Identification of components of electron transport chains in the extremely thermoacidophilic crenarchaeon Metallosphaera sedula through iron and sulfur compound oxidation transcriptomes - PubMed (original) (raw)

Identification of components of electron transport chains in the extremely thermoacidophilic crenarchaeon Metallosphaera sedula through iron and sulfur compound oxidation transcriptomes

Kathryne S Auernik et al. Appl Environ Microbiol. 2008 Dec.

Abstract

The crenarchaeal order Sulfolobales collectively contain at least five major terminal oxidase complexes. Based on genome sequence information, all five complexes are found only in Metallosphaera sedula and Sulfolobus tokodaii, the two sequenced Sulfolobales capable of iron oxidization. While specific respiratory complexes in certain Sulfolobales have been characterized previously as proton pumps for maintaining intracellular pH and generating proton motive force, their contribution to sulfur and iron biooxidation has not been considered. For M. sedula growing in the presence of ferrous iron and reduced inorganic sulfur compounds (RISCs), global transcriptional analysis was used to track the response of specific genes associated with these complexes, as well as other known and putative respiratory electron transport chain elements. Open reading frames from all five terminal oxidase or bc(1)-like complexes were stimulated on one or more conditions tested. Components of the fox (Msed0467 to Msed0489) and soxNL-cbsABA (Msed0500 to Msed0505) terminal/quinol oxidase clusters were triggered by ferrous iron, while the soxABCDD' terminal oxidase cluster (Msed0285 to Msed0291) were induced by tetrathionate and S(0). Chemolithotrophic electron transport elements, including a putative tetrathionate hydrolase (Msed0804), a novel polysulfide/sulfur/dimethyl sulfoxide reductase-like complex (Msed0812 to Msed0818), and a novel heterodisulfide reductase-like complex (Msed1542 to Msed1550), were also stimulated by RISCs. Furthermore, several hypothetical proteins were found to have strong responses to ferrous iron or RISCs, suggesting additional candidates in iron or sulfur oxidation-related pathways. From this analysis, a comprehensive model for electron transport in M. sedula could be proposed as the basis for examining specific details of iron and sulfur oxidation in this bioleaching archaeon.

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Figures

FIG. 1.

Composite model of respiratory electron transport chain components in the Sulfolobales. Inset table notes components identified in selected Sulfolobales. Sso, S. solfataricus; Sto, S. tokodaii; Sac, S. acidocaldarius; Mse, M. sedula; Aam, A. ambivalens; Sme, S. metallicus. Genome sequences are not yet available for organisms with a superscript 1. pmf, protein motive force.

FIG. 2.

Proposed model of M. sedula respiratory electron transport chain(s) and transcriptional response to tested conditions. Model proposed is based on previous work done in other Sulfolobales. Media are as described in Materials and Methods. YKS, Y medium plus potassium sulfate. Grayscale patterns represent differential transcription [minimum log2 relative change of 0.9 and −log10(P value) of ≥2.5] between specified test conditions, while heat plots depict normalized transcription levels for each test condition compared to an average LSM of 0. Heat plots were constructed using the software Array File Maker, version 4.0 (7). For Msed2031 and Msed2032, specified differential transcription was observed for YS versus YFS medium but not for YKT versus YFS medium; for Msed0817, specified differential transcription was observed for YKT versus YFS medium but not for YS versus YFS medium (sites marked by asterisks). Differential transcription log2 relative changes and significance values for each ORF under all test conditions can be found under GEO accession number GSE12044.

References

1. Alami, N., and P. C. Hallenbeck. 1995. Cloning and characterization of a gene cluster, phsBCDEF, necessary for the production of hydrogen sulfide from thiosulfate by Salmonella typhimurium. Gene 156:53-57. - PubMed
1. Auernik, K. S., Y. Maezato, P. H. Blum, and R. M. Kelly. 2008. The genome sequence of the metal-mobilizing, extremely thermoacidophilic archaeon Metallosphaera sedula provides insights into bioleaching-associated metabolism. Appl. Environ. Microbiol. 74:682-692. - PMC - PubMed
1. Bandeiras, T. M., C. A. Salgueiro, H. Huber, C. M. Gomes, and M. Teixeira. 2003. The respiratory chain of the thermophilic archaeon Sulfolobus metallicus: studies on the type-II NADH dehydrogenase. Biochim. Biophys. Acta 1557:13-19. - PubMed
1. Barrett, M. L., I. Harvey, M. Sundararajan, R. Surendran, J. F. Hall, M. J. Ellis, M. A. Hough, R. W. Strange, I. H. Hillier, and S. S. Hasnain. 2006. Atomic resolution crystal structures, EXAFS, and quantum chemical studies of rusticyanin and its two mutants provide insight into its unusual properties. Biochemistry 45:2927-2939. - PubMed
1. Bathe, S., and P. R. Norris. 2007. Ferrous iron- and sulfur-induced genes in Sulfolobus metallicus. Appl. Environ. Microbiol. 73:2491-2497. - PMC - PubMed

Identification of components of electron transport chains in the extremely thermoacidophilic crenarchaeon Metallosphaera sedula through iron and sulfur compound oxidation transcriptomes - PubMed (original) (raw)