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Chemolithoautotrophy in the marine, magnetotactic bacterial strains MV-1 and MV-2

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Abstract

Magnetite-producing magnetotactic bacteria collected from the oxic–anoxic transition zone of chemically stratified marine environments characterized by O2/H2S inverse double gradients, contained internal S-rich inclusions resembling elemental S globules, suggesting they oxidize reduced S compounds that could support autotrophy. Two strains of marine magnetotactic bacteria, MV-1 and MV-2, isolated from such sites grew in O2-gradient media with H2S or thiosulfate (S2O32−) as electron sources and O2 as electron acceptor or anaerobically with S2O32− and N2O as electron acceptor, with bicarbonate (HCO3−)/CO2 as sole C source. Cells grown with H2S contained S-rich inclusions. Cells oxidized S2O32− to sulfate (SO42−). Both strains grew microaerobically with formate. Neither grew microaerobically with tetrathionate (S4O62−), methanol, or Fe2+ as FeS, or siderite (FeCO3). Growth with S2O32− and radiolabeled 14C-HCO3− showed that cell C was derived from HCO3−/CO2. Cell-free extracts showed ribulose 1,5-bisphosphate carboxylase/oxygenase (RubisCO) activity. Southern blot analyses indicated the presence of a form II RubisCO (cbbM) but no form I (cbbL) in both strains. cbbM and cbbQ, a putative post-translational activator of RubisCO, were identified in MV-1. MV-1 and MV-2 are thus chemolithoautotrophs that use the Calvin–Benson–Bassham pathway. cbbM was also identified in Magnetospirillum magnetotacticum. Thus, magnetotactic bacteria at the oxic–anoxic transition zone of chemically stratified aquatic environments are important in C cycling and primary productivity.

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References

  • American Type Culture Collection (1989) Catalogue of bacteria and bacteriophages, 17th edn. American Type Culture Collection, Rockville

    Google Scholar 

  • Baker SH, Jin S, Aldrich HC, Howard GT, Shively JM (1998) Insertion mutation of the form I cbbL gene encoding ribulose bisphosphate carboxylase/oxygenase (RuBisCO) in Thiobacillus neapolitanus results in expression of form II RuBisCO, loss of carboxysomes, and an increased CO2 requirement for growth. J Bacteriol 180:4133–4139

    CAS  PubMed  Google Scholar 

  • Bazylinski DA, Blakemore RP (1983) Denitrification and assimilatory nitrate reduction in Aquaspirillum magnetotacticum. Appl Environ Microbiol 46:1118–1124

    CAS  Google Scholar 

  • Bazylinski DA, Frankel RB (2000) Biologically controlled mineralization of magnetic iron minerals by magnetotactic bacteria. In: Lovley DR (ed) Environmental microbe–metal interactions. ASM, Washington, D.C., pp 109–144

    Google Scholar 

  • Bazylinski DA, Frankel RB (2004) Magnetosome formation in prokaryotes. Nat Rev Microbiol 2:217–230

    Article  CAS  PubMed  Google Scholar 

  • Bazylinski DA, Frankel RB, Jannasch HW (1988) Anaerobic magnetite production by a marine magnetotactic bacterium. Nature 334:518–519

    Article  Google Scholar 

  • Bazylinski DA, Garratt-Reed AJ, Abedi A, Frankel RB (1993a) Copper association with iron sulfide magnetosomes in a magnetotactic bacterium. Arch Microbiol 160:35–42

    CAS  Google Scholar 

  • Bazylinski DA, Garratt-Reed AJ, Frankel RB (1993b) Electron microscopic studies of magnetosomes in magnetotactic bacteria. Microsc Res Tech 27:389–401

    Google Scholar 

  • Bazylinski DA, Frankel RB, Heywood BR, Mann S, King JW, Donaghay PL, Hanson AK (1995) Controlled biomineralization of magnetite (Fe3O4) and greigite (Fe3S4) in a magnetotactic bacterium. Appl Environ Microbiol 61:3232–3239

    CAS  Google Scholar 

  • Bazylinski DA, Dean AJ, Schüler D, Phillips EJP, Lovley DR (2000) N2-dependent growth and nitrogenase activity in the metal-metabolizing bacteria, Geobacter and Magnetospirillum species. Environ Microbiol 2:266–273

