Sulfur globule oxidation in green sulfur bacteria is dependent on the dissimilatory sulfite reductase system

Green sulfur bacteria (GSB) oxidize sulfide and thiosulfate to sulfate, with extracellular globules of elemental sulfur as an intermediate. Here we investigated which genes are involved in the formation and consumption of these sulfur globules in the green sulfur bacterium Chlorobaculum tepidum. We show that sulfur globule oxidation is strictly dependent on the dissimilatory sulfite reductase (DSR) system. Deletion of dsrM/CT2244 or dsrT/CT2245, or the two dsrCABL clusters (CT0851–CT0854, CT2247–2250), abolished sulfur globule oxidation and prevented formation of sulfate from sulfide, whereas deletion of dsrU/CT2246 had no effect. The DSR system also seems to be involved in the formation of thiosulfate, because thiosulfate was released from wild-type cells during sulfide oxidation, but not from the dsr mutants. The dsr mutants incapable of complete substrate oxidation oxidized sulfide and thiosulfate about twice as fast as the wild-type, while having only slightly lower growth rates (70–80 % of wild-type). The increased oxidation rates seem to compensate for the incomplete substrate oxidation to satisfy the requirement for reducing equivalents during growth. A mutant in which two sulfide : quinone oxidoreductases (sqrD/CT0117 and sqrF/CT1087) were deleted exhibited a decreased sulfide oxidation rate (∼50 % of wild-type), yet formation and consumption of sulfur globules were not affected. The observation that mutants lacking the DSR system maintain efficient growth suggests that the DSR system is dispensable in environments with sufficiently high sulfide concentrations. Thus, the DSR system in GSB may have been acquired by horizontal gene transfer as a response to a need for enhanced substrate utilization in sulfide-limiting habitats.

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Dominance of green sulfur bacteria in the chemocline of the meromictic Lake Suigetsu, Japan, as revealed by dissimilatory sulfite reductase gene analysis

Archives of Microbiology ◽

10.1007/s00203-013-0879-5 ◽

2013 ◽

Vol 195 (5) ◽

pp. 303-312 ◽

Cited By ~ 14

Author(s):

Yumi Mori ◽

Takafumi Kataoka ◽

Takahiko Okamura ◽

Ryuji Kondo

Keyword(s):

Green Sulfur Bacteria ◽

Meromictic Lake ◽

Gene Analysis ◽

Sulfite Reductase ◽

Dissimilatory Sulfite Reductase ◽

Sulfur Bacteria ◽

Reductase Gene ◽

Green Sulfur ◽

Dissimilatory Sulfite Reductase Gene

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Physiology and Phylogeny of Green Sulfur Bacteria Forming a Monospecific Phototrophic Assemblage at a Depth of 100 Meters in the Black Sea

Applied and Environmental Microbiology ◽

10.1128/aem.71.12.8049-8060.2005 ◽

2005 ◽

Vol 71 (12) ◽

pp. 8049-8060 ◽

Cited By ~ 168

Author(s):

Ann K. Manske ◽

Jens Glaeser ◽

Marcel M. M. Kuypers ◽

Jörg Overmann

Keyword(s):

