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

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Justice, Nicholas B ^a,b   Norman, Anders ^a,c   Brown, Christopher T ^a   Singh, Andrea ^a   Thomas, Brian C ^a   Banfield, Jillian F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; HETERODISULFIDE REDUCTASE; HYDROGEN; NITRATE REDUCTASE; NITROGEN; OXIDOREDUCTASE; SULFUR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; RIBOSOME PROTEIN; RNA 16S;

ARTICLE; BACTERIA; BACTERIAL GENOME; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM ISOLATE; CARBON METABOLISM; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON TRANSPORT; ENERGY CONSERVATION; ENERGY METABOLISM; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; GRAM POSITIVE BACTERIUM; HYDROGEN METABOLISM; METABOLISM; MOLECULAR PHYLOGENY; NITROGEN METABOLISM; NONHUMAN; POPULATION ABUNDANCE; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; SPECIES DIVERSITY; SULFOBACILLUS; SULFOBACILLUS BENEFACIENS; SULFOBACILLUS HERMOSULFIDOOXIDANS; SULFUR METABOLISM; CHEMISTRY; CLASSIFICATION; COMPARATIVE STUDY; ENDOSPORE-FORMING RODS AND COCCI; GENETICS; ISOLATION AND PURIFICATION; OXIDATION REDUCTION REACTION; PHYLOGENY; SEQUENCE ANALYSIS;

SULFOBACILLUS; SULFOBACILLUS THERMOSULFIDOOXIDANS;

BACTERIAL PROTEINS; CARBON; ENERGY METABOLISM; GENOME, BACTERIAL; GRAM-POSITIVE ENDOSPORE-FORMING RODS; HYDROGEN; NITROGEN; OXIDATION-REDUCTION; PHYLOGENY; RIBOSOMAL PROTEINS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, RNA; SULFUR;

EID: 84925685412     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1107     Document Type: Article

References (142)

1. Norris PR, Clark DA, Owen JP, Waterhouse S: Characteristics of Sulfobacillus acidophilus sp. nov. and other moderately thermophilic mineral-sulphide-oxidizing bacteria. Microbiol-Sgm 1996,142(Pt 4):775-783.
2. Li B, Chen Y, Liu Q, Hu S, Chen X: Complete genome analysis of Sulfobacillus acidophilus strain TPY, isolated from a hydrothermal vent in the Pacific Ocean. J Bacteriol 2011, 193:5555-5556. 10.1128/JB.05684-11.
3. Johnson DB, Okibe N, Roberto FF: Novel thermo-acidophilic bacteria isolated from geothermal sites in Yellowstone National Park: physiological and phylogenetic characteristics. Arch Microbiol 2003, 180:60-68. 10.1007/s00203-003-0562-3.
4. Baker BJ, Banfield JF: Microbial communities in acid mine drainage. FEMS Microbiol Ecol 2003, 44:139-152. 10.1016/S0168-6496(03)00028-X.
5. Watling HR, Perrot FA, Shiers DW: Comparison of selected characteristics of Sulfobacillus species and review of their occurrence in acidic and bioleaching environments. Hydrometallurgy 2008, 93:57-65. 10.1016/j.hydromet.2008.03.001.
6. Bond PL, Druschel GK, Banfield JF: Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl Environ Microbiol 2000, 66:4962-4971. 10.1128/AEM.66.11.4962-4971.2000.
7. Justice NB, Pan C, Mueller R, Spaulding SE, Shah V, Sun CL, Yelton AP, Miller CS, Thomas BC, Shah M, VerBerkmoes N, Hettich R, Banfield JF: Heterotrophic archaea contribute to carbon cycling in low-pH, suboxic biofilm communities. Appl Environ Microbiol 2012, 78:8321-8330. 10.1128/AEM.01938-12.
8. Druschel GK, Baker BJ, Gihring TM, Banfield JF: Acid mine drainage biogeochemistry at Iron Mountain, California. Geochem Trans 2004, 5:13-32. 10.1186/1467-4866-5-13.
9. Dick GJ, Andersson AF, Baker BJ, Simmons SL, Thomas BC, Yelton AP, Banfield JF: Community-wide analysis of microbial genome sequence signatures. Genome Biol 2009, 10:R85. 10.1186/gb-2009-10-8-r85.
10. Melamud VS, Pivovarova TA, Tourova TP, Kolganova TV, Osipov GA, Lysenko AM, Kondrat'eva TF, Karavaiko GI: Sulfobacillus sibiricus sp. nov., a New Moderately Thermophilic Bacterium - Springer. Microbiology 2003, 72:605-612. 10.1023/A:1026007620113.
