Socioeconomic drivers of the human microbiome footprint in global sewage

Highlights

● We built a read-mapping framework to profile human microbes from sewages (HSM).

● There were 95.03% human microbial species successfully recaptured from sewages.

● The HSM composition showed a distance-decay pattern at a global scale.

● The HSM communities from developed regions were separated from developing regions.

● Economy was the key socioeconomic factors driving the HSM diversity.

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.

Graphical abstract

Keywords

Human sewage microbiome / Biogeography / Socioeconomic factors / Climate factors

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Acknowledgements

We sincerely thank Prof. Zongjun Du from Shandong University for helpful comments about the early version of the manuscript. This study was financially supported by the National Natural Science Foundation of China (Nos. 42225708, 42372353, 92251304, 92351303, and 42002304).

Conflict of Interests

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-024-1889-z and is accessible for authorized users.

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