Influence of vitamin B auxotrophy on nitrogen metabolism in eukaryotic phytoplankton

Erin M. Bertrand, Andrew E. Allen

While nitrogen availability is known to limit primary production in large parts of the ocean, vitamin starvation amongst eukaryotic phytoplankton is becoming increasingly recognized as an oceanographically relevant phenomenon. Cobalamin (B(12)) and thiamine (B(1)) auxotrophy are widespread throughout eukaryotic phytoplankton, with over 50% of cultured isolates requiring B(12) and 20% requiring B(1). The frequency of vitamin auxotrophy in harmful algal bloom species is even higher. Instances of colimitation between nitrogen and B vitamins have been observed in marine environments, and interactions between these nutrients have been shown to impact phytoplankton species composition. This review surveys available data, including relevant gene expression patterns, to evaluate the potential for interactive effects of nitrogen and vitamin B(12) and B(1) starvation in eukaryotic phytoplankton. B(12) plays essential roles in amino acid and one-carbon metabolism, while B(1) is important for primary carbohydrate and amino acid metabolism and likely useful as an anti-oxidant. Here we will focus on three potential metabolic interconnections between vitamin, nitrogen, and sulfur metabolism that may have ramifications for the role of vitamin and nitrogen scarcities in driving ocean productivity and species composition. These include: (1) B(12), B(1), and N starvation impacts on osmolyte and antioxidant production, (2) B(12) and B(1) starvation impacts on polyamine biosynthesis, and (3) influence of B(12) and B(1) starvation on the diatom urea cycle and amino acid recycling through impacts on the citric acid cycle. We evaluate evidence for these interconnections and identify oceanographic contexts in which each may impact rates of primary production and phytoplankton community composition. Major implications include that B(12) and B(1) deprivation may impair the ability of phytoplankton to recover from nitrogen starvation and that changes in vitamin and nitrogen availability may synergistically impact harmful algal bloom formation.