Nitrate Assimilation and the Ecology of Prochlorococcus: Features and Implications of Intraspecific Diversity in a Model Marine Phototrophy

First discovered in 1988, Prochlorococcus is now recognized as the most abundant photosynthetic cell in the oceans and is responsible for a significant fraction of global primary productivity. Arguably one of the best studied marine microorganisms to date, Prochlorococcus is well-developed as a model system for advancing our understanding of microbial ecology. It is comprised of a collection of genetically and physiologically distinct populations that co-exist and are differentially distributed along quantifiable gradients of light, temperature, and inorganic nutrients. Early physiological studies using cultured isolates indicated that this group of cyanobacteria was unable to assimilate nitrate, typically the most abundant inorganic nitrogen source in the open ocean. This observation was supported by the first 12 genome sequences of Prochlorococcus which all lacked the genes necessary for nitrate assimilation. The lack of these genes in Prochlorococcus was puzzling given that closely related, and co-occurring, Synechococcus cells have them, and that nitrogen availability can be a significant limiting factor for primary production in marine ecosystems. Our understanding changed in 2009 with the discovery of nitrate assimilation genes in wild Prochlorococcus genomes and the isolation of an axenic strain capable of growth on nitrate (unpublished data). This discovery has lead to the overarching questions that are the subject of this project:

(*) What subset of the Prochlorococcus meta-population in the wild contains nitrate assimilation genes and how do the dynamics of this sub-population vary in time and space?

(*) What features of the environment select for cells with this functional trait?

(*) Is the phylogeny of Prochlorococcus nitrate assimilation genes better correlated with the local environment or the overall 16S-23S ITS phylogeny of Prochlorococcus?

(*) Do the genomes of cells that contain nitrate assimilation genes share specific features? What do they tell us about what other environmental variables influence the fitness of nitrate-assimilating cells?

(*0 What are the physiological tradeoffs underlying the loss or gain of assimilation genes in particular strains?

These questions will be addressed using an integrative cross-scale approach to characterize nitrate assimilation by Prochlorococcus at the population, cellular, and genomic levels. Specifically, the distribution and abundance of nitrate assimilating Prochlorococcus will be measured at two contrasting open ocean time-series stations (HOT and BATS), and along a longitudinal gradient in the Atlantic (AMT). The PI will examine the regulation of nitrate assimilation, the kinetics of growth on nitrate, and the ability of Prochlorococcus to compete with Synechococcus under nitrogen limiting conditions. Further, they will use a culture independent single cell genomics approach to assess the phylogenetic diversity of nitrate assimilation genes within the genomic context of several ribotypes. These studies will advance our understanding the biogeography of functional traits in microbes, how it is shaped by selection, and the role of intra-species functional diversity in the overall population dynamics of Prochlorococcus.