Lithogenic hydrogen supports microbial primary production in subglacial and proglacial environments

Abstract

Life in environments devoid of photosynthesis, such as on early Earth or in contemporary dark subsurface ecosystems, is supported by chemical energy. How, when, and where chemical nutrients released from the geosphere fuel chemosynthetic biospheres is fundamental to understanding the distribution and diversity of life, both today and in the geologic past. Hydrogen (H₂) is a potent reductant that can be generated when water interacts with reactive components of mineral surfaces such as silicate radicals and ferrous iron. Such reactive mineral surfaces are continually generated by physical comminution of bedrock by glaciers. Here, we show that dissolved H₂ concentrations in meltwaters from an iron and silicate mineral-rich basaltic glacial catchment were an order of magnitude higher than those from a carbonate-dominated catchment. Consistent with higher H₂ abundance, sediment microbial communities from the basaltic catchment exhibited significantly shorter lag times and faster rates of net H₂ oxidation and dark carbon dioxide (CO₂) fixation than those from the carbonate catchment, indicating adaptation to use H₂ as a reductant in basaltic catchments. An enrichment culture of basaltic sediments provided with H₂, CO₂, and ferric iron produced a chemolithoautotrophic population related to Rhodoferax ferrireducens with a metabolism previously thought to be restricted to (hyper)thermophiles and acidophiles. These findings point to the importance of physical and chemical weathering processes in generating nutrients that support chemosynthetic primary production. Furthermore, they show that differences in bedrock mineral composition can influence the supplies of nutrients like H₂ and, in turn, the diversity, abundance, and activity of microbial inhabitants.

Keywords: basalt; carbonate; chemoautotrophy; hydrogen; iron reduction.

Fig. 1.

H₂ content (A and C) and carbon fixation (B and D) in microcosms inoculated with proglacial or subglacial sediments from KJ (A and B) or RG (C and D), respectively, and incubated in the dark at 4 °C. The means and SDs of measurements from triplicate microcosms are presented. Abbreviations: Fh., ferrihydrite; gdws, gram dry weight sediment; Hem., hematite; HK, heat-killed control; Uninoc., uninoculated control.

Fig. 2.

Maximum H₂ oxidation rates in microcosms containing proglacial or subglacial sediments from KJ or RG, respectively, when incubated in the dark at 4 °C. Linear regressions were applied to selected data from the sets represented in Fig. 1 A and C, and the inverse of the slope of each regression is reported. Error bars represent the SD associated with the slope of each regression. Abbreviations: Fh., ferrihydrite; gdws, gram dry weight sediment; Hem., hematite; HK, heat-killed control; Uninoc., uninoculated control.

Fig. 3.

Maximum CO₂ fixation rates within microcosms containing proglacial or subglacial sediments from KJ or RG, respectively, when incubated in the dark at 4 °C. Linear regressions were applied to selected data from the sets represented in Fig. 1 B and D, and the slope of each regression is reported. Error bars represent the SD associated with the slope of each regression. Abbreviations: gdws, gram dry weight sediment; Hem., hematite; HK, heat-killed control. Microcosms were not amended with ferrihydrite for this experiment given the similar rates of H₂ oxidation in ferrihydrite- and hematite-amended microcosms.

Fig. 4.

Abundance of hydrogenotrophic cells capable of autotrophic growth as determined by most probable number (MPN) assays containing dilutions of proglacial or subglacial sediments from KJ or RG, respectively. The MPN was assessed first by quantifying total extractable DNA (A) and further refined by measurement of the metabolic products of CO₂, SO₄²⁻, Fe(III), or NO₃⁻ reduction (methane and/or acetate, sulfide, ferrous iron, and nitrite, respectively) (B). Microbial growth was detected in CO₂- and SO₄²⁻-amended microcosms without associated reduction of CO₂ or SO₄²⁻. This observation led to the hypothesis that growth under these conditions is supported by heterotrophy. Error bars represent 95% confidence intervals. Abbreviations: Ace., acetate; Fh., ferrihydrite; gdws, gram dry weight sediment; Hem., hematite.

Fig. 5.

Activity and growth of a KJ most probable number (MPN) culture amended with H₂, CO₂, and hematite when transferred into fresh medium containing these components. (Meta)genomic sequencing of DNA extracted from this culture reveals a single metagenome assembled genome affiliated (94% RpoB ID) with Rhodoferax ferrireducens. Culture Fe²⁺ content was calculated as the concentration of Fe²⁺ measured in the experimental microcosm minus that measured in the abiotic control. Error bars represent SEM. Abbreviations: AC, abiotic control; LOD, limit of detection.