Characterizing cobalamin cycling by Antarctic marine microbes across multiple scales

Abstract

Highly productive marine microbial communities in the coastal Southern Ocean sustain the broader Antarctic ecosystem and play a key role in Earth’s climate via the biological pump. Regional phytoplankton growth is primarily limited by iron and co-limited by cobalamin (vitamin B12), a trace cobalt-containing organometallic compound only synthesized by some bacteria and archaea. These micronutrients impact primary production and the microbial ecology of the two keystone phytoplankton types: diatoms and Phaeocystis antarctica. This thesis investigates microbe-driven cobalamin cycling in Antarctic seas across multiple spatiotemporal scales. I conducted laboratory culture experiments with complementary proteomics and transcriptomics to investigate the B12-ecophysiology of P. antarctica strain CCMP 1871 morphotypes under iron-B12 co-limitation. We observed colony formation under higher iron treatments, and a facultative use of B12-dependent (MetH) and B12-independent (MetE) methionine synthase isoforms in response to vitamin availability, demonstrating that this strain is not B12-auxotrophic. Through comparative ’omics, we identified a putative MetE protein in P. antarctica abundant under low B12, which is also found in other marine microbes. Across Antarctic seas, community-scale cobalt and B12 uptake rates were measured by 57Co radiotracer incubation experiments and integrated with hydrographic and phytoplankton pigment data. I observed significant correlations between uptake fluxes and environmental variables, providing evidence for predominantly diatom-driven uptake of these micronutrients in warmer, fresher surface waters with notable regional differences. To date, this work is the most comprehensive attempt to elucidate the processes governing the co-cycling of cobalt and B12 in any marine system. At the ecosystem-scale, I developed and tested a hypothesis of micronutrient-driven community dynamics through a trait-based model with cross-feeding interactions. The model demonstrates how the observed seasonal succession of springtime P. antarctica from solitary to colonial cells, bacterioplankton, and summertime diatoms may be explained by the microbial cycling of iron, dissolved organic carbon, and B12. Overall, this dissertation provides new information about the micronutrient-driven ecology of Antarctic marine microbes and adds to our understanding of the interconnections between organismal life cycle, trace metals, and trace organics in marine environments.