Evolutionary response of marine bacteria to the co-occurring pnictogens phosphorus and arsenic

Abstract

Phosphorus is an essential component of biomolecules, and is believed to be the limiting nutrient in the marine environment on geologic timescales. In marine waters, phosphorus co-occurs with arsenic, an element with many similar chemical properties. The occurrence of these two elements has shaped the evolutionary trajectory of the microorganisms that thrive in marine waters, and conversely, biochemical transformations by marine microorganisms influence the global cycling of these elements. Chapter 1 demonstrates the response of the marine Picocyanobacterium Prochlorococcus strain MED4 to phosphorus stress through a proteomic analysis of cells exposed to nutrient starvation and long-term nutrient limitation. A biogeographic analysis of some of the most differentially expressed proteins under phosphorus stress highlights the selective force of phosphorus scarcity on the genomic capacity of environmental Prochlorococcus populations. In Chapter 2, the inextricable link between the cycling of phosphorus and arsenic is highlighted in the evolutionary response of Prochlorococcus arsenic detoxification mechanisms, where populations which experience greater phosphorus scarcity, and therefore greater risk of cellular arsenic exposure, show greater genomic capacity for arsenic detoxification. The arsenic detoxification mechanisms outlined in Chapter 2 utilize one of the few physicochemical differences between P and As – the different reduction potentials – in the process of detoxification. Chapter 3 describes a different group of marine microorganisms which also exploit the reduction potential of arsenic, but in this case for bioenergetic gains in anoxic marine waters. The genomic capacity for a complete arsenic metabolic cycle is described, with gene presence and expression of dissimilatory arsenate reductase and a chemoautotrophic form of arsenite oxidase in anoxic pelagic waters. This thesis highlights the selective pressures of phosphorus and arsenic availability on the evolution of marine microbial communities.