11. Bogdanova TI, Tsaphna IA, Kondrat'eva TF, Duda VI, Suzina NE, Melamud VS, Tourova TP, Karavaiko GI: Sulfobacillus thermotolerans sp. nov., a thermotolerant, chemolithotrophic bacterium. Int J Syst Evol Microbiol 2006, 56:1039-1042. 10.1099/ijs.0.64106-0.
12. Golovacheva RS, Karavaiko GI: Sulfobacillus, a new genus of thermophilic sporulating bacteria. Mikrobiologiia 1978, 47:815-822.
13. Johnson DB, Joulian C, d'Hugues P, Hallberg KB: Sulfobacillus benefaciens sp. nov., an acidophilic facultative anaerobic Firmicute isolated from mineral bioleaching operations. Extremophiles 2008, 12:789-798. 10.1007/s00792-008-0184-4.
14. Bridge T, Johnson DB: Reduction of soluble iron and reductive dissolution of ferric iron-containing minerals by moderately thermophilic iron-oxidizing bacteria. Appl Environ Microbiol 1998, 64:2181-2186.
15. Tsaplina IA, Zhuravleva AE, Egorova MA, Bogdanova TI, Krasil'nikova EN, Zakharchuk LM, Kondrat'eva TF: Response to oxygen limitation in bacteria of the genus sulfobacillus. Microbiology 2010, 79:13-22. 10.1134/S0026261710010029.
16. Travisany D, Di Genova A, Sepulveda A, Bobadilla-Fazzini RA, Parada P, Maass A: Draft genome sequence of the Sulfobacillus thermosulfidooxidans Cutipay strain, an indigenous bacterium isolated from a naturally extreme mining environment in Northern Chile. J Bacteriol 2012, 194:6327-6328. 10.1128/JB.01622-12.
17. Anderson I, Chertkov O, Chen A, Saunders E, Lapidus A, Nolan M, Lucas S, Hammon N, Deshpande S, Cheng J-F, Han C, Tapia R, Goodwin LA, Pitluck S, Liolios K, Pagani I, Ivanova N, Mikhailova N, Pati A, Palaniappan K, Land M, Pan C, Rohde M, Pukall R, Göker M, Detter JC, Woyke T, Bristow J, Eisen JA, Markowitz V, et al.: Complete genome sequence of the moderately thermophilic mineral-sulfide-oxidizing firmicute Sulfobacillus acidophilus type strain (NAL(T)). Stand Genomic Sci 2012, 6:1-13.
18. Guo X, Yin H, Liang Y, Hu Q, Zhou X, Xiao Y, Ma L, Zhang X, Qiu G, Liu X: Comparative genome analysis reveals metabolic versatility and environmental adaptations of Sulfobacillus thermosulfidooxidans strain ST. PLoS One 2014, 9:e99417. 10.1371/journal.pone.0099417.
19. Markowitz VM, Chen I-MA, Palaniappan K, Chu K, Szeto E, Pillay M, Ratner A, Huang J, Woyke T, Huntemann M, Anderson I, Billis K, Varghese N, Mavromatis K, Pati A, Ivanova NN, Kyrpides NC: IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res 2014,42(Database issue):D560-D567.
20. Denef VJ, Denef VJ, Kalnejais LH, Kalnejais LH, Mueller RS, Mueller RS, Wilmes P, Wilmes P, Baker BJ, Baker BJ, Thomas BC, Thomas BC, VerBerkmoes NC, VerBerkmoes NC, Hettich RL, Hettich RL, Banfield JF, Banfield JF: Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proc Natl Acad Sci 2010, 107:2383-2390. 10.1073/pnas.0907041107.
21. Miller CS, Baker BJ, Thomas BC, Singer SW, Banfield JF: EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol 2011, 12:R44. 10.1186/gb-2011-12-5-r44.
22. JGI: Protocols in Production Sequencing. [ http://jgi.doe.gov/collaborate-with-jgi/pmooverview/protocols-sample-preparation-information/ ]
23. St John J: SeqPrep. [ https://github.com/jstjohn/SeqPrep ]
24. Denef VJ, Banfield JF: In situ evolutionary rate measurements show ecological success of recently emerged bacterial hybrids. Science 2012, 336:462-466. 10.1126/science.1218389.
