Reduced inorganic sulfur oxidation supports autotrophic and mixotrophic growth of Magnetospirillum strain J10 and Magnetospirillum gryphiswaldense

Environmental Microbiology

Volumn 12, Issue 4, 2010, Pages 1031-1040

  Geelhoed, Jeanine S ^a,b   Kleerebezem, Robbert ^a   Sorokin, Dimitry Y ^a,c   Stams, Alfons J M ^b   van Loosdrecht, Mark C M ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c WINOGRADSKY INSTITUTE OF MICROBIOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); MAGNETOSPIRILLUM; MAGNETOSPIRILLUM GRYPHISWALDENSE;

ACETIC ACID DERIVATIVE; FRESH WATER; SULFIDE; THIOSULFATE;

ARTICLE; AUTOTROPHY; CULTURE MEDIUM; GROWTH, DEVELOPMENT AND AGING; HETEROTROPHY; MAGNETOSPIRILLUM; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION;

ACETATES; AUTOTROPHIC PROCESSES; CULTURE MEDIA; FRESH WATER; HETEROTROPHIC PROCESSES; MAGNETOSPIRILLUM; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; SULFIDES; THIOSULFATES;

EID: 77954636619     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2009.02148.x     Document Type: Article

References (50)

1. Anandham R, Indiragandhi P, Madhaiyan M, Kim K, Yim W, Saravanan VS. Thiosulfate oxidation and mixotrophic growth of Methylobacterium oryzae. Can J Microbiol 2007, 53:869-876.
2. Banciu H, Sorokin DY, Kleerebezem R, Muyzer G, Galinski EA, Kuenen JG. Growth kinetics of haloalkaliphilic, sulfur-oxidizing bacterium Thioalkalivibrio versutus strain ALJ 15 in continuous culture. Extremophiles 2004, 8:185-192.
3. Bazylinski DA, Frankel RB. Magnetosome formation in prokaryotes. Nat Rev Microbiol 2004, 2:217-230.
4. Bazylinski DA, Frankel RB, Heywood BR, Mann S, King JW, Donaghay PL, Hanson AK. Controlled biomineralization of magnetite (Fe3O4) and greigite (Fe3S4) in a magnetotactic bacterium. Appl Environ Microbiol 1995, 61:3232-3239.
5. Bazylinski DA, Dean AJ, Williams TJ, Kimble Long L, Middleton SL, Dubbels BL. Chemolithoautotrophy in the marine, magnetotactic bacterial strains MV-1 and MV-2. Arch Microbiol 2004, 182:373-387.
6. Beller HR, Chain PSG, Letain TE, Chakicherla A, Larimer FW, Richardson PM. The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J Bacteriol 2006, 188:1473-1488.
7. Blakemore RP, Maratea D, Wolfe RS. Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J Bacteriol 1979, 140:720-729.
8. Dahl C, Schulte A, Stockdreher Y, Hong C, Grimm F, Sander J. Structural and molecular genetic insight into a widespread sulfur oxidation pathway. J Mol Biol 2008, 384:1287-1300.
9. Dijkhuizen L, Harder W. Regulation of autotrophic and heterotrophic metabolism in Pseudomonas oxalaticus OX1: growth on mixtures of acetate and formate in continuous culture. Arch Microbiol 1979, 123:47-53.
10. Farina M, Esquivel DMS, Debarros H. Magnetic iron-sulfur crystals from a magnetotactic microorganism. Nature 1990, 343:256-258.
11. Flies CB, Peplies J, Schüler D. Combined approach for characterization of uncultivated magnetotactic bacteria from various aquatic environments. Appl Environ Microbiol 2005a, 71:2723-2731.
12. Flies CB, Jonkers HM, De Beer D, Bosselmann K, Böttcher ME, Schüler D. Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. FEMS Microbiol Ecol 2005b, 52:185-195.
13. Frankel RB, Bazylinski DA, Johnson MS, Taylor BL. Magneto-aerotaxis in marine coccoid bacteria. Biophys J 1997, 73:994-1000.
14. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J. Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 2001, 67:2873-2882.
15. Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J. Prokaryotic sulfur oxidation. Curr Opin Microbiol 2005, 8:253-259.
16. Frigaard NU, Dahl C. Sulfur metabolism in phototrophic sulfur bacteria. Advances in Microbial Physiology 2009, 103-200. Poole RK, In, Vol. 54, ed., London, UK, Academic Press, pp.
17. Geelhoed JS, Sorokin DY, Epping E, Tourova TP, Banciu H, Muyzer G. Microbial sulfide oxidation in the oxic-anoxic transition zone of freshwater sediment: involvement of lithoautotrophic Magnetospirillum strain J10. FEMS Microbiol Ecol 2009, 70:54-65.
18. Ghosh W, Dam B. Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse Bacteria and Archaea. FEMS Microbiol Rev 2009, 33:999-1043.
19. Gommers PJF, Van Schie BJ, Van Dijken JP, Kuenen JG. Biochemical limits to microbial growth yields: an analysis of mixed substrate utilization. Biotechnol Bioeng 1988, 32:86-94.
20. Gottschal JC, Kuenen JG. Mixotrophic growth of Thiobacillus A2 on acetate and thiosulfate as growth limiting substrates in the chemostat. Arch Microbiol 1980, 126:33-42.
21. Gottschal JC, Vries SD, Kuenen JG. Competition between the facultatively chemolithotrophic Thiobacillus A2, an obligately chemolithotrophic Thiobacillus and a heterotrophic spirillum for inorganic and organic substrates. Arch Microbiol 1979, 121:241-249.
22. Guerin WF, Blakemore RP. Redox cycling of iron supports growth and magnetite synthesis by Aquaspirillum magnetotacticum. Appl Environ Microbiol 1992, 58:1102-1109.
23. Heijnen JJ. Bioenergetics of microbial growth. Encyclopedia of Bioprocess Technology: Fermentation, Biocatalysis and Bioseparation 1999, 267-291. Flickinger MCDrew SW., New York, USA, John Wiley and Sons, pp.
24. Heijnen JJ, van Dijken JP. In search of a thermodynamic description of biomass yields for the chemotropic growth of microorganisms. Biotechnol Bioeng 1992, 39:833-858.
25. Heyen U, Schüler D. Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor. Appl Microbiol Biotechnol 2003, 61:536-544.
26. Kappler U, Dahl C. Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol Lett 2001, 203:1-9.
27. Kappler U, Friedrich CG, Truper HG, Dahl C. Evidence for two pathways of thiosulfate oxidation in Starkeya novella (formerly Thiobacillus novellus). Arch Microbiol 2001, 175:102-111.
28. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin-phenol reagents. J Biol Chem 1951, 193:265-275.
29. Lu WP, Swoboda BEP, Kelly DP. Properties of the thiosulfate-oxidizing multi-enzyme system from Thiobacillus versutus. Biochim Biophys Acta 1985, 828:116-122.
30. Mason J, Kelly DP, Wood AP. Chemolithotrophic and autotrophic growth of Thermothrix thiopara and some Thiobacilli on thiosulphate and polythionates, and a reassessment of the growth yields of Thx. thiopara in chemostat culture. J Gen Microbiol 1987, 133:1249-1256.
31. Matsunaga T, Okamura Y, Fukumori Y, Wahyudi AT, Murase Y, Takeyama H. Complete genome sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp. strain AMB-1. DNA Res 2005, 12:157-166.
32. Noguchi Y, Fujiwara T, Yoshimatsu K, Fukumori Y. Iron reductase for magnetite synthesis in the magnetotactic bacterium Magnetospirillum magnetotacticum. J Bacteriol 1999, 181:2142-2147.
33. Perez RC, Matin A. Carbon-dioxide assimilation by Thiobacillus novellus under nutrient-limited mixotrophic conditions. J Bacteriol 1982, 150:46-51.
