Microbial sulfide oxidation in the oxic-anoxic transition zone of freshwater sediment: Involvement of lithoautotrophic Magnetospirillum strain J10

FEMS Microbiology Ecology

Volumn 70, Issue 1, 2009, Pages 54-65

  Geelhoed, Jeanine S ^a,b   Sorokin, Dimitry Y ^a,c   Epping, Eric ^d   Tourova, Tatjana P ^c   Banciu, Horia L ^e   Muyzer, Gerard ^a   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)

^d ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^e BABE BOLYAI UNIVERSITY   (Romania)

Author keywords

Isolation; Lithoautotrophic growth; Magnetospirillum; Oxic anoxic transition zone; Sulfur oxidation

Indexed keywords

1,5 BISPHOSPHATE CARBOXYLASE; CARBOXYLASE; IRON; OXYGEN; RNA 16S; SULFIDE; THIOSULFATE; UNCLASSIFIED DRUG;

AUTOTROPHY; BIOMASS; ENZYME ACTIVITY; FRESHWATER SEDIMENT; IRON SULFIDE; MICROBIAL ACTIVITY; MICROCOSM; OXIDATION; THIOSULFATE; TRANSITION ZONE;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATION; CONTROLLED STUDY; GENE SEQUENCE; MAGNETOSPIRILLUM; MICROCOSM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

AUTOTROPHIC PROCESSES; BIOMASS; DNA, BACTERIAL; FRESH WATER; GEOLOGIC SEDIMENTS; MAGNETOSPIRILLUM; OXIDATION-REDUCTION; OXYGEN; PHOTOSYNTHESIS; PHYLOGENY; RIBULOSE-BISPHOSPHATE CARBOXYLASE; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SULFIDES; WATER MICROBIOLOGY;

ALPHAPROTEOBACTERIA; DECHLOROSPIRILLUM; MAGNETOSPIRILLUM; MAGNETOSPIRILLUM GRYPHISWALDENSE; VIBRIO;

EID: 69949151287     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2009.00739.x     Document Type: Article

References (68)