25. Peng Y, Leung HCM, Yiu SM, Chin FYL: IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 2012, 28:1420-1428. 10.1093/bioinformatics/bts174.
26. Li H, Durbin R: Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760. 10.1093/bioinformatics/btp324.
27. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ: Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010, 11:119. 10.1186/1471-2105-11-119.
28. Lowe TM, Eddy SR: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964. 10.1093/nar/25.5.0955.
29. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410. 10.1016/S0022-2836(05)80360-2.
30. Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH: UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 2007, 23:1282-1288. 10.1093/bioinformatics/btm098.
31. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M: KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 1999, 27:29-34. 10.1093/nar/27.1.29.
32. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R: InterProScan: protein domains identifier. Nucleic Acids Res 2005, 33:W116-W120. 10.1093/nar/gki442.
33. Markowitz VM, Chen IMA, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang J, Williams P, Huntemann M, Anderson I, Mavromatis K, Ivanova NN, Kyrpides NC: IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res 2011, 40:D115-D122.
34. Edgar RC: Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26:2460-2461. 10.1093/bioinformatics/btq461.
35. Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797. 10.1093/nar/gkh340.
36. Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17:540-552. 10.1093/oxfordjournals.molbev.a026334.
37. Talavera G, Castresana J: Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007, 56:564-577. 10.1080/10635150701472164.
38. Abascal F, Zardoya R, Posada D: ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105. 10.1093/bioinformatics/bti263.
39. Stamatakis A: RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690. 10.1093/bioinformatics/btl446.
40. Letunic I, Bork P: Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2007, 23:127-128. 10.1093/bioinformatics/btl529.
41. Sorek R, Zhu Y, Creevey CJ, Francino MP, Bork P, Rubin EM: Genome-wide experimental determination of barriers to horizontal gene transfer. Science 2007, 318:1449-1452. 10.1126/science.1147112.
42. Wu M, Eisen JA: A simple, fast, and accurate method of phylogenomic inference. Genome Biol 2008, 9:R151. 10.1186/gb-2008-9-10-r151.
43. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO: SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007, 35:7188-7196. 10.1093/nar/gkm864.
44. Wright ES, Yilmaz LS, Noguera DR: DECIPHER, a search-based approach to Chimera identification for 16S rRNA sequences. Appl Environ Microbiol 2012, 78:717-725. 10.1128/AEM.06516-11.
45. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R: UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011, 27:2194-2200. 10.1093/bioinformatics/btr381.
46. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL: Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006, 72:5069-5072. 10.1128/AEM.03006-05.
47. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R: QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010, 7:335-336. 10.1038/nmeth.f.303.
48. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R: PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 2010, 26:266-267. 10.1093/bioinformatics/btp636.
49. Bond PL, Banfield JF: Design and performance of rRNA targeted oligonucleotide probes for in situ detection and phylogenetic identification of microorganisms inhabiting acid mine drainage environments. Microb Ecol 2001, 41:149-161.
50. Amann R, Ludwig W, Schleifer KH: Phylogenetic identification and in-situ detection of individual microbial-cells without cultivation. Microbiol Rev 1995, 59:143-169.
51. Saraste M: Structure and evolution of cytochrome oxidase. Antonie Van Leeuwenhoek 1994, 65:285-287. 10.1007/BF00872214.
52. Beinert H: Copper A of cytochrome c oxidase, a novel, long-embattled, biological electron-transfer site. Eur J Biochem 1997, 245:521-532. 10.1111/j.1432-1033.1997.t01-1-00521.x.
53. Borisov VB, Gennis RB, Hemp J, Verkhovsky MI: The cytochrome bd respiratory oxygen reductases. BBA - Bioenergetics 1807, 2011:1398-1413.
54. Moparthi VK, Hägerhäll C: The evolution of respiratory chain complex I from a smaller last common ancestor consisting of 11 protein subunits. J Mol Evol 2011, 72:484-497. 10.1007/s00239-011-9447-2.
55. Kerscher S, Dröse S, Zickermann V, Brandt U: The three families of respiratory NADH dehydrogenases. Results Probl Cell Differ 2008, 45:185-222. 10.1007/400_2007_028.
56. Lancaster CRD: Succinate:quinone oxidoreductases: an overview. Biochim Biophys Acta 2002, 1553:1-6. 10.1016/S0005-2728(01)00240-7.
57. Schafer G, Anemuller S, Moll R: Archaeal complex II: 'classical' and "non-classical" succinate: quinone reductases with unusual features. BBA - Bioenergetics 2002, 1553:57-73. 10.1016/S0005-2728(01)00232-8.
