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

다국어 초록 (Multilingual Abstract)

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 (δ13C) of bulk organic and inorganic phases, followed by organic geochemical analysis of the distribution and δ13C 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 (δ13CVPDB ∼ −30‰), whereas biofilms are dominated by strongly 13C‐depleted lipids (minimum δ13CVPDB −45.4‰) 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 13C‐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.
Microorganisms live underground at a range of depths and habitat types, but what these organisms eat is poorly understood. Lava caves are relatively shallow underground environments that commonly host colorful microbial biofilms on the rock walls. We examine the carbon sources used by these and other microbial communities at Lava Beds National Monument, CA, by tracking the flow of carbon into cell membrane lipids via compound‐specific isotope analysis. By comparing the stable carbon isotope signatures (δ13C) of potential carbon sources to those of cave features, we conclude that biofilm communities actively fix inorganic carbon rather than assimilate the abundant organic carbon found in cave fluids, as do microbes in other sample types. This process requires a source of energy; in the absence of photosynthesis, these microbes must instead gain their energy from inorganic mineral‐ and fluid‐derived sources. While caves are generally thought to host organic carbon‐consuming microbes, our results challenge this paradigm and have widespread implications for cave habitation on Earth and the solar system. Lava caves are common on Mars, the surface of which is likely too harsh to support life. Our results suggest that cave microbial communities may be well adapted to independent life underground.



Lava cave biofilms contain a diverse and unusual array of fatty acid biomarkers, including branched saturated and trans‐unsaturated isomers

Fatty acids likely produced by Actinobacteria in biofilms bear carbon isotopic signatures that require in situ subsurface carbon fixation

Biomass from other cave features, such as mineral‐rich speleothems, assimilate surface‐derived organic carbon based on isotopic signatures


Lava cave biofilms contain a diverse and unusual array of fatty acid biomarkers, including branched saturated and trans‐unsaturated isomers
Fatty acids likely produced by Actinobacteria in biofilms bear carbon isotopic signatures that require in situ subsurface carbon fixation
Biomass from other cave features, such as mineral‐rich speleothems, assimilate surface‐derived organic carbon based on isotopic signatures