Photosynthesis Research

, Volume 81, Issue 2, pp 113–128 | Cite as

Aerobic Phototrophic Bacteria: New Evidence for the Diversity, Ecological Importance and Applied Potential of this Previously Overlooked Group

  • Christopher Rathgeber
  • J. Thomas Beatty
  • Vladimir Yurkov
Article

Abstract

The aerobic phototrophic bacteria are a recently discovered group capable of producing a photosynthetic apparatus similar to that of purple phototrophic bacteria. However, this apparatus, in contrast to that of their anaerobic counterparts, is functional in terms of photoinduced electron transport only under aerobic conditions. Although these bacteria have been widely studied, little is yet known about their ecological importance, and why they differ from other anoxygenic phototrophs with respect to oxygen requirements. In recent years a large number of new genera and species have been described from a wide variety of habitats, and evidence has been presented to support their important ecological role. This minireview focuses on recent discoveries regarding taxonomy, ecology and physiology, as well as the latest advances in the understanding of their photosynthetic apparatus and its genetic regulation.

aerobic phototrophic bacteria bacteriochlorophyll photosynthesis Roseobacter 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alarico S, Rainey FA, Empadinhas N, Schumann P, Nobre MF and Da Costa MS (2002) Rubritepida flocculans gen. nov., sp. nov., a new slightly thermophilic member of the α-1 subclass of the Proteobacteria. Syst Appl Microbiol 25: 198–206Google Scholar
  2. Bauer CE, Buggy J and Mosley C (1993) Control of photosystem genes in Rhodobacter capsulatus. Trends Genet Rev 9: 56–60Google Scholar
  3. Beatty JT (2002) On the natural selection and evolution of the aerobic phototrophic bacteria. Photosynth Res 73: 109–114Google Scholar
  4. Beja O, Suzuki MT, Heldelberg JF, Nelson WC, Preston CM, Hamada T, Elsen JA, Fraser CM and DeLong EF (2002) Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature 415: 630–633Google Scholar
  5. Boettcher KJ, Barber BJ and Singer JT (2000) Additional evidence that juvenile oyster disease is caused by a member of the Roseobacter group and colonization of nonaffected animals by Stappia stellulata-like strains. Appl Environ Microbiol 66: 3924–3930Google Scholar
  6. Buchan A, Collier LS, Neidle EL and Moran MA (2000) Key aromatic-ring-cleaving enzyme, protocatechuate 3,4-dioxygenase, in the ecologically important marine Roseobacter lineage. Appl Environ Microbiol 66: 4662–4672Google Scholar
  7. Candela M, Zaccherini E and Zannoni D (2001) Respiratory electron transport and light-induced energy transduction in membranes from the aerobic photosynthetic bacterium Roseobacter denitrificans. Arch Microbiol 175: 168–177Google Scholar
  8. Denner EBM, Vybiral D, Koblizek M, Kampfer P, Busse H and Velimirov B (2002) Erythrobacter citreus sp. nov., a yellow-pigmented bacterium that lacks bacteriochlorophyll a, isolated from the western Mediterranean Sea. Int J Syst Evol Microbiol 52: 1655–1661Google Scholar
  9. Fischer J, Quentmeier A, Gansel S and Sabados VFCG (2002) Inducible aluminum resistance of Acidiphilium cryptum and aluminum tolerance of other acidophilic bacteria. Arch Microbiol 178: 554–558Google Scholar
  10. Fleischman D and Kramer D (1998) Photosynthetic rhizobia. Biochim Biophys Acta 1364: 17–36Google Scholar
  11. Garcia D, Richaud P, Breton J and Vermeglio A (1994) Structure and function of the tetraheme cytochrome associated to the reaction center of Roseobacter denitrificans. Biochimie 76: 666–673Google Scholar
  12. Gest H (1993) Photosynthetic and quasi-photosynthetic bacteria. FEMS Microbiol Lett 112: 1–6Google Scholar
