Genome-Resolved Metaproteomics Decodes the Microbial and Viral Contributions to Coupled Carbon and Nitrogen Cycling in River Sediments

Rodríguez-Ramos, Josué A.; Borton, Mikayla A.; McGivern, Bridget B.; Smith, Garrett J.; Solden, Lindsey M.; Shaffer, Michael; Daly, Rebecca A.; Purvine, Samuel O.; Nicora, Carrie D.; Eder, Elizabeth K.; Lipton, Mary S.; Hoyt, David W.; Stegen, James C.; Wrighton, Kelly C.

doi:10.1128/msystems.00516-22

Genome-Resolved Metaproteomics Decodes the Microbial and Viral Contributions to Coupled Carbon and Nitrogen Cycling in River Sediments

Journal Article · Wed Jul 20 20:00:00 EDT 2022 · mSystems

DOI:https://doi.org/10.1128/msystems.00516-22· OSTI ID:1889470

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Colorado State Univ., Fort Collins, CO (United States)
Colorado State Univ., Fort Collins, CO (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Radboud Univ., Nijmegen (Netherlands)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Rivers have a significant role in global carbon and nitrogen cycles, serving as a nexus for nutrient transport between terrestrial and marine ecosystems. Although rivers have a small global surface area, they contribute substantially to worldwide greenhouse gas emissions through microbially mediated processes within the river hyporheic zone. Despite this importance, research linking microbial and viral communities to specific biogeochemical reactions is still nascent in these sediment environments. To survey the metabolic potential and gene expression underpinning carbon and nitrogen biogeochemical cycling in river sediments, we collected an integrated data set of 33 metagenomes, metaproteomes, and paired metabolomes. We reconstructed over 500 microbial metagenome-assembled genomes (MAGs), which we dereplicated into 55 unique, nearly complete medium- and high-quality MAGs spanning 12 bacterial and archaeal phyla. We also reconstructed 2,482 viral genomic contigs, which were dereplicated into 111 viral MAGs (vMAGs) of >10 kb in size. As a result of integrating gene expression data with geochemical and metabolite data, we created a conceptual model that uncovered new roles for microorganisms in organic matter decomposition, carbon sequestration, nitrogen mineralization, nitrification, and denitrification. We show how these metabolic pathways, integrated through shared resource pools of ammonium, carbon dioxide, and inorganic nitrogen, could ultimately contribute to carbon dioxide and nitrous oxide fluxes from hyporheic sediments. Further, by linking viral MAGs to these active microbial hosts, we provide some of the first insights into viral modulation of river sediment carbon and nitrogen cycling.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)

Grant/Contract Number:: AC05-76RL01830; SC0018170; SC0021350; AC02-05CH11231

OSTI ID:: 1889470

Alternate ID(s):: OSTI ID: 3012459

Report Number(s):: PNNL-SA-164701

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 4 Vol. 7; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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