Abstract
Alcohols are commonly derived from the degradation of organic matter and yet are rarely measured in environmental samples. Wetlands in the Prairie Pothole Region (PPR) support extremely high methane emissions and the highest sulfate reduction rates reported to date, likely contributing to a significant proportion of organic matter mineralization in this system. While ethanol and isopropanol concentrations up to 4 to 5 mM in PPR wetland pore fluids have been implicated in sustaining these high rates of microbial activity, the mechanisms that support alcohol cycling in this ecosystem are poorly understood. We leveraged metagenomic and transcriptomic tools to identify genes, pathways, and microorganisms potentially accounting for alcohol cycling in PPR wetlands. Phylogenetic analyses revealed diverse alcohol dehydrogenases and putative substrates. Alcohol dehydrogenase and aldehyde dehydrogenase genes were included in 62 metagenome-assembled genomes (MAGs) affiliated with 16 phyla. The most frequently encoded pathway (in 30 MAGs) potentially accounting for alcohol production was a Pyrococcus furiosus-like fermentation which can involve pyruvate:ferredoxin oxidoreductase (PFOR). Transcripts for 93 of 137 PFOR genes in these MAGs were detected, as well as for 158 of 243 alcohol dehydrogenase genes retrieved from these same MAGs. Mixed acid fermentation and heterofermentative lactate fermentation were also frequently encoded. Finally, we identified 19 novel putative isopropanol dehydrogenases in 15 MAGs affiliated with Proteobacteria, Acidobacteria, Chloroflexi, Planctomycetes, Ignavibacteriae, Thaumarchaeota, and the candidate divisions KSB1 and Rokubacteria We conclude that diverse microorganisms may use uncommon and potentially novel pathways to produce ethanol and isopropanol in PPR wetland sediments.IMPORTANCE Understanding patterns of organic matter degradation in wetlands is essential for identifying the substrates and mechanisms supporting greenhouse gas production and emissions from wetlands, the main natural source of methane in the atmosphere. Alcohols are common fermentation products but are poorly studied as key intermediates in organic matter degradation in wetlands. By investigating genes, pathways, and microorganisms potentially accounting for the high concentrations of ethanol and isopropanol measured in Prairie Pothole wetland sediments, this work advanced our understanding of alcohol fermentations in wetlands linked to extremely high greenhouse gas emissions. Moreover, the novel alcohol dehydrogenases and microbial taxa potentially involved in alcohol metabolism may serve biotechnological efforts in bioengineering commercially valuable alcohol production and in the discovery of novel isopropanol producers or isopropanol fermentation pathways.
Highlights
Alcohols are commonly derived from the degradation of organic matter and yet are rarely measured in environmental samples
Temperature perturbation experiments revealed a close coupling between fermentation and sulfate reduction [3], while iron reduction and methanogenesis were inferred to be supported by fermentation products in Arctic tundra soils [4]
Extremely high ethanol and isopropanol concentrations, methane concentrations, and sulfate reduction rates were measured in these sediments, with substrates depleted from spring to summer when methane emissions and sulfate reduction rates were highest [11]
Summary
Alcohols are commonly derived from the degradation of organic matter and yet are rarely measured in environmental samples. Pathways, and microorganisms potentially accounting for the high concentrations of ethanol and isopropanol measured in Prairie Pothole wetland sediments, this work advanced our understanding of alcohol fermentations in wetlands linked to extremely high greenhouse gas emissions. Using nonconcentrated sediment pore waters, ethanol and isopropanol concentrations of up to 4 to 5 mM have been measured using 1H-NMR in PPR wetland sediments [11], suggesting that fermentation may play a key role in organic matter degradation into these alcohols. This ecosystem is carbon rich, with pore fluid dissolved organic carbon concentrations reaching ϳ180 mg/liter [12]. 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
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