Viral and metabolic controls on high rates of microbial sulfur and carbon cycling in wetland ecosystems

Martins, Paula Dalcin; Danczak, Robert E.; Roux, Simon; Frank, Jeroen; Borton, Mikayla A.; Wolfe, Richard A.; Burris, Marie N.; Wilkins, Michael J.

doi:10.1186/s40168-018-0522-4

Viral and metabolic controls on high rates of microbial sulfur and carbon cycling in wetland ecosystems

Journal Article · Tue Aug 07 00:00:00 EDT 2018 · Microbiome

DOI:https://doi.org/10.1186/s40168-018-0522-4· OSTI ID:1627047

Martins, Paula Dalcin ^[1]; Danczak, Robert E. ^[2]; Roux, Simon ^[3]; Frank, Jeroen ^[4]; Borton, Mikayla A. ^[2]; Wolfe, Richard A. ^[2]; Burris, Marie N. ^[2]; ^[2]

The Ohio State Univ., Columbus, OH (United States); DOE/OSTI
The Ohio State Univ., Columbus, OH (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Radboud Univ., Nijmegen (Netherlands)

Microorganisms drive high rates of methanogenesis and carbon mineralization in wetland ecosystems. These signals are especially pronounced in the Prairie Pothole Region of North America, the tenth largest wetland ecosystem in the world. Sulfate reduction rates up to 22 μmol cm^-3 day^-1 have been measured in these wetland sediments, as well as methane fluxes up to 160 mg m^-2 h^-1—some of the highest emissions ever measured in North American wetlands. While pore waters from PPR wetlands are characterized by high concentrations of sulfur species and dissolved organic carbon, the constraints on microbial activity are poorly understood. Here, we utilized metagenomics to investigate candidate sulfate reducers and methanogens in this ecosystem and identify metabolic and viral controls on microbial activity. Results: We recovered 162 dsrA and 206 dsrD sequences from 18 sediment metagenomes and reconstructed 24 candidate sulfate reducer genomes assigned to seven phyla. These genomes encoded the potential for utilizing a wide variety of electron donors, such as methanol and other alcohols, methylamines, and glycine betaine. We also identified 37 mcrA sequences spanning five orders and recovered two putative methanogen genomes representing the most abundant taxa—Methanosaeta and Methanoregulaceae. However, given the abundance of Methanofollisaffiliated mcrA sequences, the detection of F420-dependent alcohol dehydrogenases, and millimolar concentrations of ethanol and 2-propanol in sediment pore fluids, we hypothesize that these alcohols may drive a significant fraction of methanogenesis in this ecosystem. Finally, extensive viral novelty was detected, with approximately 80% of viral populations being unclassified at any known taxonomic levels and absent from publicly available databases. Many of these viral populations were predicted to target dominant sulfate reducers and methanogens. Our results indicate that diversity is likely key to extremely high rates of methanogenesis and sulfate reduction observed in these wetlands. The inferred genomic diversity and metabolic versatility could result from dynamic environmental conditions, viral infections, and niche differentiation in the heterogeneous sediment matrix. These processes likely play an important role in modulating carbon and sulfur cycling in this ecosystem.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: Netherlands Organisation for Scientific Research (NWO); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627047

Journal Information:: Microbiome, Journal Name: Microbiome Journal Issue: 1 Vol. 6; ISSN 2049-2618

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Additional file 11: of Viral and metabolic controls on high rates of microbial sulfur and carbon cycling in wetland ecosystems Martins, Paula Dalcin; Danczak, Robert; Roux, Simon https://doi.org/10.6084/m9.figshare.6944399.v1 The current record is supplemented by this dataset	dataset	January 2018
Additional file 1: of Viral and metabolic controls on high rates of microbial sulfur and carbon cycling in wetland ecosystems Martins, Paula Dalcin; Danczak, Robert; Roux, Simon https://doi.org/10.6084/m9.figshare.6944447 The current record is supplemented by this dataset	dataset	January 2018
Additional file 2: of Viral and metabolic controls on high rates of microbial sulfur and carbon cycling in wetland ecosystems Martins, Paula Dalcin; Danczak, Robert; Roux, Simon https://doi.org/10.6084/m9.figshare.6944468.v1 The current record is supplemented by this dataset	dataset	January 2018
Additional file 3: of Viral and metabolic controls on high rates of microbial sulfur and carbon cycling in wetland ecosystems Martins, Paula Dalcin; Danczak, Robert; Roux, Simon https://doi.org/10.6084/m9.figshare.6944486.v1 The current record is supplemented by this dataset	dataset	January 2018
Additional file 7: of Viral and metabolic controls on high rates of microbial sulfur and carbon cycling in wetland ecosystems Martins, Paula Dalcin; Danczak, Robert; Roux, Simon https://doi.org/10.6084/m9.figshare.6944561 The current record is supplemented by this dataset	dataset	January 2018
Additional file 8: of Viral and metabolic controls on high rates of microbial sulfur and carbon cycling in wetland ecosystems Martins, Paula Dalcin; Danczak, Robert; Roux, Simon https://doi.org/10.6084/m9.figshare.6944579.v1 The current record is supplemented by this dataset	dataset	January 2018
Viral and metabolic controls on high rates of microbial sulfur and carbon cycling in wetland ecosystems Martins, Paula Dalcin; Danczak, Robert; Roux, Simon https://doi.org/10.6084/m9.figshare.c.4191728.v1 The current record is supplemented by this collection	collection	January 2018

Viral and metabolic controls on high rates of microbial sulfur and carbon cycling in wetland ecosystems

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