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Coassimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus.

ABSTRACT: Chloroflexus aurantiacus is a facultative autotrophic green nonsulfur bacterium that grows phototrophically in thermal springs and forms microbial mats with cyanobacteria. Cyanobacteria produce glycolate during the day (photorespiration) and excrete fermentation products at night. C. aurantiacus uses the 3-hydroxypropionate bi-cycle for autotrophic carbon fixation. This pathway was thought to be also suited for the coassimilation of various organic substrates such as glycolate, acetate, propionate, 3-hydroxypropionate, lactate, butyrate, or succinate. To test this possibility, we added these compounds at a 5 mM concentration to autotrophically pregrown cells. Although the provided amounts of H(2) and CO(2) allowed continuing photoautotrophic growth, cells immediately consumed most substrates at rates equaling the rate of autotrophic carbon fixation. Using [(14)C]acetate, half of the labeled organic carbon was incorporated into cell mass. Our data suggest that C. aurantiacus uses the 3-hydroxypropionate bi-cycle, together with the glyoxylate cycle, to channel organic substrates into the central carbon metabolism. Enzyme activities of the 3-hydroxypropionate bi-cycle were marginally affected when cells were grown heterotrophically with such organic substrates. The 3-hydroxypropionate bi-cycle in Chloroflexi is unique and was likely fostered in an environment in which traces of organic compounds can be coassimilated. Other bacteria living under oligotrophic conditions acquired genes of a rudimentary 3-hydroxypropionate bi-cycle, possibly for the same purpose. Examples are Chloroherpeton thalassium, Erythrobacter sp. strain NAP-1, Nitrococcus mobilis, and marine gammaproteobacteria of the OM60/NOR5 clade such as Congregibacter litoralis.

SUBMITTER: Zarzycki J

PROVIDER: S-EPMC3165406 | biostudies-literature | 2011 Sep

REPOSITORIES: biostudies-literature

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Coassimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus.

Zarzycki Jan J Fuchs Georg G

Applied and environmental microbiology 20110715 17

Chloroflexus aurantiacus is a facultative autotrophic green nonsulfur bacterium that grows phototrophically in thermal springs and forms microbial mats with cyanobacteria. Cyanobacteria produce glycolate during the day (photorespiration) and excrete fermentation products at night. C. aurantiacus uses the 3-hydroxypropionate bi-cycle for autotrophic carbon fixation. This pathway was thought to be also suited for the coassimilation of various organic substrates such as glycolate, acetate, propiona ...[more]

PMID: 21764971

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Project description:BACKGROUND: Chloroflexus aurantiacus is a thermophilic filamentous anoxygenic phototrophic (FAP) bacterium, and can grow phototrophically under anaerobic conditions or chemotrophically under aerobic and dark conditions. According to 16S rRNA analysis, Chloroflexi species are the earliest branching bacteria capable of photosynthesis, and Cfl. aurantiacus has been long regarded as a key organism to resolve the obscurity of the origin and early evolution of photosynthesis. Cfl. aurantiacus contains a chimeric photosystem that comprises some characters of green sulfur bacteria and purple photosynthetic bacteria, and also has some unique electron transport proteins compared to other photosynthetic bacteria. METHODS: The complete genomic sequence of Cfl. aurantiacus has been determined, analyzed and compared to the genomes of other photosynthetic bacteria. RESULTS: Abundant genomic evidence suggests that there have been numerous gene adaptations/replacements in Cfl. aurantiacus to facilitate life under both anaerobic and aerobic conditions, including duplicate genes and gene clusters for the alternative complex III (ACIII), auracyanin and NADH:quinone oxidoreductase; and several aerobic/anaerobic enzyme pairs in central carbon metabolism and tetrapyrroles and nucleic acids biosynthesis. Overall, genomic information is consistent with a high tolerance for oxygen that has been reported in the growth of Cfl. aurantiacus. Genes for the chimeric photosystem, photosynthetic electron transport chain, the 3-hydroxypropionate autotrophic carbon fixation cycle, CO2-anaplerotic pathways, glyoxylate cycle, and sulfur reduction pathway are present. The central carbon metabolism and sulfur assimilation pathways in Cfl. aurantiacus are discussed. Some features of the Cfl. aurantiacus genome are compared with those of the Roseiflexus castenholzii genome. Roseiflexus castenholzii is a recently characterized FAP bacterium and phylogenetically closely related to Cfl. aurantiacus. According to previous reports and the genomic information, perspectives of Cfl. aurantiacus in the evolution of photosynthesis are also discussed. CONCLUSIONS: The genomic analyses presented in this report, along with previous physiological, ecological and biochemical studies, indicate that the anoxygenic phototroph Cfl. aurantiacus has many interesting and certain unique features in its metabolic pathways. The complete genome may also shed light on possible evolutionary connections of photosynthesis.

Dataset Information

Coassimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus.

Publications

Coassimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus.

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