Abstract
Organic matter deposits in alluvial aquifers have been shown to result in the formation of naturally reduced zones (NRZs), which can modulate aquifer redox status and influence the speciation and mobility of metals, affecting groundwater geochemistry. In this study, we sought to better understand how natural organic matter fuels microbial communities within anoxic biogeochemical hot spots (NRZs) in a shallow alluvial aquifer at the Rifle (CO) site. We conducted a 20-day microcosm experiment in which NRZ sediments, which were enriched in buried woody plant material, served as the sole source of electron donors and microorganisms. The microcosms were constructed and incubated under anaerobic conditions in serum bottles with an initial N2 headspace and were sampled every 5 days for metagenome and metatranscriptome profiles in combination with biogeochemical measurements. Biogeochemical data indicated that the decomposition of native organic matter occurred in different phases, beginning with mineralization of dissolved organic matter (DOM) to CO2 during the first week of incubation, followed by a pulse of acetogenesis that dominated carbon flux after 2 weeks. A pulse of methanogenesis co-occurred with acetogenesis, but only accounted for a small fraction of carbon flux. The depletion of DOM over time was strongly correlated with increases in expression of many genes associated with heterotrophy (e.g., amino acid, fatty acid, and carbohydrate metabolism) belonging to a Hydrogenophaga strain that accounted for a relatively large percentage (~8%) of the metatranscriptome. This Hydrogenophaga strain also expressed genes indicative of chemolithoautotrophy, including CO2 fixation, H2 oxidation, S-compound oxidation, and denitrification. The pulse of acetogenesis appears to have been collectively catalyzed by a number of different organisms and metabolisms, most prominently pyruvate:ferredoxin oxidoreductase. Unexpected genes were identified among the most highly expressed (>98th percentile) transcripts, including acetone carboxylase and cell-wall-associated hydrolases with unknown substrates (numerous lesser expressed cell-wall-associated hydrolases targeted peptidoglycan). Many of the most highly expressed hydrolases belonged to a Ca. Bathyarchaeota strain and may have been associated with recycling of bacterial biomass. Overall, these results highlight the complex nature of organic matter transformation in NRZs and the microbial metabolic pathways that interact to mediate redox status and elemental cycling.
Highlights
Shallow aquifers are often characterized as oligotrophic environments in which a heterotrophic microbial lifestyle is supported by surface-derived allochthonous organic matter (Ghiorse and Wilson, 1988), at least in aquifers that are not subject to subsurface anthropogenic contamination
naturally reduced zones (NRZs) have been characterized as biogeochemical hot spots at the Rifle site and have been associated with a relative enrichment of organic matter and anaerobic microbial metabolism, including both fermentative and respiratory [e.g., sulfate and Fe(III) reduction] pathways, based on geochemical and metagenomic data (Campbell et al, 2012; Hug et al, 2013; Janot et al, 2015)
We further investigated dynamic metabolic activity in NRZ hot spots at the Rifle site by integrating strain-specific metatranscriptomic and metagenomic data with geochemical data in anaerobic microcosms in which NRZ aquifer sediment served as the sole source of microorganisms and electron donors
Summary
Shallow aquifers are often characterized as oligotrophic environments in which a heterotrophic microbial lifestyle is supported by surface-derived allochthonous organic matter (Ghiorse and Wilson, 1988), at least in aquifers that are not subject to subsurface anthropogenic contamination. One exception to the generalization of aquifers as oligotrophic is the occurrence of organic-rich, naturally reduced zones (NRZs) in alluvial aquifers, which have been well documented in shallow, alluvial aquifers of the Colorado River Basin, at the U.S Department of Energy study site in Rifle, CO (e.g., Blazejewski et al, 2009; Campbell et al, 2012; Janot et al, 2015; Wainwright et al, 2016). The buried organic matter (e.g., weathered plant biomass) in these deposits has likely served as a long-lived electron donor fueling sulfate reduction and, directly or indirectly, Fe(III) and U(VI) reduction, contributing to the formation of iron sulfide minerals and deposits of poorly soluble U(IV) (e.g., Campbell et al, 2012; Janot et al, 2015)
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