Photosynthesis Research

, Volume 97, Issue 3, pp 235–244 | Cite as

Vertical distribution and characterization of aerobic phototrophic bacteria at the Juan de Fuca Ridge in the Pacific Ocean

  • Christopher Rathgeber
  • Michael T. Lince
  • Jean Alric
  • Andrew S. Lang
  • Elaine Humphrey
  • Robert E. Blankenship
  • André Verméglio
  • F. Gerald Plumley
  • Cindy L. Van Dover
  • J. Thomas Beatty
  • Vladimir Yurkov
Regular Paper

Abstract

The vertical distribution of culturable anoxygenic phototrophic bacteria was investigated at five sites at or near the Juan de Fuca Ridge in the Pacific Ocean. Twelve similar strains of obligately aerobic phototrophic bacteria were isolated in pure culture, from depths ranging from 500 to 2,379 m below the surface. These strains appear morphologically, physiologically, biochemically, and phylogenetically similar to Citromicrobium bathyomarinum strain JF-1, a bacterium previously isolated from hydrothermal vent plume waters. Only one aerobic phototrophic strain was isolated from surface waters. This strain is morphologically and physiologically distinct from the strains isolated at deeper sampling locations, and phylogenetic analysis indicates that it is most closely related to the genus Erythrobacter. Phototrophs were cultivated from three water casts taken above vents but not from two casts taken away from active vent sites. No culturable anaerobic anoxygenic phototrophs were detected. The photosynthetic apparatus was investigated in strain JF-1 and contains light-harvesting I and reaction center complexes, which are functional under aerobic conditions.

Keywords

Aerobic phototrophic bacteria Anoxygenic photosynthesis Bacteriochlorophyll Erythrobacter Citromicrobium Juan de Fuca Ridge 