    Article  CAS  PubMed  Google Scholar 

  • Beudeker RF, Cannon GC, Kuenen JG, Shively JM (1980) Relations between d-ribulose-1,5-bisphosphate carboxylase, carboxysomes and CO2 fixing capacity in the obligate chemolithotroph Thiobacillus neapolitanus grown under different limitations in the chemostat. Arch Microbiol 124:185–189

    CAS  Google Scholar 

  • Blakemore RP (1982) Magnetotactic bacteria. Annu Rev Microbiol 36:217–238

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cox RB, Quayle JR (1975) The autotrophic growth of Micrococcus denitrificans on methanol. Biochem J 150:569–571

    CAS  PubMed  Google Scholar 

  • Cox BL, Popa R, Bazylinski DA, Lanoil B, Douglas S, Belz A, Engler DL, Nealson KH (2002) Organization and elemental analysis of P-, S-, and Fe-inclusions in a population of freshwater magnetococci. Geomicrobiol J 19:387–406

    Article  CAS  Google Scholar 

  • Dean AJ, Bazylinski DA (1999) Genome analysis of several marine, magnetotactic bacterial strains by pulsed-field gel electrophoresis. Curr Microbiol 39:219–225

    Article  CAS  PubMed  Google Scholar 

  • DeLong EF, Frankel RB, Bazylinski DA (1993) Multiple evolutionary origins of magnetotaxis in bacteria. Science 259:803–806

    Google Scholar 

  • Doolittle RF (1981) Similar amino acid sequences: chance or common ancestry? Science 214:149–159

    CAS  PubMed  Google Scholar 

  • Emerson D, Moyer C (1997) Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microbiol 63:4784–4792

    CAS  PubMed  Google Scholar 

  • English RS, Williams CA, Lorbach SC, Shively JM (1992) Two forms of ribulose-1,5-bisphosphate carboxylase/oxygenase from Thiobacillus denitrificans. FEMS Microbiol Lett 94:111–119

    Article  CAS  Google Scholar 

  • Falcone DL, Tabita FR (1993) Complementation analysis and regulation of CO2 fixation gene expression in a ribulose-1,5-bisphosphate carboxylase/oxygenase deletion strain of Rhodospirillum rubrum. J Bacteriol 175:5066–5077

    CAS  PubMed  Google Scholar 

  • Frankel RB, Blakemore RP, Wolfe RS (1979) Magnetite in freshwater magnetotactic bacteria. Science 203:1355–1356

    CAS  Google Scholar 

  • Frankel RB, Bazylinski DA, Johnson MS, Taylor BL (1997) Magneto-aerotaxis in marine coccoid bacteria. Biophys J 73:994–1000

    CAS  PubMed  Google Scholar 

  • Gibson JL, Falcone DL, Tabita FR (1991) Nucleotide sequence, transcriptional analysis, and expression of genes encoded within the form I CO2 fixation operon of Rhodobacter sphaeroides. J Biol Chem 266:14646–14653

    CAS  PubMed  Google Scholar 

  • Guerin WF, Blakemore RP (1992) Redox cycling of iron supports growth and magnetite synthesis by Aquaspirillum magnetotacticum. Appl Environ Microbiol 58:1102–1109

    CAS  Google Scholar 

  • Hayashi NR, Arai H, Kodama T, Igarashi Y (1997) The novel genes, cbbQ and cbbO, located downstream from the RubisCO genes of Pseudomonas hydrogenothermophila, affect the conformational states and activity of RubisCO. Biochem Biophys Res Commun 241:565–569

    Article  CAS  PubMed  Google Scholar 

  • Hayashi NR, Arai H, Kodama T, Igarashi Y (1998) The nirQ gene, which is required for denitrification of Pseudomonas aeruginosa, can activate the RubisCO from Pseudomonas hydrogenothermophila. Biochim Biophys Acta 1381:347–350

    Article  CAS  PubMed  Google Scholar 

  • Hayashi NR, Arai H, Kodama T, Igarashi Y (1999) The cbbQ genes, located downstream of the form I and form II RubisCO genes, affect the activity of both RubisCOs. Biochem Biophys Res Commun 265:177–183

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Iida A, Akai J (1996) Crystalline sulfur inclusions in magnetotactic bacteria. Sci Rep Niigata Univ, Ser E 11:35–42

    Google Scholar 

  • Jordan DB, Ogren WL (1981) Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature 291:513–515

    CAS  Google Scholar 

  • Jukes TH, Holmquist R, Moise H (1975) Amino acid composition of proteins: selection against the genetic code. Science 189:50–51

