Chemolithotrophic growth of the aerobic hyperthermophilic bacterium Thermocrinis ruber OC 14/7/2 on monothioarsenate and arsenite

FEMS Microbiology Ecology

Volumn 90, Issue 3, 2014, Pages 747-760

  Härtig, Cornelia ^a   Lohmayer, Regina ^a   Kolb, Steffen ^a   Horn, Marcus A ^a   Inskeep, William P ^b   Planer Friedrich, Britta ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

Aquificales; Biogeochemistry; Chemolithotrophy; Thioarsenic species; Yellowstone National Park

Indexed keywords

AQUIFICALES; BACTERIA (MICROORGANISMS); THERMOCRINIS RUBER;

ARSENIC; ARSENIC ACID; ARSENIC ACID DERIVATIVE; ARSENIC TRIOXIDE; ARSENOUS ACID DERIVATIVE; SULFATE; SULFIDE; SULFUR;

BACTERIUM; CHEMOAUTOTROPHY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PH; THERMAL SPRING;

ARSENATES; ARSENIC; ARSENITES; BACTERIA; CHEMOAUTOTROPHIC GROWTH; HOT SPRINGS; HYDROGEN-ION CONCENTRATION; OXIDATION-REDUCTION; SULFATES; SULFIDES; SULFUR;

EID: 84914816148     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12431     Document Type: Article

References (61)

