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Evidence for Autotrophy via the Reverse Tricarboxylic Acid Cycle in the Marine Magnetotactic Coccus Strain MC-1

Department of Biochemistry, Biophysics, and Molecular Biology, Iowa State University, Ames, Iowa 50011,¹ Savannah River Ecology Laboratory, University of Georgia, Drawer E, Aiken, South Carolina 29802,² Department of Marine Sciences, University of Georgia, Athens, Georgia 30602,³ Carnegie Institution of Washington, Geophysical Laboratory, 5251 Broad Branch Rd. NW, Washington, D.C. 20015-1305⁴

Received 25 September 2005/ Accepted 30 November 2005

Strain MC-1 is a marine, microaerophilic, magnetite-producing, magnetotactic coccus phylogenetically affiliated with the -Proteobacteria. Strain MC-1 grew chemolithotrophically with sulfide and thiosulfate as electron donors with HCO₃^–/CO₂ as the sole carbon source. Experiments with cells grown microaerobically in liquid with thiosulfate and H¹⁴CO₃^–/¹⁴CO₂ showed that all cell carbon was derived from H¹⁴CO₃^–/¹⁴CO₂ and therefore that MC-1 is capable of chemolithoautotrophy. Cell extracts did not exhibit ribulose-1,5-bisphosphate carboxylase-oxygenase (RubisCO) activity, nor were RubisCO genes found in the draft genome of MC-1. Thus, unlike other chemolithoautotrophic, magnetotactic bacteria, strain MC-1 does not appear to utilize the Calvin-Benson-Bassham cycle for autotrophy. Cell extracts did not exhibit carbon monoxide dehydrogenase activity, indicating that the acetyl-coenzyme A pathway also does not function in strain MC-1. The ¹³C content of whole cells of MC-1 relative to the ¹³C content of the inorganic carbon source (¹³C) was –11.4 . Cellular fatty acids showed enrichment of ¹³C relative to whole cells. Strain MC-1 cell extracts showed activities for several key enzymes of the reverse (reductive) tricarboxylic acid (rTCA) cycle including fumarate reductase, pyruvate:acceptor oxidoreductase and 2-oxoglutarate:acceptor oxidoreductase. Although ATP citrate lyase (another key enzyme of the rTCA cycle) activity was not detected in strain MC-1 using commonly used assays, cell extracts did cleave citrate, and the reaction was dependent upon the presence of ATP and coenzyme A. Thus, we infer the presence of an ATP-dependent citrate-cleaving mechanism. These results are consistent with the operation of the rTCA cycle in MC-1. Strain MC-1 appears to be the first known representative of the -Proteobacteria to use the rTCA cycle for autotrophy.

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