extensive metagenomic assembly.Genome Biol2021;22:209 PMCID:PMC8278651

[21]

Tett A,Asnicar F.The prevotella copri complex comprises four distinct clades underrepresented in westernized populations.Cell Host Microbe2019;26:666-679.e7 PMCID:PMC6854460

[22]

Hidalgo-Cantabrana C,Ruiz L,Sánchez B.Bifidobacteria and their health-promoting effects.Microbiol Spectr2017;5

[23]

Sarkar A.Bifidobacteria-Insight into clinical outcomes and mechanisms of its probiotic action.Microbiol Res2016;192:159-71

[24]

Holmes I,Quince C.Dirichlet multinomial mixtures: generative models for microbial metagenomics.PLoS One2012;7:e30126 PMCID:PMC3272020

[25]

Huerta-Cepas J,Heller D.EggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses.Nucleic Acids Res2019;47:D309-14

[26]

Yin Y,Yang J,Mao F.dbCAN: a web resource for automated carbohydrate-active enzyme annotation.Nucleic Acids Res2012;40:W445-51 PMCID:PMC3394287

[27]

Odamaki T,Kato K.Genomic diversity and distribution of Bifidobacterium longum subsp. longum across the human lifespan.Sci Rep2018;8:85 PMCID:PMC5758520

[28]

Schnorr SL,Rampelli S.Gut microbiome of the Hadza hunter-gatherers.Nat Commun2014;5:3654

[29]

Gupta VK,Bakshi U.A predictive index for health status using species-level gut microbiome profiling.Nat Commun2020;11:4635 PMCID:PMC7492273

[30]

Gacesa R,Vich Vila A.Environmental factors shaping the gut microbiome in a Dutch population.Nature2022;604:732-9

[31]

FitzGerald J,Eckenberger J.Improved gut microbiome recovery following drug therapy is linked to abundance and replication of probiotic strains.Gut Microbes2022;14:2094664 PMCID:PMC9348039

[32]

Palleja A,Forslund SK.Recovery of gut microbiota of healthy adults following antibiotic exposure.Nat Microbiol2018;3:1255-65

[33]

Mangin I,Magne F,Pochart P.Long-term changes in human colonic Bifidobacterium populations induced by a 5-day oral amoxicillin-clavulanic acid treatment.PLoS One2012;7:e50257 PMCID:PMC3507739

[34]

Liu Z,Gerritsen J,Zoetendal EG.Microbiome-based stratification to guide dietary interventions to improve human health.Nutr Res2020;82:1-10

[35]

Feng W,Ao H,Peng C.Targeting gut microbiota for precision medicine: focusing on the efficacy and toxicity of drugs.Theranostics2020;10:11278-301 PMCID:PMC7532689

[36]

Odamaki T,Sugahara H.Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study.BMC Microbiol2016;16:90 PMCID:PMC4879732

[37]

Costea PI,Arumugam M.Enterotypes in the landscape of gut microbial community composition.Nat Microbiol2018;3:8-16 PMCID:PMC5832044

[38]

Stewart CJ,O'Brien JL.Temporal development of the gut microbiome in early childhood from the TEDDY study.Nature2018;562:583-8 PMCID:PMC6415775

[39]

Beller L,Falony G.Successional stages in infant gut microbiota maturation.mBio2021;12:e0185721 PMCID:PMC8686833

[40]

Vieira-Silva S,Belda E.Statin therapy is associated with lower prevalence of gut microbiota dysbiosis.Nature2020;581:310-5

[41]

Ding T.Dynamics and associations of microbial community types across the human body.Nature2014;509:357-60 PMCID:PMC4139711

[42]

Roswall J,Kovatcheva-Datchary P.Developmental trajectory of the healthy human gut microbiota during the first 5 years of life.Cell Host Microbe2021;29:765-776.e3

[43]

Das P,Kovatcheva-Datchary P,Nielsen J.In vitro co-cultures of human gut bacterial species as predicted from co-occurrence network analysis.PLoS One2018;13:e0195161 PMCID:PMC5877883

[44]

Kato K,Mitsuyama E,Xiao JZ.Age-related changes in the composition of gut bifidobacterium species.Curr Microbiol2017;74:987-95 PMCID:PMC5486783

[45]

