On the Origin of Thermophilic Endospores

Abstract

Marine sediment covers ~70% of Earth’s surface. Diverse microbial populations inhabit the subseafloor biosphere substantially contributing to global biomass. Patterns demonstrating microbial biogeography are well established in many environments, but conspicuous examples of thermophilic endospores in permanently cold seabed sediments highlight how the ecological processes controlling biogeography in the deep biosphere remain poorly understood. This thesis examines environmental selection in subsurface petroleum reservoirs and assesses large scale microbial dispersal associated with these habitats to better understand the factors shaping microbial communities. The diversity in the global petroleum reservoir microbiome was assessed by examining 16S rRNA gene amplicon and shotgun metagenomic libraries from oil reservoirs around the world. Taxonomic composition varies among reservoirs with different physicochemical characteristics, and by geographic location, yet gene composition analysis highlights a common functional core. Shared functions include diverse capabilities for carbon acquisition and energy conservation consistent with metabolisms characteristic of the deep biosphere. Taxonomic variation with functional redundancy demonstrates environmental selection acting in these subsurface biogeochemical hotspots. Firmicutes are among the most prevalent taxa, while genetic potential for sporulation is widespread. Correlation of geophysical and geochemical evidence of hydrocarbon seepage with biogeographic patterns in the seabed distributions of endospores of thermophilic bacteria reveals geofluid-facilitated cell migration pathways connecting petroleum reservoirs with the surface. Genomic sequencing in high temperature incubations highlight adaptations of these microorganisms to life in anoxic petroleum systems, while phylogenetic comparisons reveal close resemblance to oil reservoir microbiomes globally. Microbial activity and selection of diverse populations of Firmicutes in crude oil-amended incubations further validates the origin of these thermophilies. Upon transport out of the subsurface, viable endospores re-enter the geosphere by sediment burial, enabling germination and environmental selection at depth where new petroleum systems establish. This newly termed ‘microbial dispersal loop’ circulates living biomass in and out of the deep biosphere. Microbial ecology and Earth system processes are tightly linked. Deep biosphere populations possess extensive physiological and metabolic diversity and influence biogeochemical cycling on a global scale. By connecting geology and geological frameworks with factors that influence survival and evolution, the geosphere can be a model system to better understand microbial ecology.