  13. Goericke R (2002) Bacteriochlorophyll a in the ocean: is anoxygenic bacterial photosynthesis important? Limnol Oceanog 47: 290–295Google Scholar
  14. Gram L, Grossart H, Schlingloff A and Kiorboe T (2002) Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl Environ Microbiol 68: 4111–4116Google Scholar
  15. Gregor J and Klug G (1999) Regulation of bacterial photosynthesis genes by oxygen and light. FEMS Microbiol Lett 179: 1–9Google Scholar
  16. Grigioni S, Boucher-Rodoni R, Demarta A Tonolla M and Peduzzi R (2000) Phylogenetic characterisation of bacterial symbionts in the accessory nidamental glands of the sepioid Sepia officinalis (Cephalopoda: Decapoda). Mar Biol 136: 217–222Google Scholar
  17. Harashima K, Nakagava M and Murata N (1982) Photochemical activity of bacteriochlorophyll in aerobically grown cells of heterotrophs, Erythrobacter species (OCh114) and Erythrobacter longus (OCh101). Plant Cell Phys 23: 185–193Google Scholar
  18. Hiraishi A and Shimada K (2001) Aerobic anoxygenic photosynthetic bacteria with zinc-bacteriochlorophyll. J Gen Appl Microbiol 47: 161–180Google Scholar
  19. Hiraishi A, Matsuzawa Y, Kanbe T and Wakao N (2000) Acidisphaera rubrifaciens gen. nov., sp. nov., an aerobic bacteriochlorophyll-containing bacterium isolated from acidic environments. Int J Syst Evol Microbiol 50: 1539–1546Google Scholar
  20. Hiraishi A, Yonemitsu Y, Matsushita M, Shin YK, Kuraishi H and Kawahara K (2002) Characterization of Porphyrobacter sanguineus sp. nov., an aerobic bacteriochlorophyll-containing bacterium capable of degrading biphenyl and dibenzofuran. Arch Microbiol 178: 45–52Google Scholar
  21. Jannasch HW and Jones GE (1959) Bacterial populations in sea water as determined by different methods of enumeration. Limnol Oceanog 4: 128–139Google Scholar
  22. Jones BE, Grant WD, Duckworth AW and Avenson GG (1998) Microbial diversity of soda lakes. Extremophiles 2: 191–200Google Scholar
  23. Kobayashi M, Akiyama M, Yamamura M, Kise H, Takaichi S, Watanabe T, Shimada K, Iwaki M, Itoh S, Ishida N, Koizumi M, Kano H, Wakao N and Hiraishi A (1998) Structural determination of the novel Zn-containing bacteriochlorophyll in Acidiphilium rubrum. Photomed Photobiol 20: 75–80Google Scholar
  24. Kolber ZS, Prasil O and Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367: 88–106Google Scholar
  25. Kolber ZS, Van Dover CL, Niederman RA and Falkowski PG (2000) Bacterial photosynthesis in surface waters of the open ocean. Nature 407: 177–179Google Scholar
  26. Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, VanDover CL, Vetriani C, Koblizek M, Rathgeber C and Falkowski PG (2001) Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292: 2492–2495Google Scholar
  27. Labrenz M, Collins MD, Lawson PA, Tindall BJ, Schumann P and Hirsch P (1999) Roseovarius tolerans gen. nov., sp. nov., a budding bacterium with variable bacteriochlorophyll a production from hypersaline Ekho Lake. Int J Syst Evol Microbiol 49: 137–147Google Scholar
  28. Labrenz M, Tindall BJ, Lawson PA, Collins MDSP and Hirsch P (2000) Staleya guttiformis gen. nov., sp. nov. and Sulfitobacter brevis sp. nov., α-3-Proteobacteria from hypersaline, heliothermal and meromictic antarctic Ekho Lake. Int J Syst Evol Microbiol 50: 303–313Google Scholar
  29. Lafay B, Ruimy R, Rauch de Traubenberg C, Breitmayer V, Gauthier M J and Christen R (1995) Roseobacter algicola sp. nov., a new marine bacterium isolated from the phycosphere of the toxin-producing dinoflaggellata Prorocentum lima. Int J Syst Bacteriol 45: 290–296Google Scholar
  30. Madigan MT, Martinko JM and Parker J (2003) Brock Biology of Microorganisms. Prentice Hall, Upper Saddle River, New JerseyGoogle Scholar
  31. Mahapatra NR, Ghosh S, Deb C and Banerjee PC (2002) Resistance to cadmium and zinc in Acidiphilium symbioticum KM2 is plasmid mediated. Current Microbiol 45: 180–186Google Scholar
