Biogeochemical and phylogenetic signals of Proterozoic and Phanerozoic microbial metabolisms

Abstract

Life is ubiquitous in the environment and an important mediator of Earth's carbon cycle, but quantifying the contribution of microbial biomass and its metabolic fluxes is difficult, especially in spatially and temporally-remote environments. Microbes leave behind an often scarce, unidentifiable, or nonspecific record on geologic timescales. This thesis develops and employs novel geochemical and genetic approaches to illuminate diagnostic signals of microbial metabolisms. Field studies, laboratory cultures, and computational models explain how methanogens produce unique nonequilibrium methane clumped isotopologue (1 3CH3D ) signals that do not correspond to growth temperature. Instead, [Delta]13CH3D values may be driven by enzymatic reactions common to all methanogens, the C-H bond inherited from substrate precursors including acetate and methanol, isotope exchange, or environmental processes such as methane oxidation. The phylogenetic relationship between substrate-specific methyl-corrinoid proteins provides insight into the evolutionary history of methylotrophic methanogenesis. The distribution of corrinoid proteins in methanogens and related bacteria suggests that these substrate-specific proteins evolved via a complex history of horizontal gene transfer (HGT), gene duplication, and loss. Furthermore, this work identifies a previously unrecognized HGT involving chitinases (ChiC/D) distributed between fungi and bacteria (~650 Ma). This HGT is used to tether fossil-calibrated ages from within fungi to bacterial lineages. Molecular clock analyses show that multiple clades of bacteria likely acquired chitinase homologs via HGT during the late Neoproterozoic into the early Paleozoic. These results also show that, following these HGT events, recipient terrestrial bacterial clades diversified ~400-500 Ma, consistent with established timescales of arthropod and plant terrestrialization. Divergence time estimates for bacterial lineages are broadly consistent with the dispersal of chitinase genes throughout the microbial world in direct response to the evolution and expansion of detrital-chitin producing groups including arthropods. These chitinases may aid in dating microbial lineages over geologic time and provide insight into an ecological shift from marine to terrestrial systems in the Proterozoic and Phanerozoic eons. Taken together, this thesis may be used to improve assessments of microbial activity in remote environments, and to enhance our understanding of the evolution of Earth's carbon cycle.