Hydrogen and dark oxygen drive microbial productivity in diverse groundwater ecosystems

Abstract

Around 50% of humankind relies on groundwater as a source of drinking water. Here we investigate the age, geochemistry, and microbiology of 138 groundwater samples from 95 monitoring wells (<250 m depth) located in 14 aquifers in Canada. The geochemistry and microbiology show consistent trends suggesting large-scale aerobic and anaerobic hydrogen, methane, nitrogen, and sulfur cycling carried out by diverse microbial communities. Older groundwaters, especially in aquifers with organic carbon-rich strata, contain on average more cells (up to 1.4 × 107 mL−1) than younger groundwaters, challenging current estimates of subsurface cell abundances. We observe substantial concentrations of dissolved oxygen (0.52 ± 0.12 mg L−1 [mean ± SE]; n = 57) in older groundwaters that seem to support aerobic metabolisms in subsurface ecosystems at an unprecedented scale. Metagenomics, oxygen isotope analyses and mixing models indicate that dark oxygen is produced in situ via microbial dismutation. We show that ancient groundwaters sustain productive communities and highlight an overlooked oxygen source in present and past subsurface ecosystems of Earth.

Hydrological and Geological Controls for the Depth Distribution of Dissolved Oxygen and Iron in Silicate Catchments

“…The depth of the oxic-anoxic transition in silicate catchments is controlled by the relative importance of the reducing capacity of the rocks and the effective transport of oxygen from the surface, quantified here by the Damköhler number (Figure 6a). Consistently with our model, linear trends in DO with depth have been seen in various hard-rock systems, including the Clara mine in Germany (Bucher et al, 2009) or the Western Canadian Sedimentary Basin (Ruff et al, 2023).…”

“…Several field works documenting weathering profiles in hard‐rocks, either from outcrops (Antoniellini et al., 2017) or borehole cores (Bazilevskaya et al., 2013; Dideriksen et al., 2010; Hampl et al., 2021; Holbrook et al., 2019), have suggested that DO transport by subsurface flow could explain the presence of secondary minerals and weathering induced fracturing (WIF) in ferrous silicates (Bazilevskaya et al., 2013; Kim et al., 2017) from deep regolith. Likewise, evidence from field measurements in fractured‐rock aquifers has shown that DO can effectively persist in deep aquifers(Bucher et al., 2009; DeSimone et al., 2014; Edmunds et al., 1984; Ruff et al., 2023; Sullivan et al., 2016; Winograd & Robertson, 1982). Based on field observations, the presence or absence of DO in the subsurface has been attributed to lithological differences of the bedrock (Malard & Hervant, 1999; Winograd & Robertson, 1982) or to the spatial distribution of oxidation fronts (Liao et al., 2022).…”

A global atlas of subsurface microbiomes reveals phylogenetic novelty, large scale biodiversity gradients, and a marine-terrestrial divide

“…Moreover, many of the environments we studied cannot be easily defined as surface or subsurface environment. Subsurface or subsurface-impacted ecosystems are not necessarily energy depleted and, in fact, can be relatively energy rich -such as hydrocarbon seeps (80), brines (81), hydrothermal vents (82), oil, coal and shale deposits (51,83,84), serpentinizing systems (85)(86)(87), and caves (88). The subsurface is often replete with methane, hydrogen, and other energy and carbon sources (45,(89)(90)(91)(92).…”

Extremely oligotrophic and complex carbon degrading microaerobic bacteria from Arabian Sea oxygen minimum zone sediments

“…Microbial dismutation of nitric oxide (NO) can be a potential source of O 2 within dark ecosystems (Ettwig et al 2010;Kraft et al 2022;Ruff et al 2023). The NO dismutase (Nod)…”

“…NO dismutation, and other potential sources, of cryptic O 2 for aerobic bacteria in OMZ sediments Albeit the present state of knowledge does not offer any empirical insight to the absence or presence of O 2 (at whatever miniscule concentration that may be) in the ASOMZ sediments, all information available thus far on the biogeochemistry of the system (Fernandes et al 2018(Fernandes et al , 2022 indicate that this sulfidic habitat is essentially anoxic below a few centimeters from the seafloor (Bhattacharya et al 2019). From a biochemical perspective it is noteworthy that aerobic bacteria can thrive on nanomolar, or even lower, O 2 concentrations in vitro (Stolper et al 2010), as well as in natural habitats (Ruff et al 2023) including marine territories Wright et al 2012;Kalvelage et al 2015;Garcia-Robledo et al 2017) that are apparently anoxic. Whereas, "dark oxygen" produced by means of dismutation reactions is thought to provide potential sustenance to aerobic microbial communities in acutely O 2 -limited ancient groundwater ecosystems (Ruff et al 2023), minute spatiotemporal variations in the O 2 level of the chemical milieu have been hypothesized as the key driver of the stable cooccurrence of aerobic and anaerobic microorganisms in anoxic marine waters (Zakem et al 2020).…”