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Cited by 30Genomics and Phylogenetic StudiesGut microbiota and healthMicrobial Community Ecology and Physiology

Insights into early evolutionary adaptations of the Akkermansia genus to the vertebrate gut

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González, Dámariz, Morales-Olavarria, Mauricio, Vidal-Veuthey, Boris, Cárdenas, Juan P.·2023·Frontiers in Microbiology
DOI 10.3389/fmicb.2023.1238580PMC PMC10540074
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Abstract

Akkermansia, a relevant mucin degrader from the vertebrate gut microbiota, is a member of the deeply branched Verrucomicrobiota, as well as the only known member of this phylum to be described as inhabitants of the gut. Only a few Akkermansia species have been officially described so far, although there is genomic evidence addressing the existence of more species-level variants for this genus. This niche specialization makes Akkermansia an interesting model for studying the evolution of microorganisms to their adaptation to the gastrointestinal tract environment, including which kind of functions were gained when the Akkermansia genus originated or how the evolutionary pressure functions over those genes. In order to gain more insight into Akkermansia adaptations to the gastrointestinal tract niche, we performed a phylogenomic analysis of 367 high-quality Akkermansia isolates and metagenome-assembled genomes, in addition to other members of Verrucomicrobiota. This work was focused on three aspects: the definition of Akkermansia genomic species clusters and the calculation and functional characterization of the pangenome for the most represented species; the evolutionary relationship between Akkermansia and their closest relatives from Verrucomicrobiota, defining the gene families which were gained or lost during the emergence of the last Akkermansia common ancestor (LAkkCA) and; the evaluation of the evolutionary pressure metrics for each relevant gene family of main Akkermansia species. This analysis found 25 Akkermansia genomic species clusters distributed in two main clades, divergent from their non-Akkermansia relatives. Pangenome analyses suggest that Akkermansia species have open pangenomes, and the gene gain/loss model indicates that genes associated with mucin degradation (both glycoside hydrolases and peptidases), (micro)aerobic metabolism, surface interaction, and adhesion were part of LAkkCA. Specifically, mucin degradation is a very ancestral innovation involved in the origin of Akkermansia. Horizontal gene transfer detection suggests that Akkermansia could receive genes mostly from unknown sources or from other Gram-negative gut bacteria. Evolutionary metrics suggest that Akkemansia species evolved differently, and even some conserved genes suffered different evolutionary pressures among clades. These results suggest a complex evolutionary landscape of the genus and indicate that mucin degradation could be an essential feature in Akkermansia evolution as a symbiotic species.

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  • In this review, Akkermansia was characterized by several host-interaction and persistence-related features, including epithelial adherence, aggregation, pili, autotransporters, sulfatases, mucin-associated enzymes, oxygen tolerance, Amuc-related proteins, and genes associated with B12/corrin-related biosynthesis.

    “In this review, Akkermansia was characterized by several host-interaction and persistence-related features, including epithelial adherence, aggregation, pili, autotransporters, sulfatases, mucin-associated enzymes, oxygen tolerance, Amuc-related proteins, and genes associated with B12/corrin-related biosynthesis. 12,14,21,24,31”

    From Comparative Genomic Insights into Pangenome Diversity and Functional Adaptation of Akkermansia and Faecalibacterium as Gut-Associated Next-Generation Probiotics: A Systematic Review (2026) · cites this paper as [14]

    The Results (‘Predicted metabolism and genetic features of LAkkCA’; page unavailable) describe predicted pili and autotransporters with possible roles in adherence and mucin degradation, as well as genes associated with oxygen use and oxidative stress. The mucin-metabolism Results identify conserved sulfatases, but the searched passages do not substantiate aggregation, Amuc-related proteins, or B12/corrin biosynthesis genes. Adherence is presented as a prediction, not a demonstrated epithelial-adherence finding. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Akkermansia was mainly associated with mucin degradation, human milk oligosaccharide utilization, and host-glycan utilization, reflecting its adaptation to the mucus layer and host-derived nutrient niches.

    “Akkermansia was mainly associated with mucin degradation, human milk oligosaccharide utilization, and host-glycan utilization, reflecting its adaptation to the mucus layer and hostderived nutrient niches. 14,30,31”

    From Comparative Genomic Insights into Pangenome Diversity and Functional Adaptation of Akkermansia and Faecalibacterium as Gut-Associated Next-Generation Probiotics: A Systematic Review (2026) · cites this paper as [14]

    The Results section on mucin metabolism reports conserved genes for degrading mucin glycans, and the Discussion links mucin degradation to Akkermansia’s adaptation to the gut mucus environment (page numbers unavailable). Our copy does not establish human milk oligosaccharide utilization; searches for that term and for “milk” found no supporting passage. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

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Cited by

Sorted by citations

Authors
González, D., Morales-Olavarria, M., Vidal-Veuthey, B., & Cárdenas, J. P.
Affiliations
Universidad Mayor (CL)
Corresponding author
Cárdenas, Juan P.
ORCID
Cárdenas, Juan P.
Venue
Frontiers in Microbiology
Publisher
Frontiers Media SA
Published
2023-09-14
Volume
14
Pages
1238580-1238580
ISSN
1664-302X (ISSN-L)
DOI
10.3389/fmicb.2023.1238580
PMC
PMC10540074
OpenAlex
W4386791345
Cited by
30
References
11
Citations by year
2026: 11 · 2025: 11 · 2024: 8
FWCI
2.67
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Microbiology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Agencia Nacional de Investigación y Desarrollo (11200209)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
Akkermansia, Verrucomicrobia, gut microbiota, mucin degradation, intestinal adaptation, phylogenomics, pan-genome, gene gain and loss, last common ancestor, horizontal gene transfer, glycoside hydrolases, proteolytic enzymes, evolutionary pressure, metagenome-assembled genomes, symbiosis

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