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

Abstract

BackgroundMicroorganisms 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.ResultsWe 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 Methanofollis-affiliated 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0522-4) contains supplementary material, which is available to authorized users.

Wetland Sediments Host Diverse Microbial Taxa Capable of Cycling Alcohols

“…Depth-resolved metagenomic data sets were obtained from sediments in two characteristic wetlands near Jamestown, ND, and processed as previously described (13). These wetlands are rich in dissolved organic carbon (12) and sulfur compounds (16, 17) due to the local hydrological regime and the underlying pyrite-rich glacial till (18).…”

“…The depletion of alcohols during a period of high sulfate reduction, as well as the identification of candidate sulfate-reducing bacterium genomes encoding alcohol dehydrogenases, suggested a possible role for these substrates in driving sulfate reduction in this system. Moreover, the detection of F420-dependent alcohol dehydrogenases and mcrA genes affiliated with alcohol-utilizing Methanofollis species indicated that methanogenesis may also be directly supported by these fermentation products (13). Despite the potential importance of alcohols in supporting biogeochemical activity in PPR sediments, the microbial members and the pathways responsible for alcohol fermentation in this system remain unknown.…”

“…Here, we used metagenomics and metatranscriptomics to investigate putative alcohol-cycling microorganisms in PPR wetland sediments using sequencing data obtained for samples previously analyzed (11, 13). We have examined genome-encoded alcohol dehydrogenases and pathways that could result in ethanol and isopropanol production in Prairie Pothole wetlands.…”

Temporal Dynamics of Soil Virus and Bacterial Populations in Agricultural and Early Plant Successional Soils

“…The first direct counts of agricultural soil viruses using epifluorescence microscopy were reported in 2003 (Williamson et al, 2003). Since that time various aspects of soil viral ecology have been examined in wetlands, forest soils, and extreme cold desert soils of Antarctica (Williamson et al, 2007;Martins et al, 2018;Rodela et al, 2019;Liang et al, 2020). Though viruses appear to be highly abundant in soils, relatively few studies have attempted to determine the extent to which soil microorganisms are infected by viruses.…”

Viral Abundance and Diversity of Production Fluids in Oil Reservoirs

“…In addition, many viruses are able to integrate their genome into their host chromosome and act as biological agents for horizontal gene transfer through lysogenic cycles contributing to microbial evolution. Although a lot of research has been conducted regarding viral ecology in soil [ 9 , 10 , 11 , 12 , 13 , 14 , 15 ], marine [ 4 , 8 , 16 , 17 , 18 ], river [ 19 ], wet-land [ 20 ] and paddy [ 21 ] environments, little effort has been made to study viral populations and viral communities in the oil reservoir. Microbial ecology in oil reservoirs mainly focuses on the relationship between injected and indigenous microbes, and the effects of injected nutrients and environmental factors on microbes and microbial community composition in the reservoir.…”