58. Schippers A, Jozsa P, Sand W: Sulfur chemistry in bacterial leaching of pyrite. Appl Environ Microbiol 1996, 62:3424-3431.
59. Dopson M, Johnson DB: Biodiversity, metabolism and applications of acidophilic sulfur-metabolizing microorganisms. Environ Microbiol 2012, 14:2620-2631. 10.1111/j.1462-2920.2012.02749.x.
60. Luther GW: Pyrite oxidation and reduction: molecular orbital theory considerations. Geochim Cosmochim Acta 1987, 51:3193-3199. 10.1016/0016-7037(87)90127-X.
61. Urich T, Gomes CM, Kletzin A, Frazão C: X-ray structure of a self-compartmentalizing sulfur cycle metalloenzyme. Science 2006, 311:996-1000. 10.1126/science.1120306.
62. Chen L, Ren Y, Lin J, Liu X, Pang X, Lin J: Acidithiobacillus caldus sulfur oxidation model based on transcriptome analysis between the wild type and sulfur oxygenase reductase defective mutant. PLoS One 2012, 7:e39470. 10.1371/journal.pone.0039470.
63. Zhang H, Guo W, Xu C, Zhou H, Chen X: Site-specific mutagenesis and functional analysis of active sites of sulfur oxygenase reductase from Gram-positive moderate thermophile Sulfobacillus acidophilus TPY. Microbiol Res 2013, 168:654-660. 10.1016/j.micres.2013.04.008.
64. 2 activation. J Mol Microbiol Biotechnol 2005, 10:92-104. 10.1159/000091557.
65. Grein F, Ramos AR, Venceslau SS, Pereira IAC: Unifying concepts in anaerobic respiration: insights from dissimilatory sulfur metabolism. Biochim Biophys Acta 1827, 2013:145-160.
66. Hedderich R, Klimmek O, Kröger A, Dirmeier R, Keller M, Stetter KO: Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol Rev 1999, 22:353-381.
67. Quatrini R, Appia-Ayme C, Denis Y, Jedlicki E, Holmes DS, Bonnefoy V: Extending the models for iron and sulfur oxidation in the extreme Acidophile Acidithiobacillus ferrooxidans. BMC Genomics 2009, 10:394. 10.1186/1471-2164-10-394.
68. Rohwerder T: The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp. Microbiology 2003, 149:1699-1710. 10.1099/mic.0.26212-0.
69. Rohwerder T, Sand W: Oxidation of inorganic sulfur compounds in acidophilic prokaryotes. Eng Life Sci 2007, 7:301-309. 10.1002/elsc.200720204.
70. Hamann N, Mander GJ, Shokes JE, Scott RA, Bennati M, Hedderich R: A cysteine-rich CCG domain contains a novel [4Fe-4S] cluster binding motif as deduced from studies with subunit B of heterodisulfide reductase from Methanothermobacter marburgensis. Biochemistry 2007, 46:12875-12885. 10.1021/bi700679u.
71. Stockdreher Y, Sturm M, Josten M, Sahl H-G, Dobler N, Zigann R, Dahl C: New proteins involved in sulfur trafficking in the cytoplasm of allochromatium vinosum. J Biol Chem 2014, 289:12390-12403. 10.1074/jbc.M113.536425.
72. Stockdreher Y, Venceslau SS, Josten M, Sahl H-G, Pereira IAC, Dahl C: Cytoplasmic sulfurtransferases in the purple sulfur bacterium allochromatium vinosum: evidence for sulfur transfer from DsrEFH to DsrC. PLoS One 2012, 7:e40785. 10.1371/journal.pone.0040785.
73. Morris TW, Reed KE, Cronan JE: Identification of the gene encoding lipoate-protein ligase-a of escherichia-coli - molecular-cloning and characterization of the Lpla gene and gene-product. J Biol Chem 1994, 269:16091-16100.
74. Perham RN: Swinging arms and swinging domains in multifunctional enzymes: catalytic machines for multistep reactions. Annu Rev Biochem 2000, 69:961-1004. 10.1146/annurev.biochem.69.1.961.
75. Liu L-J, Stockdreher Y, Koch T, Sun S-T, Fan Z, Josten M, Sahl H-G, Wang Q, Luo Y-M, Liu S-J, Dahl C, Jiang C-Y: Thiosulfate transfer mediated by DsrE/TusA homologs from acidothermophilic sulfur-oxidizing archaeon metallosphaera cuprina. J Biol Chem 2014, 289:26949-26959. 10.1074/jbc.M114.591669.
