Environmental niche partitioning of microbial community genomic diversity, gene expression, and metabolism in a marine oxygen minimum zone

Abstract

Oxygen Minimum Zones (OMZs) serve as habitats to diverse assemblages of microorganisms that play an important role in mediating global biogeochemical cycles. OMZ microbial communities have not been extensively characterized, and the linkages between microbial community structure, and ecological and biogeochemical processes are still unclear. OMZs act as model systems to study partitioning of microbial niches and biogeochemical transformations owing to their steep vertical gradients of oxygen, nutrient, and redox substrates. This thesis combined genomic tools with environmental measurements of nitrogen transformation rates to characterize how microbial community structure, function and ecological diversity vary at the microscale between free-living (planktonic) and particle-associated microbial communities and over vertical and longitudinal gradients in two of the world’s largest permanent OMZs. The results show an important role for particle-association as a major driver of OMZ microbial community metabolic potential and genome content, and identify wide variation in nitrogen transformation rates in the presence versus absence of particles. These results highlight the dependence of free-living microorganisms on particles for substrates and nutrients, as well as selective partitioning of genes facilitating key steps of an important nitrogen loss pathway, denitrification, in the particle-associated microbial fraction. Finally, this thesis describes the genomic composition and gene expression variation of an important OMZ bacterium, Candidatus Scalindua sp., responsible for anaerobic ammonia oxidation (anammox), the second major nitrogen loss pathway in OMZs. Combining single cell genomics, transcriptome profiling, and rate measurements, this study identifies high metabolic plasticity of OMZ anammox bacteria in different niches along the OMZ redoxcline, including a potential for use of diverse nitrogen substrates to drive anammox. Collectively, these studies enhance our understanding of the environmental determinants of microbial diversity and biochemical activity in low oxygen marine systems.