1. Aguiar P, Beveridge TJ & Reysenbach AL (2004) Sulfurihydrogenibium azorense, sp. nov., a thermophilic hydrogen-oxidizing microaerophile from terrestrial hot springs in the Azores. Int J Syst Evol Microbiol 54: 33-39.
2. Amend JP & Shock EL (2001) Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol Rev 25: 175-243.
3. Akerman NH, Price RE, Pichler T & Ahmend JP (2011) Energy sources for chemolithotrophs in an arsenic- and iron-rich shallow-sea hydrothermal system. Geobiol 9: 436-445.
4. Braakman R, Smith E & de Crécy-Lagard V (2014) Metabolic evolution of a deep-branching hyperthermophilic chemoautotrophic bacterium. PLoS One 9: e87950.
5. Brauner B & Tomicek F (1888) Ueber die Einwirkung von Schwefelwasserstoff auf Arsensäure. Fresenius Z Anal Chem 27: 508-513.
6. Breitbart M, Wegley L, Leeds S, Schoenfeld T & Rohwer F (2004) Phage community dynamics in hot springs. Appl Environ Microbiol 70: 1633-1640.
7. Cherney MM, Zhang Y, Solomonson M, Weiner JH & James MNG (2010) Crystal structure of sulfide: quinone oxidoreductase from Acidithiobacillus ferrooxidans: insights into sulfidotrophic respiration and detoxification. J Mol Biol 398: 292-305.
8. Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14: 454-459.
9. Connon SA, Koski AK, Neal AL, Wood SA & Magnuson TS (2008) Ecophysiology and geochemistry of microbial arsenic oxidation within a high arsenic, circumneutral hot spring system of the Alvord Desert. FEMS Microbiol Ecol 64: 117-128.
10. Dahl C & Friedrich CG (2008) Microbial Sulfur Metabolism, 1st edn. Springer, Berlin, New York.
11. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A & Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by Bacteria: emergence of a common mechanism? Appl Environ Microbiol 67: 2873-2882.
12. Friedrich CG, Bardischewsky F, Rother D, Quentmeier A & Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8: 253-259.
13. Ghosh W & Dam B (2009) Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse Bacteria and Archaea. FEMS Microbiol Rev 33: 999-1043.
14. Ghosh W, Mallick S & DasGupta SK (2009) Origin of the Sox multienzyme complex system in ancient thermophilic Bacteria and coevolution of its constituent proteins. Res Microbiol 160: 409-420.
15. Gihring TM, Druschel GK, McCleskey RB, Hamers RJ & Banfield JF (2001) Rapid arsenite oxidation by Thermus aquaticus and Thermus thermophilus: field and laboratory investigations. Environ Sci Technol 35: 3857-3862.
16. Hall JR, Mitchell KR, Jackson-Weaver O, Kooser AS, Cron BR, Crossey LJ & Takacs-Vesbach CD (2008) Molecular characterization of the diversity and distribution of a thermal spring microbial community using rRNA and Metabolic Genes. Appl Environ Microbiol 74: 4910-4922.
17. Hamamura N, Macur RE, Korf S, Ackerman G, Taylor WP, Kozubal M, Reysenbach A & Inskeep WP (2009) Linking microbial oxidation of arsenic with detection and phylogenetic analysis of arsenite oxidase genes in diverse geothermal environments. Environ Microbiol 11: 421-431.
18. Hamamura N, Macur RE, Liu Y, Inskeep WP & Reysenbach A (2010) Distribution of aerobic arsenite oxidase genes within the Aquificales. Interdisciplinary Studies on Environmental Chemistry, Volume 3. Biological Responses to Contaminants: From Molecular to Community Level (Hamamura N, Suzuki S, Mendo S, Barroso CM, Iwata H & Tanabe S, eds), pp. 47-55. Terrapub, Tokyo. http://www.terrapub.co.jp/onlineproceedings/ec/03/pdf/BR_03047.pdf.
19. Härtig C & Planer-Friedrich B (2012) Thioarsenate transformation by filamentous microbial mats thriving in an alkaline, sulfidic hot spring. Environ Sci Technol 46: 4348-4356.
20. Hensen D, Sperling D, Trüper HG, Brune DC & Dahl C (2006) Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Mol Microbiol 62: 794-810.
21. Hetzer A, McDonald IR & Morgan HW (2008) Venenivibrio stagnispumantis gen. nov., sp. nov., a thermophilic hydrogen-oxidizing bacterium isolated from Champagne Pool, Waiotapu, New Zealand. Int J Syst Evol Microbiol 58: 398-403.
22. Hollibaugh JT, Carini S, Gürleyük H, Jellison R, Joye SB, LeCleir G, Meile C, Vasquez L & Wallschläger D (2005) Arsenic speciation in Mono Lake, California: response to seasonal stratification and anoxia. Geochim Cosmochim Acta 69: 1925-1937.
23. Huber R, Eder W, Heldwein S, Wanner G, Huber H, Rachel R & Stetter KO (1998) Thermocrinis ruber gen. nov., sp. nov., a pink-filament-forming hyperthermophilic bacterium isolated from Yellowstone National Park. Appl Environ Microbiol 64: 3576-3583.
24. 2 fixation via the reductive tricarboxylic acid cycle in different lineages within the phylum Aquificae: evidence for two ways of citrate cleavage. Environ Microbiol 9: 81-92.
25. Inskeep WP, Ackerman G, Taylor KG, Kozubal M, Korf S & Macur RE (2005) On the energetics of chemolithotrophy in non-equilibrium systems: case studies of geothermal springs in Yellowstone National Park. Geobiology 3: 297-317.
26. Inskeep WP, Macur RE, Hamamura N, Warelow TP, Ward SA & Santini JM (2007) Detection, diversity and expression of aerobic bacterial arsenite oxidase genes. Environ Microbiol 9: 934-943.
27. Jackson CR, Langner HW, Donahoe-Christiansen J, Inskeep WP & McDermott TR (2001) Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring. Environ Microbiol 3: 532-542.
28. Jahnke LL, Eder W, Huber R, Hope JM, Hinrichs KU, Hayes JM, Des Marais DJ, Cady SL & Summons RE (2001) Signature lipids and stable carbon isotope analyses of Octopus Spring hyperthermophilic communities compared with those of Aquificales representatives. Appl Environ Microbiol 67: 5179-5189.
29. Kamyshny A, Ekeltchik I, Gun J & Lev O (2006) Method for the determination of inorganic polysulfide distribution in aquatic systems. J Anal Chem 78: 2631-2639.