    CAS  PubMed  Google Scholar 

  • Kimble LK, Mandelco L, Woese CR, Madigan MT (1995) Heliobacterium modesticaldum, sp. nov., a thermophilic heliobacterium of hot springs and volcanic soils. Arch Microbiol 163:259–267

    Article  CAS  Google Scholar 

  • Kimble LK, Bazylinski DA (1996) Sequence of form I RubisCO gene (cbbL) from Anacystis nidulans, Chromatium vinosum, and Rhodobacter sphaeroides. Abstr Gen Meet Am Soc Microbiol 96:K-174

    Google Scholar 

  • Mann S, Sparks NHC, Frankel RB, Bazylinski DA, Jannasch HW (1990) Biomineralization of ferrimagnetic greigite (Fe3S4) and iron pyrite (FeS2) in a magnetotactic bacterium. Nature 343:258–260

    Article  CAS  Google Scholar 

  • Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3:208–218

    CAS  Google Scholar 

  • Moench TT (1988) Bilophococcus magnetotacticus gen. nov. sp. nov., a motile, magnetic coccus. Antonie van Leeuwenhoek 54:483–496

    CAS  PubMed  Google Scholar 

  • Moench TT, Konetzka WA (1978) A novel method for the isolation and the study of a magnetotactic bacterium. Arch Microbiol 119:203–212

    CAS  PubMed  Google Scholar 

  • Nargang F, McIntosh L, Somerville CR (1984) Nucleotide sequence of the ribulosebisphosphate carboxylase gene from Rhodospirillum rubrum. Mol Gen Genet 193:220–224

    CAS  Google Scholar 

  • Nelson DC, Jannasch HW (1983) Chemoautotrophic growth of a marine Beggiatoa in sulfide-gradient cultures. Arch Microbiol 136:262–269

    CAS  Google Scholar 

  • Noguchi Y, Fujiwara T, Yoshimatsu K, Fukumori Y (1999) Iron reductase for magnetite synthesis in the magnetotactic bacterium Magnetospirillum magnetotacticum. J Bacteriol 181:2142–2147

    CAS  PubMed  Google Scholar 

  • Paoli GC, Soyer F, Shively JM, Tabita FR (1998a) Rhodobacter capsulatus genes encoding form I ribulose-1,5-bisphosphate carboxylase/oxygenase (cbbLS) and neighboring genes were acquired by a horizontal gene transfer. Microbiology 144:219–227

    CAS  PubMed  Google Scholar 

  • Paoli GC, Vichivanives P, Tabita FR (1998b) Physiological control and regulation of the Rhodobacter capsulatus cbb operons. J Bacteriol 180:4258–4269

    CAS  PubMed  Google Scholar 

  • Pichard SL, Campbell L, Paul JH (1997) Diversity of the ribulose bisphosphate carboxylase/oxygenase form I gene (rbcL) in natural phytoplankton communities. Appl Environ Microbiol 63:3600–3606

    CAS  PubMed  Google Scholar 

  • Robinson JJ, Stein JL, Cavanaugh CC (1998) Cloning and sequencing of a form II ribulose-1,5-bisphosphate carboxylase/oxygenase from the bacterial symbiont of the hydrothermal vent tubeworm Riftia pachyptila. J Bacteriol 180:1596–1599

    CAS  PubMed  Google Scholar 

  • Rodgers FG, Blakemore RP, Blakemore NA, Frankel RB, Bazylinski DA, Maratea D, Rodgers C (1990) Intercellular structure in a many-celled magnetotactic prokaryote. Arch Microbiol 154:18–22

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor,N.Y.

    Google Scholar 

  • Schleifer K-H, Schüler D, Spring S, Weizenegger M, Amann R, Ludwig W, Kohler 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

    Google Scholar 

  • Shinozaki K, Sugiura M (1983) The gene for the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is located close to the large subunit in the cyanobacterium Anacystis nidulans 6301. Nucleic Acids Res 11:6957–6964

    CAS  PubMed  Google Scholar 

  • Shively JM, Saluja A, McFadden BA (1978) Ribulose-bisphophate carboxylase from methanol-grown Paracoccus denitrificans. J Bacteriol 134:1123–1132

    CAS  PubMed  Google Scholar 

  • Somerville CR, Somerville SC (1984) Cloning and expression of the Rhodospirillum rubrum ribulose-bisphosphate carboxylase gene in E. coli. Mol Gen Genet 193:214–219

