Metapangenomics reveals an increased proportion of an Escherichia coli-dominated enterotype in older Chinese people

Abstract

Background:Gut microbial communities are likely remodeled along with accumulated physiological decline during aging. Here, we performed a metagenomics-based enterotype analysis in a geographically homogeneous cohort of 367 enrolled Chinese individuals between the ages of 60 and 94, with the goal of characterizing the gut microbiome of the older Chinese individuals and identifying factors linked to enterotype variations.Results:In addition to two adult-like enterotypes were dominated by Bacteroides spp. (ET-Bacteroides spp.) and Prevotella copri (ET-P. copri), we further identified a novel enterotype dominated by Escherichia coli (ET-E. coli), whose prevalence increased in advanced age. ET-E. coli presented some characteristics previously observed in the microbiomes of older people, including low species diversity and diminished abundance of the butyrate producer Faecalibacterium prausnitzii (F. prausnitzii), and exhibited distinct functions as well as a complex, highly stable microbial co-occurrence network, as evidenced by cohesion and natural connectivity analysis. Furthermore, a series of correlation analyses and co-abundance network analyses were carried out and showed that several factors were likely linked to the overabundance of Escherichia members, including advanced age, different vegetable, and fruit intake. Notably, there may be a niche pre-emption of E. coli by P. copri in ET-P. copri via several functional pathways involved in queuosine, braided glycoside, UMP, L-lysine and aromatic amino acid biosynthesis. Overall, our data demonstrated that age explained more of the variance in the gut microbiome than previously identified factors such as type 2 diabetes mellitus (T2DM) and diet. Overgrowth of Escherichia members might occur in a senior's gut where the dominance of core functional microbiota was impaired by long-term changes in dietary habits, gut physiology, and gastrointestinal motility during aging.Conclusion:This study demonstrates an enterotype variation featured by E. coli enrichment in some older Chinese individuals, indicating a potential dissimilation of the gut microbial community with altered host conditions eventually leading to enterotype transitions in advanced age. These findings provide new insights into the changes in the gut microbiome in older age and clues for mechanistic investigations on the driving forces.

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“…Investigations into the oral microbiome demonstrated that different oral habitats are associated with specific functions, such as oxaloacetate decarboxylase metabolism in a tongue-enriched subgroup of H. parainfluenzae [28]. In humans, meta-pangenomics of Escherichia in older Chinese individuals highlighted higher abundance in the gut microbiome, with implications for dietary habits and gut health during aging [29]. The meta-pangenomics give us new insights into bacteria genome in its host and/or environmental metagenomes and its microbial functions related to host physiology and habitat preferences.…”

“…Meta-pangenomics is a novel approach combining pangenomes and metagenomes to investigate bacterial genomes recruited reads in their environmental metagenomes, providing broader perspectives of understanding the roles of its distribution and biogeographical patterns through the microbial population [27,28]. Meta-pangenomics have been applied to investigate the human microbiome, revealing the distribution of identical genes in pangenomes across populations in different locations and ages [28,29]. The adaptation of microbial populations in extreme environment from deep sea microbiome also has been investigated by metapangenomics [30,31].…”