1. Anderson RE Fuller RC (1969) Photosynthesis in Rhodospirillum rubrum. IV Isolation and characterization of ribulose 1,5-diphosphate carboxylase. J Biol Chem 244 : 3105 3109.
2. Banciu H, Sorokin DY, Kleerebezem R, Muyzer G, Galinski EA Kuenen JG (2004) Growth kinetics of haloalkaliphilic, sulfur-oxidizing bacterium Thioalkalivibrio versutus strain ALJ 15 in continuous culture. Extremophiles 8 : 185 192.
3. Bazylinski DA Blakemore RP (1983) Denitrification and assimilatory nitrate reduction in Aquaspirillum magnetotacticum. Appl Environ Microb 46 : 1118 1124.
4. Bazylinski DA Frankel RB (2004b) Magnetosome formation in prokaryotes. Nat Rev Microbiol 2 : 217 230.
5. 2-dependent growth and nitrogenase activity in the metal-metabolizing bacteria, Geobacter and Magnetospirillum species. Environ Microbiol 2 : 266 273.
6. Bazylinski DA, Dean AJ, Williams TJ, Kimble Long L, Middleton SL Dubbels BL (2004a) Chemolithoautotrophy in the marine, magnetotactic bacterial strains MV-1 and MV-2. Arch Microbiol 182 : 373 387.
7. Bender KS, Rice MR, Fugate WH, Coates JD Achenbach LA (2004) Metabolic primers for detection of (per)chlorate-reducing bacteria in the environment and phylogenetic analysis of cld gene sequences. Appl Environ Microb 70 : 5651 5658.
8. Blakemore RP, Maratea D Wolfe RS (1979) Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J Bacteriol 140 : 720 729.
9. Bradley DE (1962) A study of the negative staining process. J Gen Microbiol 29 : 503 516.
10. Broecker WS Peng TH (1974) Gas-exchange rates between air and sea. Tellus 26 : 21 35.
11. Campbell BJ Cary SC (2004) Abundance of reverse tricarboxylic acid cycle genes in free-living microorganisms at deep-sea hydrothermal vents. Appl Environ Microb 70 : 6282 6289.
12. Campbell BJ, Stein JL Cary SC (2003) Evidence of chemolithoautotrophy in the bacterial community associated with Alvinella pompejana, a hydrothermal vent polychaete. Appl Microbiol Biot 69 : 5070 5078.
13. Coates JD, Michaelidou U, Bruce RA, O'Connor SM, Crespi JN Achenbach LA (1999) Ubiquity and diversity of dissimilatory (per)chlorate-reducing bacteria. Appl Environ Microb 65 : 5234 5241.
14. Dahl C, Schulte A, Stockdreher Y, Hong C, Grimm F, Sander J, Kim R, Kim SH Shin DH (2008) Structural and molecular genetic insight into a widespread sulfur oxidation pathway. J Mol Biol 384 : 1287 1300.
15. DeLong EF, Frankel RB Bazylinski DA (1993) Multiple evolutionary origins of magnetotaxis in bacteria. Science 259 : 803 806.
16. Emerson D Moyer C (1997) Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microb 63 : 4784 4792.
17. Escalante-Semerena JC, Blakemore RP Wolfe RS (1980) Nitrate dissimilation under microaerophilic conditions by a magnetic spirillum. Appl Environ Microb 40 : 429 430.
18. Flies CB, Jonkers HM, De Beer D, Bosselmann K, Böttcher ME Schüler D (2005a) Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. FEMS Microbiol Ecol 52 : 185 195.
19. Flies CB, Peplies J Schüler D (2005b) Combined approach for characterization of uncultivated magnetotactic bacteria from various aquatic environments. Appl Environ Microb 71 : 2723 2731.
20. Frankel RB, Bazylinski DA, Johnson MS Taylor BL (1997) Magneto-aerotaxis in marine coccoid bacteria. Biophys J 73 : 994 1000.
21. Friedrich CG, Bardischewsky F, Rother D, Quentmeier A Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8 : 253 259.
22. Gottschal JC Kuenen JG (1980) Mixotrophic growth of Thiobacillus A2 on acetate and thiosulfate as growth limiting substrates in the chemostat. Arch Microbiol 126 : 33 42.
23. Guerin WF Blakemore RP (1992) Redox cycling of iron supports growth and magnetite synthesis by Aquaspirillum magnetotacticum. Appl Environ Microb 58 : 1102 1109.
24. Hernandez JM, Baker SH, Lorbach SC, Shively JM Tabita FR (1996) Deduced amino acid sequence, functional expression, and unique enzymatic properties of the form I and form II ribulose bisphosphate carboxylase/oxygenase from the chemoautotrophic bacterium Thiobacillus denitrificans. J Bacteriol 178 : 347 356.
