Archives of Microbiology

, Volume 180, Issue 5, pp 327–338 | Cite as

Isolation and characterization of Erythrobacter sp. strains from the upper ocean

  • Michal Koblížek
  • Oded Béjà
  • Robert R. Bidigare
  • Stephanie Christensen
  • Bryan Benitez-Nelson
  • Costantino Vetriani
  • Marcin K. Kolber
  • Paul G. Falkowski
  • Zbigniew S. Kolber
Original Paper


Seven strains of marine aerobic anoxygenic phototrophs belonging to the genus Erythrobacter were isolated. The strains were characterized regarding their physiological and biochemical properties, 16S rDNA and pufM gene sequences, morphological features, substrate preference, as well as pigment and lipid composition. All strains had functional type-2 reaction centers containing bacteriochlorophyll, served by small, light-harvesting complex 1, and were photosynthetically competent. In addition, large pools of carotenoids were found, but only some of the accessory pigments transfer energy to the reaction centers. All of the isolates were facultative photoheterotrophs. They required an organic carbon substrate for growth; however, they are able to supplement a significant fraction of their metabolic requirements with photosynthetically derived energy.


Aerobic anoxygenic phototrophs Aerobic photosynthetic bacteria Bacteriochlorophyll a Erythrobacter Photoheterotrophy 











Fatty acid methyl esters


Infrared fast repetition rate

LH1, LH2

Light-harvesting complex 1 and 2, respectively




Polyunsaturated fatty acids




Ribulose-1,5-bisphosphate carboxylase/oxygenase


Growth rate


Functional cross-section of the photosynthetic unit at 470 nm



The authors thank Maxim Gorbunov, Michael Behrenfeld, Yoram Gerchman and Ondrej Prasil for supplying the water samples, and Kevin Wyman for laboratory assistance. This research was supported by Rutgers University through a Post-doctoral Research Fellowship to MK and by grants from NSF (Biocomplexity to PGF, and OCE-022095 to ZSK), EEC-9731725 (RRB) and OCE-9617409 (RRB), from NASA NAG5-7171 (RRB) and NAGW-3439 (RRB) and from Czech MSMT projects LN00A141 and MSM12310001 (MK) and GACR 206/03/P079 (MK).


