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Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms.

Justice NB, Norman A, Brown CT, Singh A, Thomas BC, Banfield JF - BMC Genomics (2014)

Bottom Line: Pathways of sulfur oxidation vary considerably across the genus, including the number and type of subunits of putative heterodisulfide reductase complexes likely involved in sulfur oxidation.Only the AMDSBA3 genome encodes a dissimilatory nitrate reducatase and only the AMDSBA5 and S. thermosulfidooxidans genomes encode assimilatory nitrate reductases.Overall, the results significantly expand our understanding of carbon, sulfur, nitrogen, and hydrogen metabolism within the Sulfobacillus genus.

View Article: PubMed Central - PubMed

Affiliation: Department of Earth and Planetary Science, University of California, Berkeley, CA 94720, USA. njustice@berkeley.edu.

ABSTRACT

Background: Bacteria of the genus Sulfobacillus are found worldwide as members of microbial communities that accelerate sulfide mineral dissolution in acid mine drainage environments (AMD), acid-rock drainage environments (ARD), as well as in industrial bioleaching operations. Despite their frequent identification in these environments, their role in biogeochemical cycling is poorly understood.

Results: Here we report draft genomes of five species of the Sulfobacillus genus (AMDSBA1-5) reconstructed by cultivation-independent sequencing of biofilms sampled from the Richmond Mine (Iron Mountain, CA). Three of these species (AMDSBA2, AMDSBA3, and AMDSBA4) have no cultured representatives while AMDSBA1 is a strain of S. benefaciens, and AMDSBA5 a strain of S. thermosulfidooxidans. We analyzed the diversity of energy conservation and central carbon metabolisms for these genomes and previously published Sulfobacillus genomes. Pathways of sulfur oxidation vary considerably across the genus, including the number and type of subunits of putative heterodisulfide reductase complexes likely involved in sulfur oxidation. The number and type of nickel-iron hydrogenase proteins varied across the genus, as does the presence of different central carbon pathways. Only the AMDSBA3 genome encodes a dissimilatory nitrate reducatase and only the AMDSBA5 and S. thermosulfidooxidans genomes encode assimilatory nitrate reductases. Within the genus, AMDSBA4 is unusual in that its electron transport chain includes a cytochrome bc type complex, a unique cytochrome c oxidase, and two distinct succinate dehydrogenase complexes.

Conclusions: Overall, the results significantly expand our understanding of carbon, sulfur, nitrogen, and hydrogen metabolism within the Sulfobacillus genus.

No MeSH data available.


Related in: MedlinePlus

Operon structure of putative heterodisulfide reductase complexes. Hdr cluster I is found in S. thermosulfidooxidans, AMDSBA1, AMDSBA2, and AMDSBA5. Hdr cluster IIa is found in S. thermosulfidooxidans AMDSBA1, AMDSBA2, AMDSBA4, and AMDSBA5. Hdr cluster IIb is found in S. acidophilus and AMDSBA3. Gene abbreviations are as follows: thdx, thioredoxin; gcsh, glycine cleavage system protein H; hdrABC, heterodisulfide reductases; hypo, hypothetical; dsrE, dsrE-like sulfur relay protein; tusA, sulfur transfer protein; lpl, lipoate protein ligase; etfAB, electron transfer flavoprotein. Gene colors correspond to protein orthology as defined in methods.
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Fig4: Operon structure of putative heterodisulfide reductase complexes. Hdr cluster I is found in S. thermosulfidooxidans, AMDSBA1, AMDSBA2, and AMDSBA5. Hdr cluster IIa is found in S. thermosulfidooxidans AMDSBA1, AMDSBA2, AMDSBA4, and AMDSBA5. Hdr cluster IIb is found in S. acidophilus and AMDSBA3. Gene abbreviations are as follows: thdx, thioredoxin; gcsh, glycine cleavage system protein H; hdrABC, heterodisulfide reductases; hypo, hypothetical; dsrE, dsrE-like sulfur relay protein; tusA, sulfur transfer protein; lpl, lipoate protein ligase; etfAB, electron transfer flavoprotein. Gene colors correspond to protein orthology as defined in methods.

Mentions: Two different types of Sulfobacillus hdr gene clusters were found with varying gene content (Figure 4). One group, hdr gene cluster I, was identified only in S. thermosulfidooxidans, AMDSBA1 and AMDSBA5. This cluster includes an HdrA-like protein with an FAD-binding site and a conserved-cysteine motif (CxGCRDx6-8CSx2CC) typical in binding an Fe-S cluster. Two HdrB proteins are present which contain the cysteine-rich CCG domains (CxnCCGxmC) predicted to bind [4Fe-4S] clusters [70]. The HdrC protein contains another [4Fe-4S] binding center. Furthermore, two DsrE-family proteins and a TusA homolog are encoded in this locus. DsrE and TusA proteins are strongly implicated in persulfidic sulfur (RS-SH) transfer in Allochromatium. vinosum[71, 72]. It is also interesting to note that a homolog to the glycine cleavage protein H (a lipoic acid containing protein) is found in this locus as is a lipoate-protein ligase that catalyzes the attachment of lipoic acid to target proteins [73]. The lipoic acid moiety of glycine cleavage protein H acts as a “swinging arm” that serves to transfer reaction intermediates between the various catalytic sites of the other proteins in the glycine cleavage system complex [74]. It is tempting to speculate that lipoic acid, with its disulfide bond, may play a key role in sulfur species transfers amongst this heterodisulfide complex, as has been noted by others [75].Figure 4


Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms.

