Spatial and Temporal Dynamics of Microorganisms Living Along Steep Energy Gradients and Implications for Ecology and Geologic Preservation in the Deep Biosphere

Abstract

The deep biosphere represents a massive repository of life with unknown effects on global biogeochemical cycles. Even the fundamental life strategies of the endemic microorganisms that inhabit this biome remain enigmatic; some studies have indicated that subsurface organisms subsist in energetic regimes below the theoretical lower limit for life. A boom-bust life cycle, mediated by tectonic disturbances and subsurface fractures, may help explain these phenomena. This work addresses and expands on this question, first by exploring the response of continental deep biosphere microorganisms to an in situ organic matter amendment, then by analyzing the microbial community dynamics of the sediments and carbonate along a naturally-occurring energy gradient at a methane seep. Our experiments in the continental deep biosphere confirmed that mineralogical heterogeneity can drive differential colonization of the native microorganisms, implying that selection and adaptation to in situ conditions occurs, differentiating individual microbial niches. We also observed the formation of secondary framboidal iron sulfide minerals, a well-known phenomenon in marine sediments but not extensively observed in the deep subsurface, that were correlated to the presence of abundant sulfur-metabolizing microorganisms. Chapters 2 and 3 are instead focused on the microbial ecology of a methane seep on the Pacific margin of Costa Rica. Cold methane seeps themselves represent sharp boundaries between the generally low-energy background seafloor and abundant chemical energy in the form of methane. Chapter 2 describes that the microorganisms living at these seeps occupy a significantly narrower spatial scale than the endemic megafauna. In addition, by correlating community dissimilarity and geographic distance, the functional center of the seep was identified, allowing for insight into the ecological differentiation between clades of anaerobic methanotrophic archaea (ANME). Chapter 3 examines in greater detail the endolithic microbial community, principally composed of ANME-1. By conducting transplantation experiments of carbonates on the seafloor, we tested the response of the in situ endolithic communities and found that carbonates moved distinctly outside the active zone changed less than communities moved to regions of less activity.