76. Strittmatter AW, Liesegang H, Rabus R, Decker I, Amann J, Andres S, Henne A, Fricke WF, Martinez-Arias R, Bartels D, Goesmann A, Krause L, Puehler A, Klenk H-P, Richter M, Schueler M, Gloeckner FO, Meyerdierks A, Gottschalk G, Amann R: Genome sequence of Desulfobacterium autotrophicum HRM2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide. Environ Microbiol 2009, 11:1038-1055. 10.1111/j.1462-2920.2008.01825.x.
77. Marcia M, Ermler U, Peng G, Michel H: A new structure-based classification of sulfide:quinone oxidoreductases. Proteins: Struct Funct Bioinformatics 2009, 78:1073-1083.
78. Wakai S, Tsujita M, Kikumoto M, Manchur MA, Kanao T, Kamimura K: Purification and characterization of sulfide: quinone oxidoreductase from an acidophilic iron-oxidizing bacterium, Acidithiobacillus ferrooxidans. Biosci Biotechnol Biochem 2007, 71:2735-2742. 10.1271/bbb.70332.
79. Cherney MM, Zhang Y, Solomonson M, Weiner JH, James MNG: Crystal structure of sulfide: quinone oxidoreductase from acidithiobacillus ferrooxidans: insights into sulfidotrophic respiration and detoxification. J Mol Biol 2010, 398:292-305. 10.1016/j.jmb.2010.03.018.
80. Lencina AM, Ding Z, Schurig-Briccio LA, Gennis RB: Characterization of the type III sulfide:quinone oxidoreductase from Caldivirga maquilingensis and its membrane binding. Biochim Biophys Acta 1827, 2013:266-275.
81. De Jong GA, Hazeu W, Bos P, Kuenen JG: Isolation of the tetrathionate hydrolase from Thiobacillus acidophilus. Eur J Biochem 1997, 243:678-683. 10.1111/j.1432-1033.1997.00678.x.
82. Kanao T, Kamimura K, Sugio T: Identification of a gene encoding a tetrathionate hydrolase in Acidithiobacillus ferrooxidans. J Biotechnol 2007, 132:16-22. 10.1016/j.jbiotec.2007.08.030.
83. Bugaytsova Z, Lindström EB: Localization, purification and properties of a tetrathionate hydrolase from Acidithiobacillus caldus. Eur J Biochem 2004, 271:272-280. 10.1046/j.1432-1033.2003.03926.x.
84. Egorova MA, Tsaplina IA, Zakharchuk LM, Bogdanova TI, Krasil'nikova EN: Effect of cultivation conditions on the growth and activities of sulfur metabolism enzymes and carboxylases of Sulfobacillus thermosulfidooxidans subsp asporogenes strain 41. Appl Biochem Microbiol 2004, 40:381-387.
85. Shiers DW, Ralph DE, Watling HR: A comparative study of substrate utilisation by Sulfobacillus species in mixed ferrous ion and tetrathionate growth medium. Hydrometallurgy 2010, 104:363-369. 10.1016/j.hydromet.2010.03.023.
86. Protze J, Müller F, Lauber K, Naß B, Mentele R, Lottspeich F, Kletzin A: An extracellular tetrathionate hydrolase from the thermoacidophilic archaeon acidianus ambivalens with an activity optimum at pH 1. Front Microbiol 2011, 2:68.
87. Müller FH, Bandeiras TM, Urich T, Teixeira M, Gomes CM, Kletzin A: Coupling of the pathway of sulphur oxidation to dioxygen reduction: characterization of a novel membrane-bound thiosulphate:quinone oxidoreductase. Mol Microbiol 2004, 53:1147-1160. 10.1111/j.1365-2958.2004.04193.x.
88. Rothery RA, Workun GJ, Weiner JH: The prokaryotic complex iron-sulfur molybdoenzyme family. Biochim Biophys Acta 2008, 1778:1897-1929. 10.1016/j.bbamem.2007.09.002.
89. Hinsley AP, Berks BC: Specificity of respiratory pathways involved in the reduction of sulfur compounds by Salmonella enterica. Microbiol-Sgm 2002, 148:3631-3638.
90. Guiral M, Tron P, Aubert C, Gloter A, Iobbi-Nivol C, Giudici-Orticoni M-T: A membrane-bound multienzyme, hydrogen-oxidizing, and sulfur-reducing complex from the hyperthermophilic bacterium Aquifex aeolicus. J Biol Chem 2005, 280:42004-42015. 10.1074/jbc.M508034200.
