Flexible elemental stoichiometry in Trichodesmium spp. and its ecological implications

We conducted laboratory experiments to assess the bioelemental plasticity of cultures of Trichodesmium IMS101 under phosphorus (P)-replete, P-restricted, and light-limited conditions. The results reveal a high degree of stoichiometric flexibility. Specifically, Trichodesmium IMS101 is capable of growth with carbon (C) : nitrogen (N) : P ratios of C585656 : N90610 : P1, approximately six times higher than would be predicted by the Redfield reference ratio (C106 : N16 : P1), thus signifying low cellular P quotas relative to C and N. Luxury consumption of P occurs rapidly after periods of prolonged P restriction, under both light and dark conditions, resulting in substantial increases in P quotas and reductions of C : N : P ratios (C9668 : N1661 : P1). Comparisons of laboratory culture data to our field observations from the Northwest Atlantic and the North Pacific indicate that, while natural populations of Trichodesmium exhibit persistently low P content relative to C and N (C290615 : N5363 : P1), the highest and lowest C : P and N : P ratios recorded in the laboratory are rarely observed in nature. We have also performed laboratory experiments intended to simulate the energetic and nutritional extremes that would occur as naturally migrating populations of Trichodesmium sink out of the euphotic zone into P-rich regions of the upper disphotic zone. The duration of dark survival for this isolate is on the order of 3–6 d, after which time cells are unable to recover from light deprivation. This finding provides a constraint on the temporal scale of vertical migration. Species of the colony-forming marine cyanobacterial genus Trichodesmium have been well described as prominent dinitrogen (N2) fixing organisms (diazotrophs) in the oligotrophic tropical and subtropical regions of the global ocean (Capone 2001; Karl et al. 2002). The notoriety of this genus has only increased in recent years as revisions of abundance estimates and N2 fixation rates have emphasized Trichodesmium as a significant source of new nitrogen to otherwise nitrogen (N)-deficient ecosystems (LaRoche and Breitbarth 2005). More than just a delivery vehicle for reactive N (NR), Trichodesmium spp. are also noted for their ability to episodically form large surface accumulations, thereby transiently dominating primary productivity and N cycling (Bowman and Lancaster 1965; Karl et al. 1992; Capone et al. 1998). Trichodesmium is ecologically significant in oligotrophic oceanic regimes, such as the North Atlantic and North Pacific gyres, where the process of biological N2 fixation has been documented to seasonally enhance the net transport of carbon (C) and nitrogen (N) out of the euphotic zone (Karl et al. 1997; Capone et al. 2005). Given that Trichodesmium-based productivity is by nature stochastic, a composite understanding of the role of this genus in elemental cycling will require characterization of physiological variability rather than just the biological averages. Specifically, if we can define the range of physiological and stoichiometric flexibility and begin to understand the underlying functionality driving deviations from average elemental composition, we will improve our capability to predict potential responses of oligotrophic marine ecosystems to the stresses imposed by a changing environment. Assuming a fixed elemental stoichiometry for marine biota, e.g., the Redfield reference ratio (Redfield 1958), requires that the internal chemical content of cells is strictly regulated. From this perspective, variable stoichiometry must be the consequence of the modulation of the relative proportions or the governing transformation rates of intracellular pools of biomolecules. In the North Pacific Subtropical Gyre (NPSG), a fundamental characteristic of increased Trichodesmium productivity is a systematic alternation of the particulate and dissolved elemental pools relative to the canonical Redfield ratios (C106 : N16 : P1) occurring as a primary result of the excess production of NR through N2 fixation (Karl et al. 1997; Dore et al. 2002). Particularly during bloom periods, the stoichiometric 1 Corresponding author ([email protected]).