Stable Carbon Isotope Depletions in Lipid Biomarkers Suggest Subsurface Carbon Fixation in Lava Caves

Lava caves, formed through basaltic volcanism, are accessible conduits into the shallow subsurface and the microbial life residing there. While evidence for this life is widespread, the level of dependence of these microbial communities on surface inputs, especially that of organic carbon (OC), is a persistent knowledge gap, with relevance to both terrestrial biogeochemistry and the characterization of lava caves as Mars analog environments. Here, we explore carbon cycling processes within lava caves at Lava Beds National Monument, CA. We interrogate a range of cave features and surface soils, characterizing the isotopic composition (delta C-13) of bulk organic and inorganic phases, followed by organic geochemical analysis of the distribution and delta C-13 signatures of fatty acids derived from intact polar lipids (IPLs). From these data, we estimate the carbon sources of different sample types, finding that surface soils and mineral-rich speleothems incorporate plant-derived biomass (delta C-13(VPDB) similar to -30 parts per thousand), whereas biofilms are dominated by strongly C-13-depleted lipids (minimum delta C-13(VPDB) -45.4 parts per thousand) specific to bacteria, requiring a significant proportion of their biomass to derive from in situ fixation of inorganic carbon from previously respired OC. Based on the prevalence and abundance of these C-13-depleted lipids, we conclude that biofilms here are fueled by in situ chemolithoautotrophy, despite relatively high concentrations of dissolved OC in colocated cave waters. This unexpected metabolic potential mirrors that found in other deep subsurface biospheres and has significant positive implications for the potential microbial habitability of the Martian subsurface.

Automated summary

By studying carbon cycling processes in lava caves, it was found that biofilms within the caves primarily derive their energy from in situ chemolithoautotrophy, despite the presence of relatively high concentrations of dissolved organic carbon in cave waters. The C-13-depleted lipids in the biofilms suggest that a significant proportion of their biomass is derived from in situ fixation of inorganic carbon from previously respired organic carbon.