91. Dahl C, Franz B, Hensen D, Kesselheim A, Zigann R: Sulfite oxidation in the purple sulfur bacterium Allochromatium vinosum: identification of SoeABC as a major player and relevance of SoxYZ in the process. Microbiol-Sgm 2013, 159:2626-2638. 10.1099/mic.0.071019-0.
92. Kopriva S, Buchert T, Fritz G, Suter M, Benda RD, Schunemann V, Koprivova A, Schurmann P, Trautwein AX, Kroneck P, Brunold C: The presence of an iron-sulfur cluster in adenosine 5 '-phosphosulfate reductase separates organisms utilizing adenosine 5 '-phosphosulfate and phosphoadenosine 5'-phosphosulfate for sulfate assimilation. J Biol Chem 2002, 277:21786-21791. 10.1074/jbc.M202152200.
93. Bick JA, Dennis JJ, Zylstra GJ, Nowack J, Leustek T: Identification of a new class of 5'-adenylylsulfate (APS) reductases from sulfate-assimilating bacteria. J Bacteriol 2000, 182:135-142. 10.1128/JB.182.1.135-142.2000.
94. Bonnefoy V, Holmes DS: Genomic insights into microbial iron oxidation and iron uptake strategies in extremely acidic environments. Environ Microbiol 2011, 14:1597-1611.
95. Coupland K, Johnson DB: Evidence that the potential for dissimilatory ferric iron reduction is widespread among acidophilic heterotrophic bacteria. FEMS Microbiol Lett 2008, 279:30-35. 10.1111/j.1574-6968.2007.00998.x.
96. Johnson DB, Kanao T, Hedrich S: Redox transformations of iron at extremely low pH: fundamental and applied aspects. Front Microbiol 2012, 3:1-13.
97. Ohmura N, Sasaki K, Matsumoto N, Saiki H: Anaerobic respiration using Fe3+, S0, and H2 in the chemolithoautotrophic bacterium acidithiobacillus ferrooxidans. J Bacteriol 2002, 184:2081-2087. 10.1128/JB.184.8.2081-2087.2002.
98. Kucera J, Bouchal P, Cerna H, Potesil D, Janiczek O, Zdrahal Z, Mandl M: Kinetics of anaerobic elemental sulfur oxidation by ferric iron in Acidithiobacillus ferrooxidans and protein identification by comparative 2-DE-MS/MS. Antonie Van Leeuwenhoek 2011, 101:561-573.
99. Osorio H, Mangold S, Denis Y, Nancucheo I, Esparza M, Johnson DB, Bonnefoy V, Dopson M, Holmes DS: Anaerobic sulfur metabolism coupled to dissimilatory iron reduction in the extremophile acidithiobacillus ferrooxidans. Appl Environ Microbiol 2013, 79:2172-2181. 10.1128/AEM.03057-12.
100. Thamdrup B, Finster K, Hansen JW, Bak F: Bacterial disproportionation of elemental sulfur coupled to chemical reduction of iron or manganese. Appl Environ Microbiol 1993, 59:101-108.
101. Hardisty DS, Olyphant GA, Bell JB, Johnson AP, Pratt LM: Acidophilic sulfur disproportionation. Geochim Cosmochim Acta 2013,113(C):136-151.
102. Karavaiko GI, Krasil'nikova EN, Tsaplina IA, Bogdanova TI, Zakharchuk LM: Growth and carbohydrate metabolism of sulfobacilli. Microbiology 2001, 70:245-250. 10.1023/A:1010463007138.
103. Vignais PM, Billoud B: Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 2007, 107:4206-4272. 10.1021/cr050196r.
104. Constant P, Chowdhury SP, Pratscher J, Conrad R: Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase. Environ Microbiol 2010, 12:821-829. 10.1111/j.1462-2920.2009.02130.x.
105. Constant P, Chowdhury SP, Hesse L, Pratscher J, Conrad R: Genome data mining and soil survey for the novel group 5 NiFe -hydrogenase to explore the diversity and ecological importance of presumptive high-affinity H-2-oxidizing bacteria. Appl Environ Microbiol 2011, 77:6027-6035. 10.1128/AEM.00673-11.
106. Thauer RK, Kaster A-K, Goenrich M, Schick M, Hiromoto T, Shima S: Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H 2Storage. Annu Rev Biochem 2010, 79:507-536. 10.1146/annurev.biochem.030508.152103.