Black Sea ◽

Sulfide Oxidation ◽

Green Sulfur Bacteria ◽

The Black Sea ◽

Rrna Gene ◽

Green Sulfur Bacterium ◽

Sulfur Bacteria ◽

Light Intensities ◽

Green Sulfur

ABSTRACT The biomass, phylogenetic composition, and photoautotrophic metabolism of green sulfur bacteria in the Black Sea was assessed in situ and in laboratory enrichments. In the center of the western basin, bacteriochlorophyll e (BChl e) was detected between depths of 90 and 120 m and reached maxima of 54 and 68 ng liter−1. High-pressure liquid chromatography analysis revealed a dominance of farnesyl esters and the presence of four unusual geranyl ester homologs of BChl e. Only traces of BChl e (8 ng liter−1) were found at the northwestern slope of the Black Sea basin, where the chemocline was positioned at a significantly greater depth of 140 m. Stable carbon isotope fractionation values of farnesol indicated an autotrophic growth mode of the green sulfur bacteria. For the first time, light intensities in the Black Sea chemocline were determined employing an integrating quantum meter, which yielded maximum values between 0.0022 and 0.00075 μmol quanta m−2 s−1 at the top of the green sulfur bacterial layer around solar noon in December. These values represent by far the lowest values reported for any habitat of photosynthetic organisms. Only one 16S rRNA gene sequence type was detected in the chemocline using PCR primers specific for green sulfur bacteria. This previously unknown phylotype groups with the marine cluster of the Chlorobiaceae and was successfully enriched in a mineral medium containing sulfide, dithionite, and freshly prepared yeast extract. Under precisely controlled laboratory conditions, the enriched green sulfur bacterium proved to be capable of exploiting light intensities as low as 0.015 μmol quanta m−2 s−1 for photosynthetic 14CO2 fixation. Calculated in situ doubling times of the green sulfur bacterium range between 3.1 and 26 years depending on the season, and anoxygenic photosynthesis contributes only 0.002 to 0.01% to total sulfide oxidation in the chemocline. The stable population of green sulfur bacteria in the Black Sea chemocline thus represents the most extremely low-light-adapted and slowest-growing type of phototroph known to date.

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Thiosulfate-Dependent Chemolithoautotrophic Growth of Bradyrhizobium japonicum

Applied and Environmental Microbiology ◽

10.1128/aem.02783-09 ◽

2010 ◽

Vol 76 (8) ◽

pp. 2402-2409 ◽

Cited By ~ 31

Author(s):

Sachiko Masuda ◽

Shima Eda ◽

Seishi Ikeda ◽

Hisayuki Mitsui ◽

Kiwamu Minamisawa

Keyword(s):

Bradyrhizobium Japonicum ◽

Green Sulfur Bacteria ◽

Growth Conditions ◽

Deletion Mutation ◽

Resting Cells ◽

Wild Type ◽

Sulfur Bacteria ◽

Chemolithotrophic Growth ◽

Green Sulfur ◽

Sulfur Oxidizing

ABSTRACT Thiosulfate-oxidizing sox gene homologues were found at four loci (I, II, III, and IV) on the genome of Bradyrhizobium japonicum USDA110, a symbiotic nitrogen-fixing bacterium in soil. In fact, B. japonicum USDA110 can oxidize thiosulfate and grow under a chemolithotrophic condition. The deletion mutation of the soxY 1 gene at the sox locus I, homologous to the sulfur-oxidizing (Sox) system in Alphaproteobacteria, left B. japonicum unable to oxidize thiosulfate and grow under chemolithotrophic conditions, whereas the deletion mutation of the soxY 2 gene at sox locus II, homologous to the Sox system in green sulfur bacteria, produced phenotypes similar to those of wild-type USDA110. Thiosulfate-dependent O2 respiration was observed only in USDA110 and the soxY 2 mutant and not in the soxY 1 mutant. In the cells, 1 mol of thiosulfate was stoichiometrically converted to approximately 2 mol of sulfate and consumed approximately 2 mol of O2. B. japonicum USDA110 showed 14CO2 fixation under chemolithotrophic growth conditions. The CO2 fixation of resting cells was significantly dependent on thiosulfate addition. These results show that USDA110 is able to grow chemolithoautotrophically using thiosulfate as an electron donor, oxygen as an electron acceptor, and carbon dioxide as a carbon source, which likely depends on sox locus I including the soxY 1 gene on USDA110 genome. Thiosulfate oxidation capability is frequently found in members of the Bradyrhizobiaceae, which phylogenetic analysis showed to be associated with the presence of sox locus I homologues, including the soxY 1 gene of B. japonicum USDA110.

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Origin and Evolution of Photosystems: Lessons from Green Sulfur Bacteria

ChemPhotoChem ◽

10.1002/cptc.202100019 ◽

2021 ◽

Author(s):

Guillaume Tcherkez ◽

Nicolas Papon

Keyword(s):

Green Sulfur Bacteria ◽

Origin And Evolution ◽

Sulfur Bacteria ◽

Green Sulfur

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Novel green sulfur bacteria phylotypes detected in saline environments: ecophysiological characters versus phylogenetic taxonomy

Antonie van Leeuwenhoek ◽

10.1007/s10482-010-9420-x ◽

2010 ◽

Vol 97 (4) ◽

pp. 419-431

Author(s):