  1. Béjà O, Suzuki MT, Heidelberg JF, Nelson WC, Preston CM, Hamada T, Eisen JA, Fraser CM, DeLong EF (2002) Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature 415:630–633CrossRefPubMedGoogle Scholar
  2. Bidigare RR, Trees CC (2000) HPLC phytoplankton pigments: Sampling, laboratory methods, and quality assurance procedures. In: Mueller J, Fargion G (eds) Ocean optics protocols for satellite ocean color sensor validation, revision 2. NASA Technical Memorandum 2000–209966, pp 154–161Google Scholar
  3. Des Marais, D.J. 2000. When did photosynthesis emerge on Earth? Science 289:1703–1704.Google Scholar
  4. Falkowski PG, Raven JA (1997) Aquatic photosynthesis. Blackwell Science, Malden, MassachusettsGoogle Scholar
  5. Fleischman D, Kramer D (1998) Photosynthetic rhizobia. Biochim Biophys Acta 1364:17–36CrossRefPubMedGoogle Scholar
  6. Fuerst JA, Hawkins JA, Holmes A, Sly LI, Moore CJ, Stackebrandt E (1993) Porphyrobacter neustonensis gen. nov., sp. nov., an aerobic bacteriochlorophyll-synthesizing budding bacterium from fresh water. Int J Syst Bacteriol 43:125–34PubMedGoogle Scholar
  7. Giovannoni SJ, DeLong EF, Olsen GJ, Pace NR (1988) Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells. J Bacteriol 170:720–726PubMedGoogle Scholar
  8. Göbel F (1978) Quantum efficiences of growth. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum , New York, pp 907–925Google Scholar
  9. Gorbunov MY, Falkowski PG, Kolber ZS (2000) Measurement of photosynthetic parameters in benthic organisms in situ using a SCUBA-based fast repetition rate fluorometer. Limnol Oceanogr 45:242–245Google Scholar
  10. Guillard RRL, Ryther JH (1962) Studies on marine planktonic diatoms I. Cyclotella nana (Hustedt) and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239Google Scholar
  11. Harashima K, Shiba T, Totsuka T, Simidu U, Taga N (1978) Occurrence of bacteriochlorophyll a in a strain of an aerobic heterotrophic bacterium. Agric Biol Chem 42:1627–1628Google Scholar
  12. Imhoff JF (2001) The anoxygenic phototrophic purple bacteria. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey's mannual of systematic bacteriology, 2nd edn, vol 1. Springer, Berlin Heidelberg New York, pp 631–637Google Scholar
  13. Jeffrey SW, Mantoura RFC, Wright SW (eds) 1997: Phytoplankton pigments in oceanography. Monographs on Oceanographic Methodology, UNESCOGoogle Scholar
  14. Ke B, Imsgard F, Kjøsen H, Liaaen-Jensen S (1970) Electronic spectra of carotenoids at 77°K. Biochim Biophys Acta 210:139–152CrossRefPubMedGoogle Scholar
  15. Kenyon CN (1978) Complex lipids and fatty acids of photosynthetic bacteria. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum, New York, pp 281–313Google Scholar
  16. Kolber ZS, Prasil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367:88–106CrossRefPubMedGoogle Scholar
  17. Kolber ZS, Van Dover CL, Niederman RA, Falkowski PG (2000) Bacterial photosynthesis in surface waters of the open ocean. Nature 407:177–179Google Scholar
  18. Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, VanDover CL, Vetriani C, Koblizek M, Rathgeber C, Falkowski PG (2001) Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292:2492–2495Google Scholar
  19. Lane DJ (1991) 16S/23S rRNA sequencing. In Stackebrant E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New YorkGoogle Scholar
  20. Nagashima KVP, Hiraishi A, Shimada K, Matsuura K (1997) Horizontal transfer of genes coding for the photosynthetic reaction centers of purple bacteria. J Mol Evol 45:131–136PubMedGoogle Scholar
  21. Nishimura Y, Muroga Y, Saito S, Shiba T, Takamiya KI, Shioi Y (1994) DNA relatedness and chemotaxonomic feature of aerobic bacteriochlorophyll-containing bacteria isolated from coast of Australia. J Gen Appl Microbiol 40:287–296Google Scholar
  22. Permentier HP, Schmidt KA, Kobayashi M, Akiyama M, Hager-Braun C, Neerken S, Miller M, Amesz J (2000) Composition and optical properties of reaction centre core complexes from the green sulfur bacteria Prosthecochloris aestuarii and Chlorobium tepidum Photosynth Res 64:27–39Google Scholar
  23. Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60:1232–1240PubMedGoogle Scholar
  24. Rye R, Holland HD (1998) Paleosols and the evolution of atmospheric oxygen: a critical review. Am J Sci 298:621–672PubMedGoogle Scholar
  25. Scheer H (ed) (1991) Chlorophylls. CRC, Boca Raton, FloridaGoogle Scholar
