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Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1.

ABSTRACT: Strain MC-1 is a marine, microaerophilic, magnetite-producing, magnetotactic coccus phylogenetically affiliated with the alpha-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 (Deltadelta13C) was -11.4 per thousand. 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 alpha-Proteobacteria to use the rTCA cycle for autotrophy.

SUBMITTER: Williams TJ

PROVIDER: S-EPMC1392968 | biostudies-literature | 2006 Feb

REPOSITORIES: biostudies-literature

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Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1.

Williams Timothy J TJ Zhang Chuanlun L CL Scott James H JH Bazylinski Dennis A DA

Applied and environmental microbiology 20060201 2

Strain MC-1 is a marine, microaerophilic, magnetite-producing, magnetotactic coccus phylogenetically affiliated with the alpha-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 ...[more]

PMID: 16461683

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Project description:Magnetotactic bacteria (MTB) are morphologically and phylogenetically diverse prokaryotes. They can form intracellular chain-assembled magnetite (Fe3O4) or greigite (Fe3S4) nanocrystals each enveloped by a lipid bilayer membrane called a magnetosome. Magnetotactic cocci have been found to be the most abundant morphotypes of MTB in various aquatic environments. However, knowledge on magnetosome biomineralization within magnetotactic cocci remains elusive due to small number of strains that have been cultured. By using a coordinated fluorescence and scanning electron microscopy method, we discovered a unique magnetotactic coccus strain (tentatively named SHHC-1) in brackish sediments collected from the estuary of Shihe River in Qinhuangdao city, eastern China. It phylogenetically belongs to the Alphaproteobacteria class. Transmission electron microscopy analyses reveal that SHHC-1 cells formed many magnetite-type magnetosomes organized as two bundles in each cell. Each bundle contains two parallel chains with smaller magnetosomes generally located at the ends of each chain. Unlike most magnetotactic alphaproteobacteria that generally form magnetosomes with uniform crystal morphologies, SHHC-1 magnetosomes display a more diverse variety of crystal morphology even within a single cell. Most particles have rectangular and rhomboidal projections, whilst others are triangular, or irregular. High resolution transmission electron microscopy observations coupled with morphological modeling indicate an idealized model-elongated octahedral crystals, a form composed of eight {111} faces. Furthermore, twins, multiple twins and stack dislocations are frequently observed in the SHHC-1 magnetosomes. This suggests that biomineralization of strain SHHC-1 magnetosome might be less biologically controlled than other magnetotactic alphaproteobacteria. Alternatively, SHHC-1 is more sensitive to the unfavorable environments under which it lives, or a combination of both factors may have controlled the magnetosome biomineralization process within this unique MTB.

Project description:Very few bacteria are able to fix carbon via both the reverse tricarboxylic acid (rTCA) and the Calvin-Benson-Bassham (CBB) cycles, such as symbiotic, sulfur-oxidizing bacteria that are the sole carbon source for the marine tubeworm Riftia pachyptila, the fastest-growing invertebrate. To date, the coexistence of these two carbon fixation pathways had not been found in a cultured bacterium and could thus not be studied in detail. Moreover, it was not clear if these two pathways were encoded in the same symbiont individual, or if two symbiont populations, each with one of the pathways, coexisted within tubeworms. With comparative genomics, we show that Thioflavicoccus mobilis, a cultured, free-living gammaproteobacterial sulfur oxidizer, possesses the genes for both carbon fixation pathways. Here, we also show that both the CBB and rTCA pathways are likely encoded in the genome of the sulfur-oxidizing symbiont of the tubeworm Escarpia laminata from deep-sea asphalt volcanoes in the Gulf of Mexico. Finally, we provide genomic and transcriptomic data suggesting a potential electron flow toward the rTCA cycle carboxylase 2-oxoglutarate:ferredoxin oxidoreductase, via a rare variant of NADH dehydrogenase/heterodisulfide reductase in the E. laminata symbiont. This electron-bifurcating complex, together with NAD(P)+ transhydrogenase and Na+ translocating Rnf membrane complexes, may improve the efficiency of the rTCA cycle in both the symbiotic and the free-living sulfur oxidizer.IMPORTANCE Primary production on Earth is dependent on autotrophic carbon fixation, which leads to the incorporation of carbon dioxide into biomass. Multiple metabolic pathways have been described for autotrophic carbon fixation, but most autotrophic organisms were assumed to have the genes for only one of these pathways. Our finding of a cultivable bacterium with two carbon fixation pathways in its genome, the rTCA and the CBB cycle, opens the possibility to study the potential benefits of having these two pathways and the interplay between them. Additionally, this will allow the investigation of the unusual and potentially very efficient mechanism of electron flow that could drive the rTCA cycle in these autotrophs. Such studies will deepen our understanding of carbon fixation pathways and could provide new avenues for optimizing carbon fixation in biotechnological applications.

Dataset Information

Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1.

Publications

Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1.

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