References

  1. Alric J (2005) In vivo carotenoid triplet formation in response to excess light: supramolecular photoprotection mechanism revisited. Photosynth Res 83:335–341. doi:10.1007/s11120-005-1105-3 PubMedCrossRefGoogle Scholar
  2. Beatty JT (2002) On the natural selection and evolution of the aerobic phototrophic bacteria. Photosynth Res 73:109–114. doi:10.1023/A:1020493518379 PubMedCrossRefGoogle Scholar
  3. Beatty JT, Overmann J, Lince MT, Manske AK, Lang AS, Blankenship RE et al (2005) An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. Proc Natl Acad Sci USA 102:9306–9310. doi:10.1073/pnas.0503674102 PubMedCrossRefGoogle Scholar
  4. Delaney JR, Robigou V, McDuff RE, Tivey MK (1992) Geology of a vigorous hydrothermal system on the Endeavour Segment, Juan de Fuca Ridge. J Geophys Res 97:19663–19682. doi:10.1029/92JB00174 CrossRefGoogle Scholar
  5. Drews G (1983) Mikrobiologishes praktikum. Springer, BerlinGoogle Scholar
  6. Gerloff GC, Fitzgerald GP, Skoog F (1950) The isolation, purification, and culture of blue-green algae. Am J Bot 37:216–218. doi:10.2307/2437904 CrossRefGoogle Scholar
  7. Goericke R (2002) Bacteriochlorophyll a in the ocean: is anoxygenic bacterial photosynthesis important? Limnol Oceanogr 47:290–295Google Scholar
  8. Holmstrom C, Kjelleberg S (1999) Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol Ecol 30:285–293PubMedGoogle Scholar
  9. Kellenberger E, Ryter A, Sechaud J (1958) Electron microscope study of DNA-containing plasms. J Biophys Biochem Cytol 4:671–678PubMedGoogle Scholar
  10. Koblizek M, Beja O, Bidigare RR, Christensen S, Benitez-Nelson B, Vetriani C et al (2003) Isolation and characterization of Erythrobacter sp. strains from the upper ocean. Arch Microbiol 180:327–338. doi:10.1007/s00203-003-0596-6 PubMedCrossRefGoogle Scholar
  11. Kolber ZS, Van Dover CL, Niederman RA, Falkowski PG (2000) Bacterial photosynthesis in surface waters of the open ocean. Nature 407:177–179. doi:10.1038/35025044 PubMedCrossRefGoogle Scholar
  12. Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, Van Dover CL et al (2001) Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292:2492–2495. doi:10.1126/science.1059707 PubMedCrossRefGoogle Scholar
  13. Nisbet EG, Cann JR, Van Dover CL (1995) Origins of photosynthesis. Nature 373:479–480. doi:10.1038/373479a0 CrossRefGoogle Scholar
  14. Oz A, Sabehi G, Koblizek M, Massana R, Beja O (2005) Roseobacter-like bacteria in Red and Mediterranean Sea aerobic anoxygenic photosynthetic populations. Appl Environ Microbiol 71:344–353. doi:10.1128/AEM.71.1.344-353.2005 PubMedCrossRefGoogle Scholar
  15. Pfennig N (1978a) General physiology and ecology of photosynthetic bacteria. In: Clayton R, Sistrom W (eds) The photosynthetic bacteria. Plenum Press, NY, pp 3–18Google Scholar
  16. Pfennig N (1978b) Rhodocyclus purpureus gen. nov. and sp. nov., a ring-shaped vitamin B12-requiring member of the family Rhodospirillaceae. Int J Syst Bacteriol 28:283–288Google Scholar
  17. Rainey FA, Ward-Rainey N, Kroppenstedt RM, Stackebrandt E (1996) The genus Nocardiopsis represents a phylogenetically coherent taxon and a distinct actinomycete lineage: proposal of Nocardiopsaceae fam. nov. Int J Syst Bacteriol 46:1088–1092PubMedGoogle Scholar
  18. Rathgeber C, Beatty JT, Yurkov V (2004) Aerobic phototrophic bacteria: new evidence for the diversity, ecological importance and applied potential of this previously overlooked group. Photosynth Res 81:113–128. doi:10.1023/B:PRES.0000035036.49977.bc CrossRefGoogle Scholar
  19. Rathgeber C, Yurkova N, Stackebrandt E, Schumann P, Beatty JT, Yurkov V (2005) Roseicyclus mahoneyensis gen. nov., sp. nov., an aerobic phototrophic bacterium isolated from a meromictic lake. Int J Syst Evol Microbiol 55:1597–1603. doi:10.1099/ijs.0.63195-0 PubMedCrossRefGoogle Scholar
  20. Schwalbach MS, Fuhrman JA (2005) Wide-ranging abundances of aerobic anoxygenic phototrophic bacteria in the world ocean revealed by epifluorescence microscopy and quantitative PCR. Limnol Oceanogr 50:620–628Google Scholar
  21. Shiba T, Simidu U (1982) Erythrobacter longus gen. nov., sp. nov., an aerobic bacterium which contains bacteriochlorophyll a. Int J Syst Bacteriol 32:211–217Google Scholar
  22. Shiba T, Simidu U, Taga N (1979) Distribution of aerobic bacteria which contain bacteriochlorophyll a. Appl Environ Microbiol 38:43–45PubMedGoogle Scholar
  23. Shopes RJ, Holten D, Levine LMA, Wright CA (1987) Kinetics of oxidation of the bound cytochromes in reaction centers from Rhodopseudomonas viridis. Photosynth Res 12:165–180. doi:10.1007/BF00047946 CrossRefGoogle Scholar
