Genomic and Evolutionary Perspectives on Sulfur Metabolism in Green Sulfur Bacteria

Niels-Ulrik Frigaard, Donald A. Bryant

Abstract Green sulfur bacteria (GSB) are anaerobic photoautotrophs that oxidize sulfide, elemental sulfur, thiosulfate, ferrous iron, and hydrogen for growth. We present here an analysis of the distribution and evolution of enzymes involved in oxidation of sulfur compounds in GSB based on genome sequence data from 12 strains. Sulfide:quinone reductase (SQR) is found in all strains. Chlorobium ferrooxidans, which cannot grow on sulfide but grows on Fe2+, has apparently lost all genes involved in oxidation of sulfur compounds other than sqr. Instead, this organism possesses genes involved in assimilatory sulfate reduction, a trait that is unusual in GSB. The dissimilatory sulfite reductase (Dsr) enzyme system, which appears to be involved in elemental sulfur utilization, is found in all sulfide-utilizing strains except Chloroherpeton thalassium. The absence of Dsr enzymes in this early diverging GSB, in combination with phylogenetic analyses, suggests that the Dsr system in GSB could be a recent acquisition, which was obtained by lateral gene transfer in part from sulfide-oxidizing bacteria and in part from sulfate-reducing bacteria. All thiosulfate-uti-lizing GSB strains have an identical sox gene cluster. The soxCD genes, which are found in certain other thiosulfate-utilizing organisms like Paracoccus pan-totrophus, are absent from GSB. Flavocytochrome c, adenosine 5'-phosphosul-fate reductase, ATP-sulfurylase, the Qmo complex, and other enzymes related to the utilization of sulfur compounds are found in some, but not all sulfide-utiliz-ing strains. Even though different GSB strains superficially exhibit a similar sulfur oxidation phenotype, this may be caused by different combinations of enzymes. Thus, genome analyses have revealed that GSB have greater diversity in sulfur metabolism than previously suspected.

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