    CAS  Google Scholar 

  • Spring S, Amann R, Ludwig W, Schleifer K-H, Gemerden H van, Petersen N (1993) Dominating role of an unusual magnetotactic bacterium in the microaerobic zone of a freshwater sediment. Appl Environ Microbiol 59:2397–2403

    CAS  Google Scholar 

  • Tabatabai MA (1974) A rapid method for determination of sulfate in water samples. Environ Lett 7:237–243

    CAS  Google Scholar 

  • Tabita (1995) The biochemistry and metabolic regulation of carbon metabolism and CO2 fixation in purple bacteria. In: Blankenship RE, Madigan MT, Bauer C (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 885–914

    Google Scholar 

  • Tayeh MA, Madigan MT (1987) Malate dehydrogenase in phototrophic purple bacteria: purification, molecular weight, and quaternary structure. J Bacteriol 169:4196–4202

    CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  PubMed  Google Scholar 

  • Viale AM, Kobayashi H, Akazawa T (1989) Expressed genes for plant-type ribulose 1,5-bisphosphate carboxylase/oxygenase in the photosynthetic bacterium Chromatium vinosum, which possesses two complete sets of genes. J Bacteriol 171:2391–2400

    CAS  PubMed  Google Scholar 

  • Wakeham SG, Howes BL, Dacey JWH, Schwarzenbach RP, Zeyer J (1987) Biogeochemistry of dimethylsulfide in a seasonally stratified coastal salt pond. Geochim Cosmochim Acta 51:1675–1684

    Article  CAS  Google Scholar 

  • Xu HH, Tabita FR (1996) Ribulose-1,5-bisphosphate carboxylase/oxygenase gene expression and diversity of Lake Erie planktonic microorganisms. Appl Environ Microbiol 62:1913–1921

    CAS  PubMed  Google Scholar 

  • Yamazaki T, Oyanagi H, Fujiwara T, Fukumori Y (1995) Nitrite reductase from the magnetotactic bacterium Magnetospirillum magnetotacticum. A novel cytochrome cd1 with Fe(II):nitrite oxidoreductase activity. Eur J Biochem 233:665–671

    CAS  PubMed  Google Scholar 

  • Yokoyama K, Hayashi NR, Arai H, Chung SY, Igarashi Y, Kodama T (1995) Genes encoding RubisCO in Pseudomonas hydrogenothermophila are followed by a novel cbbQ gene similar to nirQ of the denitrification gene cluster from Pseudomonas species. Gene 153:75–79

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank C.E. Bradburne, J.M. Shively, F.R. Tabita, and T. Wahlund for gene probes from various microorganisms, M.T. Madigan for cultures of photosynthetic bacteria, D. Emerson for advice on culturing iron-oxidizing bacteria, S.J. Molyneaux and C.O. Wirsen for suggestions and help with various chemical and enzyme assays, and B.L. Cox, K.J. Edwards, R.B. Frankel and S.L. Simmons for helpful discussions and suggestions. This work was supported by United States NSF grants MCB 9696027, CHE-9714101, and EAR-0311950, and by NASA Johnson Space Center grant NAG 9-1115.

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  1. Annette J. Dean

    Present address: Pioneer Hy-Bred International, Inc., 7300 NW 62nd Avenue, Johnston, IA 50131, USA

  2. Linda Kimble Long

    Present address: , 843 Pinehurst Lane, Schaumburg, IL 60193, USA

  3. Shawna L. Middleton

    Present address: Mycogen Seeds, 208 Leo Street, Marshalltown, IA 50158, USA

  4. Bradley L. Dubbels

    Present address: Laboratory for Nitrogen Fixation Research, Department of Botany and Plant Pathology, Oregon State University, Cordley Hall 2082, Corvallis, OR 97331-2902, USA

Authors and Affiliations

  1. Department of Biochemistry, Biophysics, and Molecular Biology, Iowa State University, Ames, IA 50011, USA

    Dennis A. Bazylinski & Timothy J. Williams

  2. Graduate Program in Microbiology, Iowa State University, Ames, IA 50011, USA

    Annette J. Dean, Linda Kimble Long, Shawna L. Middleton & Bradley L. Dubbels

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  1. Dennis A. Bazylinski
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Bazylinski, D.A., Dean, A.J., Williams, T.J. et al. Chemolithoautotrophy in the marine, magnetotactic bacterial strains MV-1 and MV-2. Arch Microbiol 182, 373–387 (2004). https://doi.org/10.1007/s00203-004-0716-y

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