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Abstract
The microbial ecology of the deep biosphere is difficult to characterize, owing in part to sampling challenges and poorly understood response mechanisms to environmental change. Pre-drilled wells, including oil wells or boreholes, offer convenient access, but sampling is frequently limited to the water alone, which may provide only a partial view of the native diversity. Mineral heterogeneity demonstrably affects colonization by deep biosphere microorganisms, but the connections between the mineral-associated and planktonic communities remain unclear. To understand the substrate effects on microbial colonization and the community response to changes in organic carbon, we conducted an 18-month series of in situ experiments in a warm (57°C), anoxic, fractured carbonate aquifer at 752 m depth using replicate open, screened cartridges containing different solid substrates, with a proteinaceous organic matter perturbation halfway through this series. Samples from these cartridges were analyzed microscopically and by Illumina (iTag) 16S rRNA gene libraries to characterize changes in mineralogy and the diversity of the colonizing microbial community. The substrate-attached and planktonic communities were significantly different in our data, with some taxa (e.g., Candidate Division KB-1) rare or undetectable in the first fraction and abundant in the other. The substrate-attached community composition also varied significantly with mineralogy, such as with two Rhodocyclaceae OTUs, one of which was abundant on carbonate minerals and the other on silicic substrates. Secondary sulfide mineral formation, including iron sulfide framboids, was observed on two sets of incubated carbonates. Notably, microorganisms were attached to the framboids, which were correlated with abundant Sulfurovum and Desulfotomaculum sp. sequences in our analysis. Upon organic matter perturbation, mineral-associated microbial diversity differences were temporarily masked by the dominance of putative heterotrophic taxa in all samples, including OTUs identified as Caulobacter, Methyloversatilis, and Pseudomonas. Subsequent experimental deployments included a methanogen-dominated stage (Methanobacteriales and Methanomicrobiales) 6 months after the perturbation and a return to an assemblage similar to the pre-perturbation community after 9 months. Substrate-associated community differences were again significant within these subsequent phases, however, demonstrating the value of in situ time course experiments to capture a fraction of the microbial assemblage that is frequently difficult to observe in pre-drilled wells.
Highlights
The continental deep biosphere represents approximately 5–15% of the biomass on Earth, or about 27–64 Gt of carbon, yet the ecological conditions that govern community structure and activity remain poorly constrained (McMahon and Parnell, 2014; Bar-On et al, 2018; Magnabosco et al, 2018)
Inyo-BLM 1 was drilled to test hypotheses concerning deep groundwater flow across the Funeral Mountains and intersects a variety of lithologies, encountering Hidden Valley Dolomite (HVD; Silurian-Devonian, 423-393 Ma, in age) at 744 mbls (Fridrich et al, 2012), which is associated with the Lower Carbonate Aquifer (LCA), a warm, fractured rock aquifer in the discharge zone of the Death Valley Regional Flow System (Belcher et al, 2001; Bredehoeft et al, 2008; Figure 1)
Within the open hole portion at the bottom, the oxygen reduction potential (ORP) drifts toward positive values, but these types of probes are sensitive to flocculent material in the water
Summary
The continental deep biosphere represents approximately 5–15% of the biomass on Earth, or about 27–64 Gt of carbon, yet the ecological conditions that govern community structure and activity remain poorly constrained (McMahon and Parnell, 2014; Bar-On et al, 2018; Magnabosco et al, 2018). Evidence suggests that do the mineralogical composition and crystallographic axes affect which microbes attach via electrostatic interactions (Yee et al, 2000; Edwards and Rutenberg, 2001), and that microbes actively weather minerals to access scarce nutrients or by way of their central metabolism (Lovley et al, 1989; Rogers et al, 1998; Caccavo and Das, 2002; Roberts, 2004) These effects can often be challenging to detect in situ due to the difficulty of accessing underground fracture networks, and because mineralogy typically varies concurrently with changes in geochemistry, temperature, porosity, and pressure along a depth axis. In situ experiments in terrestrial boreholes drilled from the surface are an attractive option because they provide direct access to rock surfaces in the native subsurface biogeochemical context Subseafloor biosphere studies, such as (Orcutt et al, 2010), which deployed flow-through columns containing mineral colonization substrates of interest, can provide a good model for terrestrial experiments. Drilling always carries a risk of contamination, but drilling contamination can be mitigated in pumped or free-flowing boreholes by flushing with local groundwater to remove contaminants and re-establish the indigenous community (Moser et al, 2003; Davidson et al, 2011)
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