Justice NB, Norman A, Brown CT, Singh A, Thomas BC, Banfield JF - BMC Genomics (2014)

Operon structure of putative heterodisulfide reductase complexes. Hdr cluster I is found in S. thermosulfidooxidans, AMDSBA1, AMDSBA2, and AMDSBA5. Hdr cluster IIa is found in S. thermosulfidooxidans AMDSBA1, AMDSBA2, AMDSBA4, and AMDSBA5. Hdr cluster IIb is found in S. acidophilus and AMDSBA3. Gene abbreviations are as follows: thdx, thioredoxin; gcsh, glycine cleavage system protein H; hdrABC, heterodisulfide reductases; hypo, hypothetical; dsrE, dsrE-like sulfur relay protein; tusA, sulfur transfer protein; lpl, lipoate protein ligase; etfAB, electron transfer flavoprotein. Gene colors correspond to protein orthology as defined in methods.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4378227&req=5

Fig4: Operon structure of putative heterodisulfide reductase complexes. Hdr cluster I is found in S. thermosulfidooxidans, AMDSBA1, AMDSBA2, and AMDSBA5. Hdr cluster IIa is found in S. thermosulfidooxidans AMDSBA1, AMDSBA2, AMDSBA4, and AMDSBA5. Hdr cluster IIb is found in S. acidophilus and AMDSBA3. Gene abbreviations are as follows: thdx, thioredoxin; gcsh, glycine cleavage system protein H; hdrABC, heterodisulfide reductases; hypo, hypothetical; dsrE, dsrE-like sulfur relay protein; tusA, sulfur transfer protein; lpl, lipoate protein ligase; etfAB, electron transfer flavoprotein. Gene colors correspond to protein orthology as defined in methods.
Mentions: Two different types of Sulfobacillus hdr gene clusters were found with varying gene content (Figure 4). One group, hdr gene cluster I, was identified only in S. thermosulfidooxidans, AMDSBA1 and AMDSBA5. This cluster includes an HdrA-like protein with an FAD-binding site and a conserved-cysteine motif (CxGCRDx6-8CSx2CC) typical in binding an Fe-S cluster. Two HdrB proteins are present which contain the cysteine-rich CCG domains (CxnCCGxmC) predicted to bind [4Fe-4S] clusters [70]. The HdrC protein contains another [4Fe-4S] binding center. Furthermore, two DsrE-family proteins and a TusA homolog are encoded in this locus. DsrE and TusA proteins are strongly implicated in persulfidic sulfur (RS-SH) transfer in Allochromatium. vinosum[71, 72]. It is also interesting to note that a homolog to the glycine cleavage protein H (a lipoic acid containing protein) is found in this locus as is a lipoate-protein ligase that catalyzes the attachment of lipoic acid to target proteins [73]. The lipoic acid moiety of glycine cleavage protein H acts as a “swinging arm” that serves to transfer reaction intermediates between the various catalytic sites of the other proteins in the glycine cleavage system complex [74]. It is tempting to speculate that lipoic acid, with its disulfide bond, may play a key role in sulfur species transfers amongst this heterodisulfide complex, as has been noted by others [75].Figure 4

Bottom Line: Pathways of sulfur oxidation vary considerably across the genus, including the number and type of subunits of putative heterodisulfide reductase complexes likely involved in sulfur oxidation.Only the AMDSBA3 genome encodes a dissimilatory nitrate reducatase and only the AMDSBA5 and S. thermosulfidooxidans genomes encode assimilatory nitrate reductases.Overall, the results significantly expand our understanding of carbon, sulfur, nitrogen, and hydrogen metabolism within the Sulfobacillus genus.

View Article: PubMed Central - PubMed

Affiliation: Department of Earth and Planetary Science, University of California, Berkeley, CA 94720, USA. njustice@berkeley.edu.

ABSTRACT

Background: Bacteria of the genus Sulfobacillus are found worldwide as members of microbial communities that accelerate sulfide mineral dissolution in acid mine drainage environments (AMD), acid-rock drainage environments (ARD), as well as in industrial bioleaching operations. Despite their frequent identification in these environments, their role in biogeochemical cycling is poorly understood.

Results: Here we report draft genomes of five species of the Sulfobacillus genus (AMDSBA1-5) reconstructed by cultivation-independent sequencing of biofilms sampled from the Richmond Mine (Iron Mountain, CA). Three of these species (AMDSBA2, AMDSBA3, and AMDSBA4) have no cultured representatives while AMDSBA1 is a strain of S. benefaciens, and AMDSBA5 a strain of S. thermosulfidooxidans. We analyzed the diversity of energy conservation and central carbon metabolisms for these genomes and previously published Sulfobacillus genomes. Pathways of sulfur oxidation vary considerably across the genus, including the number and type of subunits of putative heterodisulfide reductase complexes likely involved in sulfur oxidation. The number and type of nickel-iron hydrogenase proteins varied across the genus, as does the presence of different central carbon pathways. Only the AMDSBA3 genome encodes a dissimilatory nitrate reducatase and only the AMDSBA5 and S. thermosulfidooxidans genomes encode assimilatory nitrate reductases. Within the genus, AMDSBA4 is unusual in that its electron transport chain includes a cytochrome bc type complex, a unique cytochrome c oxidase, and two distinct succinate dehydrogenase complexes.

Conclusions: Overall, the results significantly expand our understanding of carbon, sulfur, nitrogen, and hydrogen metabolism within the Sulfobacillus genus.

No MeSH data available.


Related in: MedlinePlus