Socioeconomic drivers of the human microbiome footprint in global sewage

Abstract

The human microbiome leaves a legacy in sewage ecosystems, also referred to as the human sewage microbiomes (HSM), and could cause potential risk to human health and ecosystem service. However, these host-associated communities remain understudied, especially at a global scale, regarding microbial diversity, community composition and the underlying drivers. Here, we built a metagenomic read mapping-based framework to estimate HSM abundance in 243 sewage samples from 60 countries across seven continents. Our approach revealed that 95.03% of human microbiome species were identified from global sewage, demonstrating the potential of sewage as a lens to explore these human-associated microbes while bypassing the limitations of human privacy concerns. We identified significant biogeographic patterns for the HSM community, with species richness increasing toward high latitudes and composition showing a distance-decay relationship at a global scale. Interestingly, the HSM communities were mainly clustered by continent, with those from Europe and North America being separated from Asia and Africa. Furthermore, global HSM diversity was shown to be shaped by both climate and socioeconomic variables. Specifically, the average annual temperature was identified as the most important factor for species richness (33.18%), whereas economic variables such as country export in goods and services contributed the most to the variation in community composition (27.53%). Economic and other socioeconomic variables, such as education, were demonstrated to have direct effects on the HSM, as indicated by structural equation modeling. Our study provides the global biogeography of human sewage microbiomes and highlights the economy as an important socioeconomic factor driving host-associated community composition.