Akkermansia beyond muciniphila - emergence of new species Akkermansia massiliensis sp. nov.

Abstract

The human gut commensal Akkermansia muciniphila is the most studied bacterial species within the Verrucomicrobiota phylum. It has been proposed as a beneficial next-generation probiotic for cardiometabolic and immune health. Efforts from various research groups have resulted in the recent discovery of new species and/or phylotypes of the genus Akkermansia. This highlighted the genetic and phenotypic diversity among the Akkermansia isolates, providing an opportunity to identify novel mechanisms pertaining to health benefits. Genetic diversity between strains warrants detailed investigation to determine beneficial Akkermansia strains. Akkermansia massiliensis sp. nov. has emerged as the second most prevalent Akkermansia species in the human gut, with unique properties and potential relevance for human health. In addition, indications of the co-existence of more than one Akkermansia phylotype or species in a subject are intriguing. These new discoveries pave the way for additional developments of effective and targeted Akkermansia species-based interventions to provide health benefits.

Keywords

Akkermansia muciniphila / Akkermansia massiliensis sp. nov. / Akkermansia biwaensis cardiometabolic health

References

[1] Derrien M,Plugge CM.Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium.Int J Syst Evol Microbiol2004;54:1469-76

[2] Ouwerkerk JP,Belzer C.Akkermansia glycaniphila sp. nov., an anaerobic mucin-degrading bacterium isolated from reticulated python faeces.Int J Syst Evol Microbiol2016;66:4614-20

[3] Kobayashi Y,Inoue S.Akkermansia biwaensis sp. nov., an anaerobic mucin-degrading bacterium isolated from human faeces.Int J Syst Evol Microbiol2023;73:

[4] Gilroy R,Getino M.Extensive microbial diversity within the chicken gut microbiome revealed by metagenomics and culture.PeerJ2021;9:e10941 PMCID:PMC8035907

[5] Ndongo S,Raoult D.Reclassification of eight Akkermansia muciniphila strains and description of Akkermansia massiliensis sp. nov. and Candidatus Akkermansia timonensis, isolated from human feces.Sci Rep2022;12:21747 PMCID:PMC9758162

[6] Olson RD,Brettin T.Introducing the Bacterial and Viral Bioinformatics Resource Center (BV-BRC): a resource combining PATRIC, IRD and ViPR.Nucleic Acids Res2023;51:D678-89 PMCID:PMC9825582

[7] Oren A.Notification that new names of prokaryotes, new combinations, and new taxonomic opinions have appeared in volume 73, part 1 of the IJSEM.Int J Syst Evol Microbiol2023;73:

[8] González D,Vidal-Veuthey B.Insights into early evolutionary adaptations of the Akkermansia genus to the vertebrate gut.Front Microbiol2023;14:1238580 PMCID:PMC10540074

[9] 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

[10] Callahan BJ,Rosen MJ,Johnson AJ.DADA2: high-resolution sample inference from Illumina amplicon data.Nat Methods2016;13:581-3 PMCID:PMC4927377

[11] McDonald D, Hyde E, Debelius JW, et al; American Gut Consortium. American gut: an open platform for citizen science microbiome research.mSystems2018;3:e00031-18 PMCID:PMC5954204

[12] Mueller KD,Davey L.Pangenomic analysis identifies correlations between Akkermansia species and subspecies and human health outcomes.Microbiome Res Rep2024;3:33

[13] Kumar R,Wang Q.Identification and characterization of a novel species of genus Akkermansia with metabolic health effects in a diet-induced obesity mouse model.Cells2022;11:2084 PMCID:PMC9265676

[14] Becken B,Middleton DR.Genotypic and phenotypic diversity among human isolates of Akkermansia muciniphila.mBio2021;12:e00478-21 PMCID:PMC8262928

[15] van der Lelie D,Taghavi S.Rationally designed bacterial consortia to treat chronic immune-mediated colitis and restore intestinal homeostasis.Nat Commun2021;12:3105 PMCID:PMC8163890

[16] Routy B,Derosa L.Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors.Science2018;359:91-7

[17] Cani PD,Derrien M,de Vos WM.Akkermansia muciniphila: paradigm for next-generation beneficial microorganisms.Nat Rev Gastroenterol Hepatol2022;19:625-37

[18] Plovier H,Druart C.A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice.Nat Med2017;23:107-13

[19] Yoon HS,Yun MS.Akkermansia muciniphila secretes a glucagon-like peptide-1-inducing protein that improves glucose homeostasis and ameliorates metabolic disease in mice.Nat Microbiol2021;6:563-73

[20] Xie S,Lyu F.Novel tripeptide RKH derived from Akkermansia muciniphila protects against lethal sepsis.Gut2023;73:78-91

[21] Bae M,Liu X.Akkermansia muciniphila phospholipid induces homeostatic immune responses.Nature2022;608:168-73 PMCID:PMC9328018

[22] Chelakkot C,Kim DK.Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions.Exp Mol Med2018;50:e450 PMCID:PMC5903829

[23] Vuerich M,Robson SC.Control of gut inflammation by modulation of purinergic signaling.Front Immunol2020;11:1882 PMCID:PMC7544737

[24] Perruzza L,Raneri M.Apyrase-mediated amplification of secretory IgA promotes intestinal homeostasis.Cell Rep2022;40:111112

[25] Pryor R,Marinos G.Host-microbe-drug-nutrient screen identifies bacterial effectors of metformin therapy.Cell2019;178:1299-312.e29 PMCID:PMC6736778

[26] Kirmiz N,Cross KL.Comparative genomics guides elucidation of vitamin B₁₂ biosynthesis in novel human-associated Akkermansia strains.Appl Environ Microbiol2020;86:e02117-19 PMCID:PMC6974653

[27] Ottman N,Suarez-Diez M.Genome-scale model and omics analysis of metabolic capacities of Akkermansia muciniphila reveal a preferential mucin-degrading lifestyle.Appl Environ Microbiol2017;83:e01014-17 PMCID:PMC5583483

[28] Kang WK,Araya A.Vitamin B₁₂ produced by gut bacteria modulates cholinergic signalling.Nat Cell Biol2024;26:72-85