Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium

Abstract

Iron availability is suggested to be a primary factor limiting nitrogen fixation in the oceans. This hypothesis is principally based on cost-benefit analyses of iron quotas in the dominant nitrogen-fixing cyanobacteria, Trichodesmium spp., in the contemporary oceans. Although previous studies with Trichodesmium have indicated that iron availability enhanced nitrogen fixation and photosynthesis, no clear relationship has been reported between cellular iron quotas and nitrogen fixation. We re-examined the proposed link between iron availability and nitrogen fixation in laboratory isolates and natural populations collected from coastal waters north of Australia. In laboratory cultures grown under iron-limiting conditions, we measured a decline in cellular iron quotas, photochemical quantum yields, the relative abundance of photosystem I to photosystem II reaction centers, and rates of nitrogen fixation. Nitrogen fixation displayed a critical threshold of the dissolved sum of total inorganic Fe species ([FeЈ]) of ca. log[FeЈ] ϭ Ϫ9.7. Field populations of Trichodesmium, collected during bloom conditions, showed high iron quotas consistent with high nitrogen fixation rates. Using seasonal maps of aeolian iron fluxes and model-derived maps of surface water total dissolved Fe, we calculated the potential of nitrogen fixation by Trichodesmium in the global ocean. Our results suggest that in 75% of the global ocean, iron availability limits nitrogen fixation by this organism. Given present trends in the hydrological cycle, we suggest that iron fluxes will be even more limiting in the coming century.Nitrogen fixation by planktonic prokaryotes is a major source of new nitrogen for the oceans (Capone et al. 1997;. In all cyanobacteria, the enzyme responsible for this process, nitrogenase, consists of two proteins, an iron 1 Corresponding author (irfrank@imcs.rutgers.edu). AcknowledgmentsWe thank J. and Y. Reinfelder for their help with the tracer experiments, iron solubility, and MINEQLϩ calculations; H. M. Geller and N. Goldman from the Department of Pharmacology, Robert Wood Johnson Medical School, for help and access to the confocal laser; P. Ludden for the antibody to nitrogenase; D. Kolber for generating the global maps; K. Wyman for invaluable lab assistance; and D. Capone, E. Carpenter, and the crew of the R/V Ewing for enabling our field sampling. We also thank J. Prospero, F. M. M. Morel, and two anonymous reviewers for their comments.

Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions

“…In addition, the N 2 -fixation rate, which reaches a maximum at midday (23), was considerably slower at 750 ppm than at 380 ppm pCO 2 (P = 0.035 and 0.009, t test) (Table 1), with a decrease of 35% and 50% at low and high Fe′, respectively. As expected from previous studies, increasing Fe availability decreased the ratio of POC to particulate organic N (PON) (P = 0.026, t test; Table 1) and increased the chlorophyll a (Chl a):C (P = 0.01, t test) (24). However, pCO 2 /pH had no significant effect on either of these parameters.…”

Analogous nutrient limitations in unicellular diazotrophs and Prochlorococcus in the South Pacific Ocean

“…The low nutrient and low chlorophyll North Atlantic Ocean is thought to be one of the most iron-rich oceans owing to eolian inputs (Jickells et al, 2005) and has diverse communities of diazotrophs (Orcutt et al, 2001;Langlois et al, 2008). Actively N 2 -fixing Trichodesmium requires more Fe relative to non-diazotrophic phytoplankton (Berman-Frank et al, 2001), however in the Atlantic its growth was suggested to be either P (Sanudo-Wilhelmy et al, 2001;Hynes et al, 2009) or Fe (Lenes et al, 2001) limited. Co-limitation of bulk N 2 fixation by P and Fe was reported (Mills et al, 2004), suggesting both nutrients may become limiting for diazotrophs in this ocean basin, supported by recent in situ gene expression data (Webb et al, 2007).…”

Interactions between CCM and N2 fixation in Trichodesmium

“…As a key species in the marine ecosystem, Trichodesmium was used in several studies on the regulation of N 2 fixation (e.g., Berman-Frank et al 2001a, b, 2007Capone et al 2005;Kana 1993;Mulholland et al 2004). Unlike other diazotrophs, this species has evolved special features allowing N 2 fixation to occur during the photoperiod.…”

“…To protect the oxygen-sensitive enzyme nitrogenase, which catalyzes the reduction of N 2 to NH 3 , from photosynthetic O 2 evolution, this species has developed distinct diurnal rhythms in photosynthesis and N 2 fixation (Berman-Frank et al 2001b). By now, the genome of Trichodesmium IMS101 has been fully sequenced (US Department of Energy Joint Genome Institute http://www.jgi.doe.gov/) and several aspects of its ecophysiology have been studied, e.g., effects of phosphorus, iron limitation, temperature, salinity, and irradiance (Berman-Frank et al 2001a;Breitbarth et al 2008;Fu and Bell 2003). The potential influence of CO 2 -induced changes in seawater chemistry or combined effects of different environmental factors have, however, been ignored for a long time.…”