Biogeochemical Cycling and Metabolic Flexibility in the Lower Oceanic Crust

The difficult to access plutonic lower oceanic crust is one of Earth’s last biological frontiers. Limited and temporally unpredictable sources of carbon and energy in this environment dictate survival strategies used by low biomass microbial communities. We report studies of rock samples spanning 10-750 meters below seafloor at Atlantis Bank, Indian Ocean, where the Earth’s lower crust is exposed at the seafloor by faulting. Assays of enzyme activities, lipid biomarkers, marker genes, and microscopy indicate heterogeneously distributed and viable biomass with ultra-low cell densities (<2000 cells/cm³). Along with the familiar autotrophic processes such as sulfur oxidation, unexpected active heterotrophic processes were detected using analyses of gene expression. These include degradation of polyaromatic hydrocarbons, use of polyhydroxyalkanoates as carbon storage molecules, and recycling of amino acids to produce compounds that can participate in redox reactions, energy production and storage. Microorganisms in the plutonic crust appear able to survive within fractures by coupling sources of energy and both organic and inorganic carbon likely delivered via subseafloor hydrothermal fluid or seawater circulation. Such metabolic flexibility may confer a competitive advantage to microorganisms occurring in this environment, which may make non-trivial contributions to global nutrient cycling.