30. Kelly DP (1999) Thermodynamic aspects of energy conservation by chemolithotrophic sulfur bacteria in relation to the sulfur oxidation pathways. Arch Microbiol 171: 219-229.
31. Kubo K, Knittel K, Amann R, Fukui M & Matsuura K (2011) Sulfur-metabolizing bacterial populations in microbial mats of the Nakabusa hot spring, Japan. Syst Appl Microbiol 34: 293-302.
32. Langner HW, Jackson CR, McDermott TR & Inskeep WP (2001) Rapid oxidation of arsenite in a hot spring ecosystem, Yellowstone National Park. Environ Sci Technol 35: 3302-3309.
33. Lett M, Muller D, Lièvremont D, Silver S & Santini J (2012) Unified nomenclature for genes involved in prokaryotic aerobic arsenite oxidation. J Bacteriol 194: 207-208.
34. Macur RE, Langner HW, Kocar BD & Inskeep WP (2004) Linking geochemical processes with microbial community analysis: successional dynamics in an arsenic-rich, acid-sulphate-chloride geothermal spring. Geobiology 2: 163-177.
35. Mamindy-Pajany Y, Bataillard P, Séby F, Crouzet C, Moulin A, Guezennec A, Hurel C, Marmier N & Battaglia-Brunet F (2013) Arsenic in marina sediments from the mediterranean coast: speciation in the solid phase and occurrence of thioarsenates. Soil Sediment Contam 22: 984-1002.
36. Marcia M, Ermler U, Peng G & Michel H (2009) The structure of Aquifex aeolicus sulfide: quinone oxidoreductase, a basis to understand sulfide detoxification and respiration. P Natl Acad Sci USA 106: 9625-9630.
37. McCay LW (1902) Die Einwirkung von Schwefelwasserstoff auf Arsensäure. Z Anorg Chem 29: 36-50.
38. McCay LW & Foster W (1904) Über die Trisulfoxyarsensäure. Z Anorg Chem 41: 452-473.
39. Meyer B, Imhoff JF & Kuever J (2007) Molecular analysis of the distribution and phylogeny of the soxB gene among sulfur-oxidizing Bacteria - evolution of the Sox sulfur oxidation enzyme system. Environ Microbiol 9: 2957-2977.
40. Noble RT & Fuhrman JA (1998) Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14: 113-118.
41. Nübel T, Klughammer C, Huber R, Hauska G & Schütz M (2000) Sulfide: quinone oxidoreductase in membranes of the hyperthermophilic bacterium Aquifex aeolicus (VF5). Arch Microbiol 173: 233-244.
42. Planer-Friedrich B & Wallschläger D (2009) A critical investigation of hydride generation-based arsenic speciation in sulfidic waters. Environ Sci Technol 43: 5007-5013.
43. Planer-Friedrich B, London J, McCleskey RB, Nordstrom DK & Wallschläger D (2007) Thioarsenates in geothermal waters of Yellowstone National Park: determination, preservation, and geochemical importance. Environ Sci Technol 41: 5245-5251.
44. Planer-Friedrich B, Fisher JC, Hollibaugh JT, Süß E & Wallschläger D (2009) Oxidative transformation of trithioarsenate along alkaline geothermal drainages - abiotic versus microbially mediated processes. Geomicrobiol J 26: 339-350.
45. Planer-Friedrich B, Suess E, Scheinost AC & Wallschläger D (2010) Arsenic speciation in sulfidic waters: reconciling contradictory spectroscopic and chromatographic evidence. J Anal Chem 82: 10228-10235.
46. Rizkov D, Lev O, Gun J, Anisimov B & Kuselman I (2004) Development of in-house reference materials for determination of inorganic polysulfides in water. Accred Qual Assur 9: 399-403.
47. Schwedt G & Rieckhoff M (1996a) Separation of thio- and oxothioarsenates by capillary zone electrophoresis and ion chromatography. J Chromatog A 736: 341-350.
48. Schwedt G & Rieckhoff M (1996b) Zur Analytik von Oxothioarsen-species in Schlacken und Grubenwässern. J Prakt Chemie 338: 55-59.
49. Stauder S, Raue B & Sacher F (2005) Thioarsenates in sulfidic waters. Environ Sci Technol 39: 5933-5939.
50. Suess E, Scheinost AC, Bostick BC, Merkel BJ, Wallschlaeger D & Planer-Friedrich B (2009) Discrimination of thioarsenites and thioarsenates by X-ray absorption spectroscopy. J Anal Chem 81: 8318-8326.
51. Takacs-Vesbach C, Inskeep WP, Jay ZJ et al. (2013) Metagenome sequence analysis of filamentous microbial communities obtained from geochemically distinct geothermal channels reveals specialization of three Aquificales lineages. Front Microbiol 4: doi:10.3389/fmicb.2013.00084.
52. Takai K, Kobayashi H, Nealson KH & Horikoshi K (2003) Sulfurihydrogenibium subterraneum gen. nov., sp. nov., from a subsurface hot aquifer. Int J Syst Evol Microbiol 53: 823-827.
53. Theissen U, Hoffmeister M, Grieshaber M & Martin W (2003) Single eubacterial origin of eukaryotic sulfide: quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Mol Biol Evol 20: 1564-1574.
54. Thilo E, Hertzog K & Winkler A (1970) Über Vorgänge bei der Bildung des Arsen(V)-sulfids beim Ansäuern von Tetrathioarsenatlösungen. Z Anorg Allg Chem 373: 111-121.
55. Ullrich MK, Pope JG, Seward TM, Wilson N & Planer-Friedrich B (2013) Sulfur redox chemistry governs diurnal antimony and arsenic cycles at Champagne Pool, Waiotapu, New Zealand. J Volcanol Geotherm Res 262: 164-177.
56. Vairavamurthy A, Manowitz B, Luther G & Jeon Y (1993) Oxidation state of sulfur in thiosulfate and implications for anaerobic energy metabolism. Geochim Cosmochim Acta 57: 1619-1623.
57. Wallschläger D & Stadey CJ (2007) Determination of (oxy)thioarsenates in sulfidic waters. J Anal Chem 79: 3873-3880.
58. Wegley L, Mosier-Boss P, Lieberman S, Andrews J, Graff-Baker A & Rohwer F (2006) Rapid estimation of microbial numbers in water using bulk fluorescence. Environ Microbiol 8: 1775-1782.
59. Wilkin RT, Wallschläger D & Ford RG (2003) Speciation of arsenic in sulfidic waters. Geochem Trans 4: 1-7.
60. Wirth R, Sikorski J, Brambilla E et al. (2010) Complete genome sequence of Thermocrinis albus type strain (HI 11/12T). Stand Genomic Sci 2: 194-202.
61. Zhang J, Kim H & Townsend T (2014) Methodology for assessing thioarsenic formation potential in sulfidic landfill environments. Chemosphere 107: 311-318.