Activity-targeted metaproteomics uncovers rare syntrophic bacteria central to anaerobic community metabolism

Friedline, Skyler; McDaniel, Elizabeth A.; Scarborough, Matthew; Madill, Maxwell; Waring, Kate; Lin, Vivian S.; Malmstrom, Rex R.; Goudeau, Danielle; Chrisler, William B.; Dueholm, Morten K. D.; Gorham, Leo J.; Kombala, Chathuri Jeewanthi; Griggs, Lydia H.; Olson, Heather M.; Lehmann, Sophie B.; Munoz Munoz, Nathalie; Trejo, Jesse; Tolic, Nikola; Pasa-Tolic, Ljiljana; Williams, Sarah M.; Lipton, Mary S.; Hallam, Steven J.; Ziels, Ryan M.

doi:10.1038/s41564-025-02146-w

Title: Activity-targeted metaproteomics uncovers rare syntrophic bacteria central to anaerobic community metabolism

Journal Article · Tue Oct 21 00:00:00 UTC 2025 · Nature Microbiology

DOI: https://doi.org/10.1038/s41564-025-02146-w · OSTI ID:3003261

^[1];

^[1]; Scarborough, Matthew ^[2]; Madill, Maxwell ^[1]; Waring, Kate ^[1]; Lin, Vivian S. ^[3];

^[4];

^[4]; Chrisler, William B. ^[3]; Dueholm, Morten K. D. ^[5]; Gorham, Leo J. ^[3];

^[3]; Griggs, Lydia H. ^[3];

^[3]; Lehmann, Sophie B. ^[3];

^[3]; Trejo, Jesse ^[3]; Tolic, Nikola ^[3];

^[3]; Williams, Sarah M. ^[3] more »

Univ. of British Columbia, Vancouver, BC (Canada)
Univ. of Vermont, Burlington, VT (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Aalborg Univ. (Denmark)

Syntrophic microbial consortia can contribute significantly to the activity and function of anoxic ecosystems, yet are often too rare to study their in situ physiologies using traditional molecular methods. Here, in this study, we describe a technical innovation combining bioorthogonal non-canonical amino acid tagging (BONCAT), stable isotope probing, and metaproteomics to improve the recovery of proteins from active community members and track isotope incorporation. Both click chemistry-enabled cell-sorting and direct protein pulldown coupled to metaproteomics improved recovery of isotopically labeled proteins during acetate oxidation within a full-scale anaerobic digester. Resulting labeled protein expression profiles revealed elevated activity of a rare and uncharacterized syntrophic bacterium belonging to the family Natronincolaceae. BONCAT-based capture of newly translated proteins provided direct molecular evidence for the expression of a previously hypothesized oxidative glycine pathway for syntrophic acetate oxidation by this microorganism, showcasing the potential of targeted metaproteomics to characterize rare and active cells central to community metabolism in natural and engineered ecosystems.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: US Department of Energy; USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Biological Systems Science Division (SC-23.2 )

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830

OSTI ID:: 3003261

Report Number(s):: PNNL-SA--209084

Journal Information:: Nature Microbiology, Journal Name: Nature Microbiology Journal Issue: 11 Vol. 10; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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