25. Jogler C, Kube M, Schubbe S, Ullrich S, Teeling H, Bazylinski DA, Reinhardt R Schuler D (2009) Comparative analysis of magnetosome gene clusters in magnetotactic bacteria provides further evidence for horizontal gene transfer. Environ Microbiol 11 : 1267 1277.
26. Kawaguchi K, Shinoda Y, Yurimoto H, Sakai Y Kato N (2006) Purification and characterization of benzoate-CoA ligase from Magnetospirillum sp. strain TS-6 capable of aerobic and anaerobic degradation of aromatic compounds. FEMS Microbiol Lett 257 : 208 213.
27. Kelly DP (1999) Thermodynamic aspects of energy conservation by chemolithotrophic sulfur bacteria in relation to the sulfur oxidation pathways. Arch Microbiol 171 : 219 229.
28. Kopp RE Kirschvink JL (2008) The identification and biogeochemical interpretation of fossil magnetotactic bacteria. Earth-Sci Rev 86 : 42 61.
29. Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic Acid Techniques in Bacterial Systematics (Stackebrandt E Goodfellow M, eds), pp. 115 175. John Wiley & Sons, Chichester, UK.
30. Li Y Gregory S (1974) Diffusion of ions in sea water and in deep-sea sediments. Geochim Cosmochim Acta 38 : 703 714.
31. Lowry OH, Rosebrough NJ, Farr AL Randall RJ (1951) Protein measurement with the Folin-phenol reagents. J Biol Chem 193 : 265 275.
32. Maratea D Blakemore RP (1981) Aquaspirillum magnetotacticum sp. nov., a magnetic spirillum. Int J Syst Bacteriol 31 : 452 455.
33. Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microb 64 : 795 799. (Pubitemid 28079862)
34. Matsunaga T, Sakaguchi T Tadokoro F (1991) Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl Microbiol Biot 35 : 651 655.
35. Matsunaga T, Okamura Y, Fukumori Y, Wahyudi AT, Murase Y Takeyama H (2005) Complete genome sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp. strain AMB-1. DNA Res 12 : 157 166.
36. 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.
37. Muyzer G, de Waal EC Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microb 59 : 695 700.
38. Nelson DC, Jørgensen BB Revsbech NP (1986) Growth pattern and yield of a chemoautotrophic Beggiatoa sp. in oxygen-sulfide microgradients. Appl Environ Microb 52 : 225 233.
39. Ogawa T, Furusawa T, Nomura R, Seo D, Hosoya-Matsuda N, Sakurai H Inoue K (2008) SoxAX binding protein, a novel component of the thiosulfate-oxidizing multienzyme system in the green sulfur bacterium Chlorobium tepidum. J Bacteriol 190 : 6097 6110.
40. Pfennig N Lippert KD (1966) Über das Vitamin B12-bedürfnis phototropher Schwefel bacterien. Arch Microbiol 55 : 245 256.
41. Pringault O, Kuhl M, de Wit R Caumette P (1998) Growth of green sulphur bacteria in experimental benthic oxygen, sulphide, pH and light gradients. Microbiol-UK 144 : 1051 1061.
42. Pringault O, Epping E, Guyoneaud R, Khalili A Kuhl M (1999) Dynamics of anoxygenic photosynthesis in an experimental green sulphur bacteria biofilm. Environ Microbiol 1 : 295 305.
43. Richter M, Kube M, Bazylinski DA, Lombardot T, Glockner FO, Reinhardt R Schuler D (2007) Comparative genome analysis of four magnetotactic bacteria reveals a complex set of group-specific genes implicated in magnetosome biomineralization and function. J Bacteriol 189 : 4899 4910.
44. Sakaguchi T, Arakaki A Matsunaga T (2002) Desulfovibrio magneticus sp. nov., a novel sulfate-reducing bacterium that produces intracellular single-domain-sized magnetite particles. Int J Syst Evol Micr 52 : 215 221.
45. Schleifer KH, Schüler D, Spring S, Weizenegger M, Amann R, Ludwig W Köhler M (1991) The genus Magnetospirillum gen. nov. Description of Magnetospirillum gryphiswaldense sp. nov. and transfer of Aquaspirillum magnetotacticum to Magnetospirillum magnetotacticum comb. nov. Syst Appl Microbiol 14 : 379 385.
46. Schübbe S, Kube M, Scheffel A, Waver C, Heyen U, Meyerdieks A, Madkour M, Mayer F, Reinhardt R Schüler D (2003) Characterization of a spontaneous nonmagnetic mutant of Magnetospirilum gryphiswaldense reveals a large deletion comprising a putative magnetosome island. J Bacteriol 185 : 5779 5790.
