Abstract
The crustal sub-seafloor covers a large portion of the Earth’s surface but is poorly understood as a habitat for life. It is unclear what metabolisms support the microscopic cells that have been observed, and how they survive under resource limitation. As the deep crustal subsurface represents a significant portion of the Earth’s surface, microbially-mediated reactions may therefore be significant contributors to biogeochemical cycling. In the present study, we used electrochemical techniques to investigate the possibility that crustal subsurface microbial groups can use the solid rock matrix (basalts, etc.) as a source of electrons for redox reactions via extracellular electron transfer (EET). Subsurface crustal fluids and mineral colonization experiments from the cool and oxic basaltic crustal subsurface at the North Pond site on the western flank of the Mid-Atlantic Ridge were used as inocula in cathodic poised potential experiments. Electrodes in oxic microbial fuel cells were poised at -200 mV versus a standard hydrogen electrode to mimic the delivery of electrons in an energy range equivalent to iron oxidation. In this way, microbes that use reduced iron in solid minerals for energy were selected for from the general community onto the electrode surface for interrogation of extracellular electron transfer activity, and potential identification by scanning electron microscopy and DNA sequencing. The results document that there are cathodic EET-capable microbial groups in the low biomass crustal subsurface at this site. The patterns of current generation in the experiments indicate that these microbial groups are active but likely not growing under the low-resource condition of the experiments, consistent with other studies of activity versus growth in the deep biosphere. Lack of growth stymied attempts to determine the phylogeny of EET-capable microbial groups from this habitat, but the results indicate that these microbial groups are a small part of the overall crustal deep biosphere community. This first demonstration of using electromicrobiology techniques to investigate microbial metabolic potential in the crustal deep biosphere reveals the challenges and opportunities for studying EET in the crustal deep biosphere.
Highlights
Oceanic crust and fluids represent a significant portion of the Earth’s habitable volume (Edwards et al, 2005; Orcutt et al, 2011b), and may be an important contributor to biogeochemical cycling based on volume alone (Shah Walter et al, 2018)
The result of our experiment suggests that: (1) replicating the Fe2/O2 redox couple with poised potential at −200 mV may be impacted by sulfide from the metal sulfides, (2) microbial communities colonizing the metal sulfides preferred other redox reactions than those involving Fe2/O2, (3) in situ electron transfer (EET)-capable microbial communities preferentially colonize the dominant substrate versus minor components of the crust at this site, or (4) that EET-capable microbes on pyrrhotite may have remained attached to the mineral and did not migrate to the electrode
Instead of removing any sequence groups that appeared in any no template control (NTC) from sample sequence libraries, we present the full results of all taxonomic groups in all samples including NTCs (Figures 6, 7), with samples grouped by treatment type rather than by experiment, to show trends more clearly
Summary
Oceanic crust and fluids represent a significant portion of the Earth’s habitable volume (Edwards et al, 2005; Orcutt et al, 2011b), and may be an important contributor to biogeochemical cycling based on volume alone (Shah Walter et al, 2018). Oxidation of reduced iron bound in cool, oxic crustal basalts may be an important source of chemolithotrophic energy for supporting a crustal biosphere (Orcutt et al, 2013b; Barco et al, 2017). Theoretical calculations suggest that the oxidation of iron and sulfur can support 41 ± 21 × 1010 g C per year of autotrophic biomass carbon formation (Bach and Edwards, 2003), approximating recent estimates of a carbon fixation rate of 109–1012 g C per year based on incubation experiments with globally distributed basalts (Orcutt et al, 2015). Cultivation-based studies indicate the presence of autotrophic and heterotrophic iron oxidation metabolisms in oceanic crust (Edwards et al, 2003a,b, 2004; Meyer et al, 2016; Russell et al, 2016). If microbial oxidation of iron in the solid crustal matrix is occurring in subseafloor ocean crust, this could have implications for the redox alteration state of oceanic crust over time, and on in-filling of vein networks with secondary alteration products that might affect fluid flow
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