34. Pfennig N, Lippert KD. Über das Vitamin B12-Bedürfnis phototropher Schwefelbakterien. Arch Microbiol 1966, 55:245-256.
35. Pronk JT, Meulenberg R, van den Berg DJC, Batenburg-van der Vegte W, Bos P, Kuenen JG. Mixotrophic and autotrophic growth of Thiobacillus acidophilus on glucose and thiosulfate. Appl Environ Microbiol 1990, 56:3395-3401.
36. Richter M, Kube M, Bazylinski DA, Lombardot T, Glockner FO, Reinhardt R, Schuler D. Comparative genome analysis of four magnetotactic bacteria reveals a complex set of group-specific genes implicated in magnetosome biomineralization and function. J Bacteriol 2007, 189:4899-4910.
37. Schübbe S, Kube M, Scheffel A, Waver C, Heyen U, Meyerdieks A. Characterization of a spontaneous nonmagnetic mutant of Magnetospirilum gryphiswaldense reveals a large deletion comprising a putative magnetosome island. J Bacteriol 2003, 185:5779-5790.
38. Schütz M, Maldener I, Griesbeck C, Hauska G. Sulfide-quinone reductase from Rhodobacter capsulatus: requirement for growth, periplasmic localization, and extension of gene sequence analysis. J Bacteriol 1999, 181:6516-6523.
39. Simmons SL, Sievert SM, Frankel RB, Bazylinski DA, Edwards KJ. Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Appl Environ Microbiol 2004, 70:6230-6239.
40. Sörbo B. A colorimetric method for the determination of thiosulfate. Biochim Biophys Acta 1957, 23:412-416.
41. Sorokin DY, Banciu H, van Loosdrecht MCM, Kuenen JG. Growth physiology and competitive interaction of obligately chemolithoautotrophic, haloalkaliphilic, sulfur-oxidizing bacteria from soda lakes. Extremophiles 2003, 7:195-203.
42. Spring S, Amann R, Ludwig W, Schleifer KH, Van Gemerden H, Petersen N. Dominating role of an unusual magnetotactic bacterium in the microaerobic zone of a freshwater sediment. Appl Environ Microbiol 1993, 59:2397-2403.
43. Stefess GC, Torremans RAM, Schrijver R, Robertson LA, Kuenen JG. Quantitative measurement of sulphur formation by steady state and transient state continuous cultures of autotrophic Thiobacillus species. Appl Microbiol Biotechnol 1996, 45:169-175.
44. Timmer-ten Hoor A. Cell yield and bioenergetics of Thiomicrospira denitrificans compared with Thiobacillus denitrificans. Antonie Van Leeuwenhoek 1981, 47:231-243.
45. Trüper HG, Schlegel HG. Sulfur metabolism in Thiorhodaceae. Quantitative measurements on growing cells of Chromatium okenii. Antonie Van Leeuwenhoek 1964, 30:225-238.
46. Ullrich S, Kube M, Schübbe S, Reinhardt R, Schüler D. A hypervariable 130-kilobase genomic region of Magnetospirillum gryphiswaldense comprises a magnetosome island which undergoes frequent rearrangements during stationary growth. J Bacteriol 2005, 187:7176-7184.
47. Verté F, Kostanjevecki V, De Smet L, Meyer TE, Cusanovich MA, Van Beeumen JJ. Identification of a thiosulfate utilization gene cluster from the green phototrophic bacterium Chlorobium limicola. Biochemistry 2002, 41:2932-2945.
48. Visser JM, Jong GAH, Robertson LA, Kuenen JG. A novel membrane-bound flavocytochrome c sulfide dehydrogenase from the colourless sulfur bacterium Thiobacillus sp. W5. Arch Microbiol 1997, 167:295-301.
49. Williams TJ, Zhang CL, Scott JH, Bazylinski DA. Evidence for autotrophy via the reverse tricaboxylic acid cycle in the marine magnetotactic coccus strain MC-1. Appl Environ Microbiol 2006, 72:1322-1329.
50. Wolin EA, Wolin MJ, Wolfe RS. Formation of methane by bacterial extracts. J Biol Chem 1963, 238:2882-2886.