A delta13C-based carbon flux model for the hydrothermal vent chemoautotrophic symbiosis Riftia pachyptila predicts sizeable CO(2) gradients at the host-symbiont interface

The chemoautotrophic symbiosis Riftia pachyptila has extremely 13C-enriched delta13C values. Neither isotopic discrimination by the RubisCO enzyme of their bacterial endosymbionts, nor the delta13C value of CO2 at their hydrothermal vent habitat, suffice to explain biomass delta13C values in this organism, which range from - 9 to - 16 per thousand. However, these 13C-enriched delta13C values are consistent with the presence of 13C-enriched CO2 within the symbiont cytoplasm. Such a 13C-enriched pool of CO2 is expected when the rate of CO2 fixation by RubisCO, which fixes 12CO2 more rapidly than 13CO2, approaches the rate of exchange between intracellular and extracellular CO2 pools. Rapid CO2 fixation rates will also generate concentration gradients between these two pools. In order to estimate the size of these concentration gradients, an equation was derived, which describes the delta13C of tubeworm biomass in terms of the size of the CO2 gradient between the hydrothermal vent environment and the symbiont cytoplasm. Using mass balance equations for CO2 exchange and fixation by the symbionts and the tubeworm host, this model predicts that a CO2 concentration gradient of up to 17-fold between the symbiont cytoplasm and the environment is sufficient to explain even the most 13C-enriched R. pachyptila biomass. This model illustrates how both physical and enzymatic factors can act to influence the delta13C of intracellular CO2, which, in turn, highlights the danger of assigning a carbon fixation pathway to an autotroph based solely on its biomass delta13C value.