Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomics

Leyuan Li, Tong Wang, Zhibin Ning, Xu Zhang, James Butcher, Joeselle M. Serrana, Caitlin M. A. Simopoulos, Janice Mayne, Alain Stintzi, David R. Mack, Yang-Yu Liu () and Daniel Figeys ()
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Leyuan Li: Beijing Institute of Lifeomics
Tong Wang: Brigham and Women’s Hospital and Harvard Medical School
Zhibin Ning: University of Ottawa
Xu Zhang: University of Ottawa
James Butcher: University of Ottawa
Joeselle M. Serrana: University of Ottawa
Caitlin M. A. Simopoulos: University of Ottawa
Janice Mayne: University of Ottawa
Alain Stintzi: University of Ottawa
David R. Mack: University of Ottawa and Children’s Hospital of Eastern Ontario Inflammatory Bowel Disease Centre and Research Institute
Yang-Yu Liu: Brigham and Women’s Hospital and Harvard Medical School
Daniel Figeys: University of Ottawa

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: Abstract Functional redundancy is a key ecosystem property representing the fact that different taxa contribute to an ecosystem in similar ways through the expression of redundant functions. The redundancy of potential functions (or genome-level functional redundancy $${{{{{{\rm{FR}}}}}}}_{g}$$ FR g ) of human microbiomes has been recently quantified using metagenomics data. Yet, the redundancy of expressed functions in the human microbiome has never been quantitatively explored. Here, we present an approach to quantify the proteome-level functional redundancy $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p in the human gut microbiome using metaproteomics. Ultra-deep metaproteomics reveals high proteome-level functional redundancy and high nestedness in the human gut proteomic content networks (i.e., the bipartite graphs connecting taxa to functions). We find that the nested topology of proteomic content networks and relatively small functional distances between proteomes of certain pairs of taxa together contribute to high $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p in the human gut microbiome. As a metric comprehensively incorporating the factors of presence/absence of each function, protein abundances of each function and biomass of each taxon, $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p outcompetes diversity indices in detecting significant microbiome responses to environmental factors, including individuality, biogeography, xenobiotics, and disease. We show that gut inflammation and exposure to specific xenobiotics can significantly diminish the $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p with no significant change in taxonomic diversity.

Date: 2023
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DOI: 10.1038/s41467-023-39149-2

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