Xavier Triadó-Margarit ◽

Xavier Vila ◽

Charles A. Abella

Keyword(s):

Green Sulfur Bacteria ◽

Saline Environments ◽

Phylogenetic Taxonomy ◽

Sulfur Bacteria ◽

Green Sulfur

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Signature pigments of green sulfur bacteria in lower Pleistocene deposits from the Banyoles lacustrine area (Spain)

Journal of Paleolimnology ◽

10.1007/s10933-005-3731-3 ◽

2005 ◽

Vol 34 (2) ◽

pp. 271-280 ◽

Cited By ~ 16

Author(s):

N. Mallorquí ◽

J.B. Arellano ◽

C.M. Borrego ◽

L.J. Garcia-Gil

Keyword(s):

Green Sulfur Bacteria ◽

Sulfur Bacteria ◽

Lower Pleistocene ◽

Green Sulfur

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Differential RNA Sequencing Implicates Sulfide as the Master Regulator of S 0 Metabolism in Chlorobaculum tepidum and Other Green Sulfur Bacteria

Applied and Environmental Microbiology ◽

10.1128/aem.01966-17 ◽

2017 ◽

Vol 84 (3) ◽

Cited By ~ 1

Author(s):

Jacob M. Hilzinger ◽

Vidhyavathi Raman ◽

Kevin E. Shuman ◽

Brian J. Eddie ◽

Thomas E. Hanson

Keyword(s):

Gene Expression ◽

Elemental Sulfur ◽

Green Sulfur Bacteria ◽

Electron Donors ◽

Reduced Sulfur Compounds ◽

Promoter Elements ◽

Content Type ◽

Sulfur Bacteria ◽

Chlorobaculum Tepidum ◽

Green Sulfur

ABSTRACT The green sulfur bacteria ( Chlorobiaceae ) are anaerobes that use electrons from reduced sulfur compounds (sulfide, S 0 , and thiosulfate) as electron donors for photoautotrophic growth. Chlorobaculum tepidum , the model system for the Chlorobiaceae , both produces and consumes extracellular S 0 globules depending on the availability of sulfide in the environment. These physiological changes imply significant changes in gene regulation, which has been observed when sulfide is added to Cba. tepidum growing on thiosulfate. However, the underlying mechanisms driving these gene expression changes, i.e., the specific regulators and promoter elements involved, have not yet been defined. Here, differential RNA sequencing (dRNA-seq) was used to globally identify transcript start sites (TSS) that were present during growth on sulfide, biogenic S 0 , and thiosulfate as sole electron donors. TSS positions were used in combination with RNA-seq data from cultures growing on these same electron donors to identify both basal promoter elements and motifs associated with electron donor-dependent transcriptional regulation. These motifs were conserved across homologous Chlorobiaceae promoters. Two lines of evidence suggest that sulfide-mediated repression is the dominant regulatory mode in Cba. tepidum . First, motifs associated with genes regulated by sulfide overlap key basal promoter elements. Second, deletion of the Cba. tepidum 1277 ( CT1277 ) gene, encoding a putative regulatory protein, leads to constitutive overexpression of the sulfide:quinone oxidoreductase CT1087 in the absence of sulfide. The results suggest that sulfide is the master regulator of sulfur metabolism in Cba. tepidum and the Chlorobiaceae . Finally, the identification of basal promoter elements with differing strengths will further the development of synthetic biology in Cba. tepidum and perhaps other Chlorobiaceae . IMPORTANCE Elemental sulfur is a key intermediate in biogeochemical sulfur cycling. The photoautotrophic green sulfur bacterium Chlorobaculum tepidum either produces or consumes elemental sulfur depending on the availability of sulfide in the environment. Our results reveal transcriptional dynamics of Chlorobaculum tepidum on elemental sulfur and increase our understanding of the mechanisms of transcriptional regulation governing growth on different reduced sulfur compounds. This report identifies genes and sequence motifs that likely play significant roles in the production and consumption of elemental sulfur. Beyond this focused impact, this report paves the way for the development of synthetic biology in Chlorobaculum tepidum and other Chlorobiaceae by providing a comprehensive identification of promoter elements for control of gene expression, a key element of strain engineering.

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