  24. Van Dover CL, Reynolds GT, Chave AD, Tyson JA (1996) Light at deep-sea hydrothermal vents. Geophys Res Lett 23:2049–2052. doi:10.1029/96GL02151 CrossRefGoogle Scholar
  25. Yurkov V, Beatty JT (1998a) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62:695–724PubMedGoogle Scholar
  26. Yurkov V, Beatty JT (1998b) Isolation of aerobic anoxygenic photosynthetic bacteria from black smoker plume waters of the Juan de Fuca Ridge in the Pacific Ocean. Appl Environ Microbiol 64:337–341PubMedGoogle Scholar
  27. Yurkov VV, Csotonyi JT (2003) Aerobic anoxygenic phototrophs and heavy metalloid reducers from extreme environments. In: Pandalai SG (ed) Recent research developments in bacteriology. Transworld Research Network, Trivandrum, pp 247–300Google Scholar
  28. Yurkov V, Van Gemerden H (1993a) Abundance and salt tolerance of obligately aerobic, phototrophic bacteria in a microbial mat. Neth J Sea Res 31:57–62. doi:10.1016/0077-7579(93)90017-M CrossRefGoogle Scholar
  29. Yurkov V, Van Gemerden H (1993b) Impact of light/dark regime on growth rate, biomass formation and bacteriochlorophyll synthesis in Erythromicrobium hydrolyticum. Arch Microbiol 159:84–89. doi:10.1007/BF00244268 CrossRefGoogle Scholar
  30. Yurkov V, Gad’on N, Drews G (1993) The major part of polar carotenoids of the aerobic bacteria Roseococcus thiosulfatophilus, RB3 and Erythromicrobium ramosusm, E5 is not bound to the bacteriochlorophyll a complexes of the photosynthetic apparatus. Arch Microbiol 160:372–376. doi:10.1007/BF00252223 CrossRefGoogle Scholar
  31. Yurkov V, Gad’on N, Angerhofer A, Drews G (1994a) Light-harvesting complexes of aerobic bacteriochlorophyll-containing bacteria Roseococcus thiosulfatophilus, RB3 and Erythromicrobium ramosum, E5 and the transfer of excitation energy from carotenoids to bacteriochlorophyll. Z Naturforsch Teil C 49:579–586Google Scholar
  32. Yurkov V, Stackebrandt E, Holmes A, Fuerst JA, Hugenholtz P, Golecki J et al (1994b) Phylogenetic positions of novel aerobic, bacteriochlorophyll a-containing bacteria and description of Roseococcus thiosulfatophilus gen. nov., sp. nov., Erythromicrobium ramosum gen. nov., sp. nov., and Erythrobacter litoralis sp. nov. Int J Syst Bacteriol 44:427–434PubMedCrossRefGoogle Scholar
  33. Yurkov V, Menin L, Schoepp B, Verméglio A (1998a) Purification and characterization of reaction centers from the obligate aerobic phototrophic bacteria Erythrobacter litoralis, Erythromonas ursincola and Sandaracinobacter sibiricus. Photosynth Res 57:129–138. doi:10.1023/A:1006087403692 CrossRefGoogle Scholar
  34. Yurkov V, Schoepp B, Verméglio A (1998b) Photoinduced electron transfer and cytochrome content in obligate aerobic phototrophic bacteria from genera Erythromicrobium, Sandaracinobacter, Erythromonas, Roseococcus and Erythrobacter. Photosynth Res 57:117–128. doi:10.1023/A:1006097120530 CrossRefGoogle Scholar
  35. Yurkov V, Krieger S, Stackebrandt E, Beatty JT (1999) Citromicrobium bathyomarinum, a novel aerobic bacterium isolated from deep-sea hydrothermal vent plume waters that contains photosynthetic pigment-protein complexes. J Bacteriol 181:4517–4525PubMedGoogle Scholar
  36. Yurkova N, Rathgeber C, Swiderski J, Stackebrandt E, Beatty JT, Hall KJ et al (2002) Diversity, distribution and physiology of the aerobic phototrophic bacteria in the mixolimnion of a meromictic lake. FEMS Microbiol Ecol 40:191–220. doi:10.1111/j.1574-6941.2002.tb00952.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Christopher Rathgeber
    • 1
  • Michael T. Lince
    • 2
  • Jean Alric
    • 3
  • Andrew S. Lang
    • 4
  • Elaine Humphrey
    • 5
  • Robert E. Blankenship
    • 2
  • André Verméglio
    • 6
  • F. Gerald Plumley
    • 7
  • Cindy L. Van Dover
    • 8
  • J. Thomas Beatty
    • 4
  • Vladimir Yurkov
    • 1
  1. 1.Department of MicrobiologyThe University of ManitobaWinnipegCanada
  2. 2.Department of Chemistry and BiochemistryArizona State UniversityTempeUSA
  3. 3.Institut de Biologie Physico-ChimiqueParisFrance
  4. 4.Department of Microbiology and ImmunologyUniversity of British ColumbiaVancouverCanada
  5. 5.Bio-Imaging FacilityThe University of British ColumbiaVancouverCanada
  6. 6.CEA-Cadarache, DSV/IBEB/SBVME/LBCUMR 6191 CNRS/CEA/Université Aix-MarseilleSaint-Paul-lez-DuranceFrance
  7. 7.Bermuda Institute of Ocean SciencesSt George’sBermuda
  8. 8.Biology DepartmentCollege of William and MaryWilliamsburgUSA

Personalised recommendations