107. Coppi MV: The hydrogenases of Geobacter sulfurreducens: a comparative genomic perspective. Microbiol-Sgm 2005, 151:1239-1254. 10.1099/mic.0.27535-0.
108. Marreiros BC, Batista AP, Duarte AMS, Pereira MM: A missing link between complex I and group 4 membrane-bound [NiFe] hydrogenases. BBA - Bioenergetics 1827, 2013:198-209.
109. King GM, Weber CF: Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat Rev Microbiol 2007, 5:107-118. 10.1038/nrmicro1595.
110. Lin JT, Lin JT, Stewart V, Stewart V: Nitrate assimilation by bacteria. Adv Microb Physiol 1998, 39:1-30. 379
111. Richardson DJ, Berks BC, Russell DA, Spiro S, Taylor CJ: Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci 2001, 58:165-178. 10.1007/PL00000845.
112. Gardner PR: Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J Inorg Biochem 2005, 99:247-266. 10.1016/j.jinorgbio.2004.10.003.
113. Poole RK, Hughes MN: New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol Microbiol 2000, 36:775-783. 10.1046/j.1365-2958.2000.01889.x.
114. Caldwell PE, MacLean MR, Norris PR: Ribulose bisphosphate carboxylase activity and a Calvin cycle gene cluster in Sulfobacillus species. Microbiol-Sgm 2007, 153:2231-2240. 10.1099/mic.0.2007/006262-0.
115. Tabita FR, Hanson TE, Li HY, Satagopan S, Singh J, Chan S: Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol Mol Biol Rev 2007, 71:576-599. 10.1128/MMBR.00015-07.
116. Barrie Johnson D, Hallberg KB: Carbon, Iron and Sulfur Metabolism in Acidophilic Micro-Organisms. In Advances in Microbial Physiology, volume 54. Edited by: Poole RK. Elsevier; 2008:201-255. [Advances in Microbial Physiology]
117. Sugiyama M, Suzuki S-I, Tonouchi N, Yokozeki K: Transaldolase/glucose-6-phosphate isomerase bifunctional enzyme and ribulokinase as factors to increase xylitol production from D-arabitol in Gluconobacter oxydans. Biosci Biotechnol Biochem 2003, 67:2524-2532. 10.1271/bbb.67.2524.
118. Kim S, Lee SB: Identification and characterization of the bacterial d-gluconate dehydratase in Achromobacter xylosoxidans. Biotechnol Bioprocess Eng 2008, 13:436-444. 10.1007/s12257-008-0152-y.
119. Krasil'nikova EN, Zakharchuk LM, Egorova MA, Bogdanova TI, Zhuravleva AE, Tsaplina IA: Regulation of metabolic pathways in sulfobacilli under different aeration regimes. Microbiology 2010, 79:147-152. 10.1134/S0026261710020037.
120. Nancucheo I, Johnson DB: Production of glycolic acid by chemolithotrophic iron- and sulfur-oxidizing bacteria and its role in delineating and sustaining acidophilic sulfide mineral-oxidizing consortia. Appl Environ Microbiol 2010, 76:461-467. 10.1128/AEM.01832-09.
121. Chai Y, Kolter R, Losick R: A widely conserved gene cluster required for lactate utilization in bacillus subtilis and its involvement in biofilm formation. J Bacteriol 2009, 191:2423-2430. 10.1128/JB.01464-08.
122. Tholozan JL, Touzel JP, Samain E, Grivet JP, Prensier G, Albagnac G: Clostridium neopropionicum sp. nov., a strict anaerobic bacterium fermenting ethanol to propionate through acrylate pathway. Arch Microbiol 1992, 157:249-257. 10.1007/BF00245158.
123. Schink B, Kremer DR, Hansen TA: Pathway of propionate formation from ethanol in Pelobacter propionicus. Arch Microbiol 1987, 147:321-327. 10.1007/BF00406127.
124. Tsaplina IA, Osipov GA, Bogdanova TI, NEDOREZOVA TP, Karavaiko GI: Fatty-acid composition of lipids in thermoacidophilic bacteria of the genus sulfobacillus. Microbiology 1994, 63:459-464.
125. Kaneda T: Iso-and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol Rev 1991, 55:288-302.
126. Oshima M, Ariga T: Omega-cyclohexyl fatty-acids in acidophilic thermophilic bacteria - studies on their presence, structure, and biosynthesis using precursors labeled with stable isotopes and radioisotopes. J Biol Chem 1975, 250:6963-6968.
