Sex-specific aging patterns of gut microbiota guild in urban Chinese adults

BACKGROUND: The loss of gut microbial stability has been observed during aging. Previous studies have noted changes in the diversity of gut microbiota and richness of specific bacteria along with age, but rarely focused on alternations in microbial guild. METHODS: Included in this study were 2944 middle-aged and elderly Chinese adults (1473 men and 1471 women) from the Shanghai Men's and Women's Health Studies, of whom 1419 healthy subjects (747 men and 672 women) self-reported no common non-communicable diseases (NCD) were selected for evaluating the healthy aging pattern. Microbiome was profiled by 16S rRNA sequencing. A guild-based method was adopted to cluster operational taxonomic units (OTU) into co-abundance groups (CAG) as functional units. PICRUSt2 were used to predict metagenome functions. The aging trend were assessed by linear regression. A random forest model incorporating significant CAGs with chronological age was developed to fit microbial age in the healthy and subsequently applied to those with NCDs. RESULTS: The age of all participants ranged from 51.4 to 89.3 years (mean of 70.2). A decline in Chao1 index and an increase in Pielou evenness with aging were observed among healthy women but not men. The microbial drift based on Bray-Curtis distance appeared driven by age and differed significantly by sex. Eleven CAGs were identified as potential aging markers in men, and twelve in women; wherein only CAG_6 (Bifidobacterium sp. dominated) and CAG_118 (Veillonella dispar dominated) were positively related with age in both genders. The 1,4-dihydroxy-2-naphthoate biosynthesis served as the core metabolic pathway that increased with age in both men and women. Subjects with metabolic diseases had an older microbial age than the healthy, particularly among men. CONCLUSIONS: This study indicates the importance of gut microbiota in healthy aging among Chinese men and women. The aging related sex-specific patterns of gut microbiota can be modified by prevalent NCDs. KEY MESSAGES: • The aging patterns of gut microbiota guild were different in middle-aged and elderly Chinese men and women. • The microbial age was older in subjects with metabolic diseases than those without.