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

Abstract

Dissolution of anthropogenic CO 2 increases the partial pressure of CO 2 (pCO 2 ) and decreases the pH of seawater. The rate of Fe uptake by the dominant N 2 -fixing cyanobacterium Trichodesmium declines as pH decreases in metal-buffered medium. The slower Fe-uptake rate at low pH results from changes in Fe chemistry and not from a physiological response of the organism. Contrary to previous observations in nutrient-replete media, increasing pCO 2 /decreasing pH causes a decrease in the rates of N 2 fixation and growth in Trichodesmium under low-Fe conditions. This result was obtained even though the bioavailability of Fe was maintained at a constant level by increasing the total Fe concentration at low pH. Short-term experiments in which pCO 2 and pH were varied independently showed that the decrease in N 2 fixation is caused by decreasing pH rather than by increasing pCO 2 and corresponds to a lower efficiency of the nitrogenase enzyme. To compensate partially for the loss of N 2 fixation efficiency at low pH, Trichodesmium synthesizes additional nitrogenase. This increase comes partly at the cost of down-regulation of Fe-containing photosynthetic proteins. Our results show that although increasing pCO 2 often is beneficial to photosynthetic marine organisms, the concurrent decreasing pH can affect primary producers negatively. Such negative effects can occur both through chemical mechanisms, such as the bioavailability of key nutrients like Fe, and through biological mechanisms, as shown by the decrease in N 2 fixation in Fe-limited Trichodesmium.climate change | cyanobacteria | iron limitation A bout one-third of the anthropogenic CO 2 released into the atmosphere dissolves into the surface ocean, increasing the partial pressure of CO 2 , pCO 2 , and lowering the pH. This ocean acidification has been shown to have various consequences for marine phytoplankton (1-5). Organisms that invest a large amount of energy in the operation of a carbon-concentrating mechanism (CCM) are expected to be particularly sensitive to changes in pCO 2 . This is the case for marine cyanobacteria, which must elevate the CO 2 concentration at the site of carbon fixation as a result of the poor affinity for CO 2 of their carboxylating enzyme, ribulose bisphosphate carboxylase oxygenase (RubisCO) (6). Of particular interest is the effect of ocean acidification on the N 2 -fixing filamentous cyanobacterium Trichodesmium, which is responsible for a major fraction of all marine N 2 fixation and thus plays a prominent role in the biogeochemical cycling of C and N (7). This bloom-forming diazotroph thrives throughout the oligotrophic tropical and subtropical oceans where P and/or Fe often limit its growth and N 2 fixation (8-10).In the past few years, the effects of ocean acidification on Trichodesmium have been studied extensively in combination with those of other environmental variables, such as temperature, light intensity, and phosphorus limitation. Stimulation of N 2 fixation and growth at elevated pCO 2 has been observed in both la...

Symbiosis revisited: phosphorus and acid buffering stimulate N<sub>2</sub> fixation but not <i>Sphagnum</i> growth

“…However, a second plausible explanation for the increase in N 2 fixation activity is a direct beneficial effect of the increase in pH in the surface water on microbial growth rates and diazotrophic activity. It is indeed known for aquatic systems that dominant diazotrophs can be inhibited by a decrease in pH (Shi et al, 2012) and for agricultural soils that diazotrophic communities are larger in higher pH soils (Silva et al, 2013). In addition, the stimulated N 2 fixation may be explained by an indirect effect of increased decomposition rates as a result of buffering (Smolders et al, 2002), leading to the mobilization of additional organic compounds and nutrients from the soil to the surface water.…”

“…Field conditions of the site where the mosses were collected are shown in Table 1. To mimic their natural habitat, including moist conditions and supply of substrate-derived CO 2 for Sphagnum development (Smolders et al, 2001), peat mosses were placed on Sphagnum peat monoliths. Both peat mosses and monoliths were collected from the Ilperveld peatland in the Netherlands (52 • 26 22.68 N; 4 • 56 54.8 E), where monoliths (25 × 12 × 20 cm depth) were placed in glass mesocosms (25 × 12 × 30 cm depth) and then transported to the lab.…”

Ocean acidification impacts on nitrogen fixation in the coastal western Mediterranean Sea

“…Spungin et al (2014) found 10 that P limitation actually led to an enhancement of the OA stimulation of N 2 fixation 11 by Trichodesmium. It would appear that limiting quantities of P might enhance 12 diazotrophy, Shi et al (2012) found that N 2 fixation rates of Trichodesmium were 13 impaired under conditions of iron depletion. Fu et al (2008) performed similar studies 14 on the unicellular cyanobacterium Crocosphaera watsonii to find that under iron 15 replete conditions N 2 fixation rates were enhanced at a pCO 2 of 750 µatm, compared 16 to iron deplete conditions where no effect was observed.…”

“…A negative impact of OA 17 was also recorded, in Nodularia spumigena, a heterocystous diazotroph common to 18 the Baltic sea (Czerny et al, 2009), where cell division rates and nitrogen fixation 19 rates were reduced at CO 2 levels up to 731 ppm. Results from this small number of 20 laboratory studies imply that N 2 fixation can be stimulated by OA, but that there may 21 be a relationship with the nutrient regime and particularly the bioavailable iron 22 concentration (Fu et al, 2008, Shi et al, 2012, and that this may vary between 23 different diazotrophic organisms. 24 The available evidence of OA impacts on natural communities of diazotrophs 1 is even more limited.…”

Processes and patterns of oceanic nutrient limitation

“…For example, model studies indicate that direct physiological responses to increasing temperature could potentially influence primary (although not export) production by a magnitude comparable to the influence of increased stratification 71,88 . Future warming and higher carbon dioxide concentrations may also influence diazotrophic growth rates 85,87,89 , potentially altering nitrogen inputs and/or phosphorus and iron uptake and hence the stoichiometry of N:P:Fe cycling in low-latitude nitrogen-limited regions (Figs 1b,c and 3). In the high latitudes, increases in stratification might increase seasonal light availability for phytoplankton and hence overall productivity 51 .…”