47. Schüler D (2008) Genetics and cell biology of magnetosome formation in magnetotactic bacteria. FEMS Microbiol Rev 32 : 654 672.
48. Schüler D, Spring S Bazylinski DA (1999) Improved technique for the isolation of magnetotactic spirilla from a freshwater sediment and their phylogenetic characterization. Syst Appl Microbiol 22 : 466 471.
49. Shinoda Y, Sakai Y, Ue M, Hiraishi A Kato N (2000) Isolation and characterization of a new denitrifying spirillum capable of anaerobic degradation of phenol. Appl Environ Microb 66 : 1286 1291.
50. Shinoda Y, Akagi J, Uchihashi Y, Hiraishi A, Yukawa H, Yurimoto H, Sakai Y Kato N (2005) Anaerobic degradation of aromatic compounds by Magnetospirillum strains: isolation and degradation genes. Biosci Biotech Bioch 69 : 1483 1491.
51. Simmons SL, Sievert SM, Frankel RB, Bazylinski DA Edwards KJ (2004) Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Appl Environ Microb 70 : 6230 6239.
52. Simmons SL, Bazylinski DA Edwards KJ (2007) Population dynamics of marine magnetotactic bacteria in a meromictic salt pond described with qPCR. Environ Microbiol 9 : 2162 2174.
53. Sörbo B (1957) A colorimetric method for the determination of thiosulfate. Biochim Biophys Acta 23 : 412 416.
54. Spiridonova EM, Berg IA, Kolganova TV, Ivanovsky RN, Kuznetsov BB Tourova TP (2004) An oligonucleotide primer system for amplification of the ribulose-1,5-bisphosphate carboxylase/oxygenase genes of bacteria of various taxonomic groups. Microbiology 73 : 316 325.
55. Spring S, Amann R, Ludwig W, Schleifer KH Petersen N (1992) Phylogenetic diversity and identification of nonculturable magnetotactic bacteria. Syst Appl Microbiol 15 : 116 122.
56. Spring S, Amann R, Ludwig W, Schleifer KH, Van Gemerden H Petersen N (1993) Dominating role of an unusual magnetotactic bacterium in the microaerobic zone of a freshwater sediment. Appl Environ Microb 59 : 2397 2403.
57. Stackebrandt E Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today Nov : 152 155.
58. Stefess GC, Torremans RAM, deSchrijver R, Robertson LA Kuenen JG (1996) Quantitative measurement of sulphur formation by steady state and transient state continuous cultures of autotrophic Thiobacillus species. Appl Microbiol Biot 45 : 169 175.
59. Tabita FR (1999) Microbial ribulose 1,5-bisphosphate carboxylase/ oxygenase: a different perspective. Photosynth Res 60 : 1 28.
60. Takai K, Campbell BJ, Cary SC et al 2005) Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsiloproteobacteria. Appl Environ Microb 71 : 7310 7320.
61. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24 : 4876 4882.
62. Timmer-ten Hoor A (1981) Cell yield and bioenergetics of Thiomicrospira denitrificans compared with Thiobacillus denitrificans. A van Leeuw J Microb 47 : 231 243.
63. Ullrich S, Kube M, Schübbe S, Reinhardt R Schüler D (2005) A hypervariable 130-kilobase genomic region of Magnetospirillum gryphiswaldense comprises a magnetosome island which undergoes frequent rearrangements during stationary growth. J Bacteriol 187 : 7176 7184.
64. Wagner SJ, Stevens SEJ, Nixon BT, Lambert DH, Quivey RG Tabita FR (1988) Nucleotide and deduced amino acid sequence of the Rhodobacter sphaeroides gene encoding form II ribulose-1,5-bisphosphate carboxylase/oxygenase and comparison with other deduced form I and II sequences. FEMS Microbiol Lett 55 : 217 222.
65. Williams TJ, Zhang CL, Scott JH Bazylinski DA (2006) Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1. Appl Environ Microb 72 : 1322 1329.
66. Wolin EA, Wolin MJ Wolfe RS (1963) Formation of methane by bacterial extracts. J Biol Chem 238 : 2882 2886.
67. Yao WS Millero FJ (1996) Oxidation of hydrogen sulfide by hydrous Fe(III) oxides in seawater. Mar Chem 52 : 1 16.
68. Zhang JZ Millero FJ (1994) Kinetics of oxidation of hydrogen sulfide in natural waters. Environmental Geochemistry of Sulfide Oxidation, ACS Symposium Series 550 (Alpers CN Blowes DW, eds), pp. 393 409. American Chemical Society, Washington, DC.