Abu-Ali GS,Lloyd-Price J.Metatranscriptome of human faecal microbial communities in a cohort of adult men.Nat Microbiol2018;3:356-66 PMCID:PMC6557121

[46]

Hansen LBS,Søndertoft NB.A low-gluten diet induces changes in the intestinal microbiome of healthy Danish adults.Nat Commun2018;9:4630 PMCID:PMC6234216

[47]

Nagara Y,Takada T,Odani T.Selective induction of human gut-associated acetogenic/butyrogenic microbiota based on specific microbial colonization of indigestible starch granules.ISME J2022;16:1502-11 PMCID:PMC9123178

[48]

Avershina E,Øien T.Bifidobacterial succession and correlation networks in a large unselected cohort of mothers and their children.Appl Environ Microbiol2013;79:497-507 PMCID:PMC3553782

[49]

Gotoh A,Sakanaka M.Sharing of human milk oligosaccharides degradants within bifidobacterial communities in faecal cultures supplemented with Bifidobacterium bifidum.Sci Rep2018;8:13958 PMCID:PMC6143587

[50]

Walsh C,van Sinderen D.Human milk oligosaccharide-sharing by a consortium of infant derived Bifidobacterium species.Sci Rep2022;12:4143 PMCID:PMC8907170

[51]

Lawson MAE,Kujawska M.Breast milk-derived human milk oligosaccharides promote Bifidobacterium interactions within a single ecosystem.ISME J2020;14:635-48 PMCID:PMC6976680

[52]

Belenguer A,Calder AG.Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut.Appl Environ Microbiol2006;72:3593-9 PMCID:PMC1472403

[53]

Rivière A,Weckx S,De Vuyst L.Mutual cross-feeding interactions between Bifidobacterium longum subsp. longum NCC2705 and Eubacterium rectale ATCC 33656 explain the bifidogenic and butyrogenic effects of arabinoxylan oligosaccharides.Appl Environ Microbiol2015;81:7767-81 PMCID:PMC4616955

[54]

Falony G,Verbrugghe K.Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose.Appl Environ Microbiol2006;72:7835-41 PMCID:PMC1694233

[55]

Le Roy CI,Leeming ER.Yoghurt consumption is associated with changes in the composition of the human gut microbiome and metabolome.BMC Microbiol2022;22:39

[56]

Derrien M.Fate, activity, and impact of ingested bacteria within the human gut microbiota.Trends Microbiol2015;23:354-66

[57]

Maldonado-Gómez MX,Bottacini F.Stable engraftment of bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome.Cell Host Microbe2016;20:515-26

[58]

Zhang C,Levenez F.Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes.ISME J2016;10:2235-45 PMCID:PMC4989305

[59]

Blanco G,Tamés H.Revisiting the metabolic capabilities of bifidobacterium longum susbp. longum and bifidobacterium longum subsp. infantis from a glycoside hydrolase perspective.Microorganisms2020;8:723 PMCID:PMC7285499

[60]

Katoh T,Sakanaka M,Gotoh A.Enzymatic adaptation of bifidobacterium bifidum to host glycans, viewed from glycoside hydrolyases and carbohydrate-binding modules.Microorganisms2020;8:481 PMCID:PMC7232152

[61]

Watanabe Y,Hara T.Xylan utilisation promotes adaptation of Bifidobacterium pseudocatenulatum to the human gastrointestinal tract.ISME COMMUN2021;1

[62]

Schöpping M,Jensen K,Zeidan AA.Genome-wide assessment of stress-associated genes in bifidobacteria.Appl Environ Microbiol2022;88:e0225121 PMCID:PMC9004370

[63]

Nishijima S,Kiguchi Y.Extensive gut virome variation and its associations with host and environmental factors in a population-level cohort.Nat Commun2022;13:5252 PMCID:PMC9448778

[64]

Schmidt V,Spector TD,Ley RE.Strain-level analysis of bifidobacterium spp. from gut microbiomes of adults with differing lactase persistence genotypes.mSystems2020;5 PMCID:PMC7527142

[65]

Rajilić-Stojanović M,Tims S,de Vos WM.Long-term monitoring of the human intestinal microbiota composition.Environ Microbiol2012:1146-59

AI Summary AI Mindmap
PDF

80

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/