Thiosulfate-Dependent Chemolithoautotrophic Growth of Bradyrhizobium japonicum

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

Microbiology ◽

10.1099/mic.0.044669-0 ◽

2011 ◽

Vol 157 (4) ◽

pp. 1229-1239 ◽

Cited By ~ 53

Author(s):

Carina Holkenbrink ◽

Santiago Ocón Barbas ◽

Anders Mellerup ◽

Hiroyo Otaki ◽

Niels-Ulrik Frigaard

Keyword(s):

Sulfide Oxidation ◽

Green Sulfur Bacteria ◽

Substrate Oxidation ◽

Sulfite Reductase ◽

Wild Type ◽

Oxidation Rates ◽

Dissimilatory Sulfite Reductase ◽

Sulfur Bacteria ◽

Sulfur Globules ◽

Green Sulfur

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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Inorganic sulfur oxidizing system in green sulfur bacteria

Photosynthesis Research ◽

10.1007/s11120-010-9531-2 ◽

2010 ◽

Vol 104 (2-3) ◽

pp. 163-176 ◽

Cited By ~ 34

Author(s):

Hidehiro Sakurai ◽

Takuro Ogawa ◽

Michiko Shiga ◽

Kazuhito Inoue

Keyword(s):

Green Sulfur Bacteria ◽

Inorganic Sulfur ◽

Sulfur Bacteria ◽

Green Sulfur ◽

Sulfur Oxidizing

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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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