How Lifestyle Shapes Gut Microbial Diversity and Keystone Taxa in Indian Tribes

Highlights

  • •
    An introduced analytical framework quantifies taxon–community associations to identify computationally inferred candidate keystone taxa.
  • •
    Application to five PVTGs identifies 121 candidate keystone taxa, most of which are population-specific, with a reproducible subset across traditional populations.
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    Several candidate keystone taxa associated with lower community dispersion also show consistent associations with multiple disease conditions, highlighting priorities for future investigation.
  • •
    A conserved metabolic core coexists with population-specific functions, while acculturation is associated with reduced microbial diversity and increased disease-associated taxa.


Abstract

Despite the critical role of the gut microbiome in host physiology and health, it remains poorly characterized in Indigenous populations undergoing rapid acculturation. This study presents high-resolution, whole-genome metagenomic profiling of gut microbiota from five Particularly Vulnerable Tribal Groups (PVTGs) of Southern India, Irula, Jenu Kuruba, Kurumba, Chenchu, and Konda Savara, spanning distinct ecological zones and cultural transitions. Using an ecology–lifestyle continuum framework, we investigated taxonomic and functional diversity with a focus on identifying computationally inferred candidate keystone taxa, defined by their association with variation in community ordination structure. A leave-one-taxon-out ordination framework identified 121 candidate keystone taxa, many of which were population-specific and have not been widely reported. Functional analyses revealed a conserved core of metabolic pathways, including glycolysis and folate biosynthesis, alongside group-specific enrichment in xenobiotic degradation, amino acid biosynthesis, mucin metabolism, and lipid processing, associated with differences in dietary and environmental exposures across populations. Large-scale disease-association mapping (n = 5,625) linked 50 candidate keystone taxa to 14 conditions, with 44 associated with health and 6 with disease. While Fusicatenibacter saccharivorans and Alistipes shahii were enriched in healthy states, Ruminococcus gnavus, Bifidobacterium longum, Flavonifractor plautii, and Blautia wexlerae were enriched in disease-associated profiles. Cross-cohort validation against an independent set of traditional metagenomes (n = 119) further showed that a subset of Indian tribal core candidate keystone taxa was consistently identified across geographically distinct populations, with partial conservation of community associations and health associations, indicating reproducible context-dependent microbial association patterns across traditional populations. Alpha diversity was highest in minimally acculturated groups, with higher degrees of acculturation associated with reduced microbial diversity and greater enrichment of disease-associated taxa. Overall, this study provides a context-aware framework for understanding gut microbiome dynamics in culturally transitioning populations, emphasizing the conservation of microbial heritage and informing population-specific microbiome-based interventions.

Read full article for free (open access):
https://www.sciencedirect.com/science/article/pii/S2666517426001069



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