127. Duda VI, Suzina NE, Severina LO, Dmitriev VV, Karavaiko GI: Formation of flat lamellar intramembrane lipid structures in microorganisms. J Membr Biol 2001, 180:33-48. 10.1007/s002320010057.
128. Kannenberg EL, Poralla K: Hopanoid biosynthesis and function in bacteria. Naturwissenschaften 1999, 86:168-176. 10.1007/s001140050592.
129. Spanova M, Daum G: Squalene - biochemistry, molecular biology, process biotechnology, and applications. Eur J Lipid Sci Technol 2011, 113:1299-1320. 10.1002/ejlt.201100203.
130. Jones DS, Jones DS, Albrecht HL, Albrecht HL, Dawson KS, Dawson KS, Schaperdoth I, Schaperdoth I, Freeman KH, Freeman KH, Pi Y, Pi Y, Pearson A, Pearson A, Macalady JL, Macalady JL: Community genomic analysis of an extremely acidophilic sulfur-oxidizing biofilm. ISME J 2011, 6:158-170.
131. Welander PV, Doughty DM, Wu C-H, Mehay S, Summons RE, Newman DK: Identification and characterization of Rhodopseudomonas palustris TIE-1 hopanoid biosynthesis mutants. Geobiology 2012, 10:163-177. 10.1111/j.1472-4669.2011.00314.x.
132. Cárdenas JP, Moya F, Covarrubias P, Shmaryahu A, Levicán G, Holmes DS, Quatrini R: Comparative genomics of the oxidative stress response in bioleaching microorganisms. Hydrometallurgy 2012,127-128(C):162-167.
133. Norambuena J, Flores R, Cárdenas JP, Quatrini R, Chávez R, Levicán G: Thiol/disulfide system plays a crucial role in redox protection in the acidophilic iron-oxidizing bacterium leptospirillum ferriphilum. PLoS One 2012, 7:e44576. 10.1371/journal.pone.0044576.
134. Empadinhas N, da Costa MS: Diversity and biosynthesis of compatible solutes in hyper/thermophiles. Int Microbiol 2006, 9:199-206.
135. Mosier AC, Justice NB, Bowen BP, Baran R, Thomas BC, Northen TR, Banfield JF: Metabolites associated with adaptation of microorganisms to an acidophilic, metal-rich environment identified by stable-isotope-enabled metabolomics. MBio 2013, 4:e00484-12.
136. Bren A, Eisenbach M: How signals are heard during bacterial chemotaxis: protein-protein interactions in sensory signal propagation. J Bacteriol 2000, 182:6865-6873. 10.1128/JB.182.24.6865-6873.2000.
137. Ghauri MA, Johnson DB: Physiological diversity amongst some moderately thermophilic iron-oxidizing bacteria. FEMS Microbiol Ecol 1991, 85:327-334. 10.1111/j.1574-6968.1991.tb04759.x.
138. Wood AP, Kelly DP: Autotrophic and mixotrophic growth of three thermoacidophilic iron-oxidizing bacteria. FEMS Microbiol Lett 1983, 20:107-112. 10.1111/j.1574-6968.1983.tb00098.x.
139. Wood AP, Kelly DP: Growth and sugar metabolism of a thermoaddophilic iron-oxidizing mixotrophic bacterium. Microbiology 1984, 130:1337-1349. 10.1099/00221287-130-6-1337.
140. Tsaplina IA, Krasil'nikova EN, Zhuravleva AE, Egorova MA, Zakharchuk LM, Suzina NE, Duda VI, Bogdanova TI, Stadnichuk IN, Kondrat'eva TF: The dependence of intracellular ATP level on the nutrition mode of the acidophilic bacteria Sulfobacillus thermotolerans and Alicyclobacillus tolerans. Microbiology 2008, 77:654-664. 10.1134/S0026261708060027.
141. Ma S, Banfield JF: Micron-scale Fe2+/Fe3+, intermediate sulfur species and O2 gradients across the biofilm-solution-sediment interface control biofilm organization. Geochim Cosmochim Acta 2011, 75:3568-3580. 10.1016/j.gca.2011.03.035.
142. Druschel GK, Hamers RJ, Banfield JF: Kinetics and mechanism of polythionate oxidation to sulfate at low pH by O2 and Fe3. Geochim Cosmochim Acta 2003, 67:4457-4469. 10.1016/S0016-7037(03)00388-0.