Combined Effects of CO₂ and Light on the N₂-Fixing Cyanobacterium Trichodesmium IMS101: Physiological Responses

Abstract

Recent studies on the diazotrophic cyanobacterium Trichodesmium erythraeum (IMS101) showed that increasing CO 2 partial pressure (pCO 2 ) enhances N 2 fixation and growth. Significant uncertainties remain as to the degree of the sensitivity to pCO 2 , its modification by other environmental factors, and underlying processes causing these responses. To address these questions, we examined the responses of Trichodesmium IMS101 grown under a matrix of low and high levels of pCO 2 (150 and 900 matm) and irradiance (50 and 200 mmol photons m 22 s 21 ). Growth rates as well as cellular carbon and nitrogen contents increased with increasing pCO 2 and light levels in the cultures. The pCO 2 -dependent stimulation in organic carbon and nitrogen production was highest under low light. High pCO 2 stimulated rates of N 2 fixation and prolonged the duration, while high light affected maximum rates only. Gross photosynthesis increased with light but did not change with pCO 2 . HCO 3 2 was identified as the predominant carbon source taken up in all treatments. Inorganic carbon uptake increased with light, but only gross CO 2 uptake was enhanced under high pCO 2 . A comparison between carbon fluxes in vivo and those derived from 13 C fractionation indicates high internal carbon cycling, especially in the low-pCO 2 treatment under high light. Light-dependent oxygen uptake was only detected under low pCO 2 combined with high light or when low-light-acclimated cells were exposed to high light, indicating that the Mehler reaction functions also as a photoprotective mechanism in Trichodesmium. Our data confirm the pronounced pCO 2 effect on N 2 fixation and growth in Trichodesmium and further show a strong modulation of these effects by light intensity. We attribute these responses to changes in the allocation of photosynthetic energy between carbon acquisition and the assimilation of carbon and nitrogen under elevated pCO 2 . These findings are supported by a complementary study looking at photosynthetic fluorescence parameters of photosystem II, photosynthetic unit stoichiometry (photosystem I:photosystem II), and pool sizes of key proteins in carbon and nitrogen acquisition.

Interactions between CCM and N2 fixation in Trichodesmium

“…Rates of N 2 fixation followed the diurnal pattern in nitrogenase abundance and its post-translational modification, with highest activities during midday (Berman-Frank et al 2001b;Levitan et al 2010aLevitan et al , 2007Milligan et al 2007). The timing of both, demodification of the iron protein and nitrogenase activity was shown to be affected by light intensities (Kranz et al 2010a;Zehr et al 1996). The described diurnal pattern in cell division, protein build-up and degradation, as well as physiological activity may represent a mean for Trichodesmium to optimize its energy budget.…”

“…The increase in N 2 fixation or PON production under elevated pCO 2 (Barcelos é Ramos et al 2007;Hutchins et al 2007;Kranz et al 2009;Levitan et al 2007) was found to be caused by a prolongation of the N 2 fixation period (Kranz et al 2010a). As these enhanced N 2 fixation rates were not accompanied by larger protein pools of nitrogenase (Levitan et al 2010b), they may have been achieved by post-translational modification and/or higher energy availability for nitrogenase activity.…”

“…1 Combined effects of pCO 2 and light. Plots are based on data taken from Kranz et al (2010a) and Eichner et al (unpublished;pCO 2 180 vs. 950 latm at 300 lmol photons m -2 s -1 ). a Growth rates, b production rates of particulate organic carbon (POC), and c production rates of particulate organic nitrogen (PON) Photosynth Res can subsequently be taken up by the vegetative cells to fuel their N demand (Fig.…”

“…Oxygenic photosynthesis as well as respiration is conducted in both types of cells, generating the energy and reductants as well as carbon skeletons required for N assimilation. ADP adenosine-5 0 -diphosphate, ATP adenosine-5 0 -triphosphate, ATP synthase adenosine-5 0 -triphosphate synthase, Glu glutamate, GOGAT glutamine oxoglutarate aminotransferase, Gln glutamine, GS glutamine synthetase, P i inorganic phosphorus, PON particulate organic nitrogen, PSI photosystem 1, PSII photosystem 2, SDH succinate dehydrogenase Photosynth Res source of energy for N 2 fixation (Breitbarth et al 2008;Kranz et al 2010a) and as a cue for synthesis and/or demodification of nitrogenase (Zehr et al 1993). N 2 fixation rates, obtained from acetylene reduction assays, have been shown to increase up to light intensities of about 300 lmol photons m -2 s -1 (Bell and Fu 2005;Breitbarth et al 2008).…”

“…They differed, however, in the light intensities applied during incubations, which may serve as an explanation for the differences in CO 2 sensitivity. A recent companion study assessed the combined effect of pCO 2 (150 vs. 900 latm) and light (50 vs. 200 lmol photons m -2 s -1 ) and could indeed show that light levels do modify the responses of Trichodesmium to pCO 2 (Kranz et al 2010a;Levitan et al 2010b). Notably, the relative stimulation in growth, POC, or PON production rates was highest in the low-light treatment and diminished under high light (Fig.…”