Loss of Novel Diversity in Human Gut Microbiota Associated with Ongoing Urbanization in China

Recent rapid and large-scale urbanization has had a profound impact on human lifestyles and is associated with an increased risk of many diseases. Recent studies have revealed large differences in the human gut microbiota across populations in countries at different stages of urbanization. However, few studies have analyzed the impact of ongoing urbanization within the same geographic region. In this study, we sampled 214 participants in communities of different urbanization levels within two provinces of China and reconstructed draft prokaryotic genomes with metagenome sequences. The genomes were clustered into 447 species-level operational taxonomic units (OTUs), among which 196 did not have genomes in public reference databases according to the GTDB-Tk pipeline. The novel OTUs comprised 19.1% abundance in rural participants and 16.0% in urban participants, increasing the proportion of classified reads from 47.6% to 65.3% across all samples. Among the unknown OTUs, 26 OTUs present in rural samples were absent in urban participants, while 70 unknown OTUs were more abundant in rural than urban participants, suggesting potential loss and growth suppression of novel human symbionts during urbanization. Moreover, there were a higher number of genes, especially transporters, identified in genomes assembled from urban samples. This change in gene functionality indicates that urbanization not only altered the community structure of the human gut microbiota but also impacted its functional capacity. Taken together, these data show a dramatic change in the microbiota with urbanization and suggest the importance of cataloging microbial diversity from rural populations while these communities still exist. IMPORTANCE Previous studies have reported the differences in human gut microbiota across populations of different urbanization levels, but most of the studies focused on populations across different geographic regions. In this study, we analyzed the impact of ongoing urbanization in neighborhoods within the same geographic region. By assembling shotgun metagenome sequences, we reconstructed prokaryotic genomes from human gut microbiota and found that the novel bacterial OTUs were less abundant and less prevalent in urban participants than in rural participants, indicating potential loss and suppression of novel human symbionts during urbanization. Genes, including transporters and antibiotic resistance genes, were enriched in genomes of urban origins, suggesting change in functional potential of the microbiota. These findings suggest the significant influence of urbanization on human gut microbiota and the necessity of exploring the microbial diversity of rural populations.