Cellular inorganic carbon fluxes in Trichodesmium: a combined approach using measurements and modelling.

Meri Eichner,Björn Rost,Silke Thoms,Sven A Kranz

doi:10.1093/jxb/eru427

Abstract

To predict effects of climate change on phytoplankton, it is crucial to understand how their mechanisms for carbon acquisition respond to environmental conditions. Aiming to shed light on the responses of extra- and intracellular inorganic C (Ci) fluxes, the cyanobacterium Trichodesmium erythraeum IMS101 was grown with different nitrogen sources (N2 vs NO3 (-)) and pCO2 levels (380 vs 1400 µatm). Cellular Ci fluxes were assessed by combining membrane inlet mass spectrometry (MIMS), (13)C fractionation measurements, and modelling. Aside from a significant decrease in Ci affinity at elevated pCO2 and changes in CO2 efflux with different N sources, extracellular Ci fluxes estimated by MIMS were largely unaffected by the treatments. (13)C fractionation during biomass production, however, increased with pCO2, irrespective of the N source. Strong discrepancies were observed in CO2 leakage estimates obtained by MIMS and a (13)C-based approach, which further increased under elevated pCO2. These offsets could be explained by applying a model that comprises extracellular CO2 and HCO3 (-) fluxes as well as internal Ci cycling around the carboxysome via the CO2 uptake facilitator NDH-14. Assuming unidirectional, kinetic fractionation between CO2 and HCO3 (-) in the cytosol or enzymatic fractionation by NDH-14, both significantly improved the comparability of leakage estimates. Our results highlight the importance of internal Ci cycling for (13)C composition as well as cellular energy budgets of Trichodesmium, which ought to be considered in process studies on climate change effects.

Highlights

Cyanobacteria are ancient organisms responsible for oxygenation of the atmosphere during times when CO2 concentrations were about two orders of magnitude higher than today
Taking the ratio of KM to half-saturation concentration (K1/2) as a measure of CO2 accumulation in the vicinity of RubisCO, our data suggest accumulation factors between ~35 and 900 and indicate that the degree of RubisCO saturation is always larger than 80%
As gross inorganic carbon (Ci) uptake was approximately twice as high as net C fixation at acclimation dissolved inorganic C (DIC) (~2100 μmol CO2 l–1), leakage measured by membrane inlet mass spectrometry (MIMS) ranged between 0.3 and 0.7 (i.e. CO2 efflux equalled 30–70% of gross Ci uptake; Table 1)

Summary

Introduction

Cyanobacteria are ancient organisms responsible for oxygenation of the atmosphere during times when CO2 concentrations were about two orders of magnitude higher than today (cf. Buick, 1992; Kasting and Siefert, 2002). Due to their origin at that time, the CO2-fixing enzyme RubisCO of cyanobacteria has one of the lowest affinities among all autotrophic organisms (Badger et al, 1998; Tortell, 2000).

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