  26. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504CrossRefPubMedGoogle Scholar
  27. Shiba T (1991) Roseobacter litoralis gen. nov., sp. nov. and Roseobacter denitrificans sp. nov., aerobic pink-pigmented bacteria which contain bacteriochlorophyll a. Syst Appl Microbiol 14:140–145Google Scholar
  28. Shiba T, Shimidu U (1982) Erythrobacter longus gen. nov., sp. nov., an aerobic bacterium which contains bacteriochlorophyll a. Int J Syst Bacteriol 32:211–217Google Scholar
  29. Shiba T, Shimidu U, Taga N (1979) Distribution of aerobic bacteria which contain bacteriochlorophyll a. Appl Environ Microbiol 38:43–45Google Scholar
  30. Shiba T, Shioi Y, Takamiya K-I, Sutton DC, Wilkinson CR (1991) Distribution and physiology of aerobic bacteria containing bacteriochlorophyll a on the east and west coasts of Australia. Appl Environ Microbiol 57:295–300Google Scholar
  31. Shimada K (1995) Aerobic anoxygenic phototrophs. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 105–122Google Scholar
  32. Shimada K, Hayashi H, Tasumi M (1985) Bacteriochlorophyll-protein complexes of aerobic bacteria, Erythrobacter longus and Erythrobacter species OCh114. Arch Microbiol 143:244–247Google Scholar
  33. Suzuki T, Muroga Y, Takahama M, Nishimura Y (2000) Roseibium denhamense gen. nov., sp. nov. and Roseibium hamelinense sp. nov., aerobic bacteriochlorophyll-containing bacteria isolated from the east and west coast of Australia. Int J Syst Bacteriol 50:2151–2156Google Scholar
  34. Takaichi S, Shimada K, Ishidsu J-I (1988) Monocyclic cross-conjugated carotenal from an aerobic photosynthetic bacterium Erythrobacter longus. Phytochemistry 27:3605–3609CrossRefGoogle Scholar
  35. Takaichi S, Furihata K, Ishidsu J-I, Shimada K (1991) Carotenoid sulphates from the aerobic photosynthetic bacterium Erythrobacter longus. Phytochemistry 30:3411–3415CrossRefGoogle Scholar
  36. Urakami T, Komagata K (1988) Cellular fatty acid composition with special reference to the existence of hydroxy fatty acids, and the occurrence of squalene and sterols in species of Rhodospirillaceae genera and Erythrobacter longus. J Gen Appl Microbiol 34:67–84Google Scholar
  37. Wright SW, Jeffrey SW, Mantoura RFC, Llewellyn CA, Bjornland T, Repeta D, Welschmeyer N (1991) Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Mar Ecol Prog Ser 77:183–196Google Scholar
  38. Yurkov VV, Gorlenko VM (1992) New species of aerobic bacteria from the genus Erythromicrobium containing Bacteriochlorophyll a. Mikrobiologia (english edition) 61:248–255Google Scholar
  39. Yurkov VV, Beatty JT (1998) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62:695–724PubMedGoogle Scholar
  40. Yurkov VV, Gorlenko VM, Kompantseva EI (1992) A new type of freshwater aerobic orange-colored bacterium Erythromicrobium gen. nov., containing bacteriochlorophyll a. Microbiologia (english edition) 61:256–260Google Scholar
  41. Yurkov VV, Gad'on N, Drews G (1993) The major part of polar carotenoids of the aerobic bacteria Roseococcus thiosulfatophilus RB3 and Erythromicrobium ramosum E5 is not bound to the bacteriochlorophyll a-complexes of the photosynthetic apparatus. Arch Microbiol 160:372–376Google Scholar
  42. Yurkov VV, Stackebrandt E, Holmes A, Fuerst J, Hugenholtz P, Golecki J, Gad'on N, Gorlenko V, Kompantseva E, Drews G (1994) 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 44:427–434PubMedGoogle Scholar
  43. Yurkov VV, 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
  44. Zehr JP, Ward BB (2002) Nitrogen cycling in the oceans: New prospectives on processes and paradigms. Appl Environ Microbiol 68:1015–1024CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Michal Koblížek
    • 1
    • 6
  • Oded Béjà
    • 2
  • Robert R. Bidigare
    • 3
  • Stephanie Christensen
    • 3
  • Bryan Benitez-Nelson
    • 3
  • Costantino Vetriani
    • 4
  • Marcin K. Kolber
    • 1
  • Paul G. Falkowski
    • 1
    • 5
  • Zbigniew S. Kolber
    • 1
    • 7
  1. 1.Environmental Biophysics and Molecular Ecology ProgramRutgers UniversityNew BrunswickUSA
  2. 2.Department of BiologyTechnion-Israel Institute of TechnologyHaifaIsrael
  3. 3.Department of OceanographyUniversity of Hawai'i at ManoaHonoluluUSA
  4. 4.Department of Biochemistry and MicrobiologyRutgers UniversityNew BrunswickUSA
  5. 5.Department of GeologyRutgers UniversityPiscatawayUSA
  6. 6.Institute of MicrobiologyTřeboňCzechia

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