The carbon-concentrating mechanism of the hydrothermal vent chemolithoautotroph Thiomicrospira crunogena.

Abstract

Chemolithoautotrophic bacteria grow in habitats with a variety of dissolved inorganic carbon (DIC) concentrations and are likely to have transport-related adaptations to DIC scarcity. Carbon-concentrating mechanisms (CCMs) are present in many species of cyanobacteria, enabling them to grow in the presence of low concentrations of CO2 by utilizing bicarbonate transporters and CO2 traps to generate high intracellular concentrations of DIC. Similar CCMs may also be present in many other autotrophic bacteria. The sulfur-oxidizing γ-proteobacterial chemolithoautotroph Thiomicrospira crunogena experiences broad fluctuations in DIC availability at its hydrothermal vent habitat and may use a CCM to facilitate growth during periods of CO2 scarcity. T. crunogena was cultivated in chemostats under DIC limitation to determine whether it has a CCM. Its KDIC for growth was 0.22 mM, with a maximum growth rate of 0.44 h−1. In short-term incubations with [14C]DIC, DIC-limited cells had higher affinities for DIC (0.026 mM) than DIC-sufficient cells (0.66 mM). DIC-limited cells demonstrated an ability to use both extracellular CO2 and HCO3−, as assayed by isotopic disequilibrium incubations. These cells also accumulated intracellular DIC to concentrations 100× higher than extracellular, as determined using the silicone oil centrifugation technique. Cells that were not provided with an electron donor did not have elevated intracellular DIC concentrations. The inducible changes in whole-cell affinity for DIC, the ability to use both extracellular CO2 and HCO3−, and the energy-dependent generation of elevated intracellular concentrations of DIC are all consistent with the presence of a CCM in T. crunogena.