  32. Masuda S and Bauer CE (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110: 613–623Google Scholar
  33. Masuda S, Matsumoto Y, Nagashima KVP, Shimada K, Inoue K, Bauer CE and Matsuura K (1999) Structural and functional analyses of photosynthetic regulatory genes regA and regB from Rhodovulum sulfidophilum, Roseobacter denitrificans and Rhodobacter capsulatus. J Bacteriol 181: 4205–4215Google Scholar
  34. Matsuda Y, Inamori K, Osaki T, Eguchi A, Watanabe A, Kawabata S, Iba K and Arata H (2002) Nitric oxide-reductase homologue that contains a copper atom and has cytochrome c-oxidase activity from an aerobic phototrophic bacterium Roseobacter denitrificans. J Biochem 131: 791–800Google Scholar
  35. Mullins TD, Britschgi TB, Krest RL and Giovannoni SJ (1995) Genetic comparisons reveal the same unknown lineages in Atlantic and Pacific bacterioplankton communities. Limnol Oceanog 40: 148–158Google Scholar
  36. Nagashima KVP, Shimada K and Matsuura K (1993) Phylogenetic analysis of photosynthetic genes of Rhodocyclus gelatinosis: possibility of horizontal gene transfer in purple bacteria. Photosynth Res 36: 185–191Google Scholar
  37. Nagashima KVP, Hiraishi A, Shimada K and Matsuura K (1997) Horizontal transfer of genes coding for the photosynthetic reaction centers of purple bacteria. J Mol Evol 45: 131–136Google Scholar
  38. Neumann U, Maier E, Schiltz E, Weckesser J and Benz R (1997) Characterization of porin from Roseobacter denitrificans. Antonie van Leeuwenhoek 72: 135–140Google Scholar
  39. Nishimura Y, Muroga Y, Saito S, Shiba T, Takamiya K and Shioi Y (1994) DNA relatedness and chemotaxonomic feature of aerobic bacteriochlorophyll-containing bacteria isolated from coasts of Australia. J Gen Appl Microbiol 40: 287–296Google Scholar
  40. Nishimura K, Shimada H, Shinmen T, Obayashi T, Masuda T, Ohta H and Takamiya K (1999) Photosynthetic regulatory gene cluster in an aerobic photosynthetic bacterium, Roseobacter denitrificans. J Gen Appl Microbiol 45: 129–143Google Scholar
  41. Oh JI and Kaplan S (2001) Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39: 1116–1123Google Scholar
  42. Okamura K, Takamiya K and Nishimura M (1985) Photosynthetic electron transfer system is inoperative in anaerobic cells of Erythrobacter species strain OCh114. Arch Microbiol 142: 12–17Google Scholar
  43. Ormerod J (2003) ‘Every dogma has its day’: a personal look at carbon metabolism in photosynthetic bacteria. Photosynth Res 76: 135–143Google Scholar
  44. Pfennig N (1978) General physiology and ecology of photosynthetic bacteria. In: Clayton R and Sistrom W (eds) The Photosynthetic Bacteria, pp 3–18. Plenum Press, New YorkGoogle Scholar
  45. Rainey FA, Silva J, Nobre MF, Silva MT and da Costa MS (2003) Porphyrobacter cryptus sp. nov., a novel slightly thermophilic, aerobic, bacteriochlorophyll a-containing species. Int J Syst Evol Microbiol 53: 35–41Google Scholar
  46. Rohwer F, Segall A, Steward G, Seguritan V, Breitbart M, Wolven F and Azam F (2000) The complete genomic sequence of the marine phage Roseophage SIO1 shares homology with nonmarine phages. Limnol Oceanog 45: 408–418Google Scholar
  47. Ruiz-Ponte C, Cilia VLC and Nicolas JL (1998) Roseobacter gallaeciensis sp. nov., a new marine bacterium isolated from rearings and collectors of the scallop Pecten maximus. Int J Syst Evol Microbiol 48: 537–542Google Scholar
  48. Ruiz-Ponte C, Samain JF, Sanchez JL and Nicolas JL (1999) The benefit of a Roseobacter species on the survival of scallop larvae. Marine Biotech 1: 52–59Google Scholar
  49. Saitoh S, Suzuki T and Nishimura Y (1998) Proposal of Craurococcus roseus gen. nov., sp. nov. and Paracraurococcus ruber gen. nov., sp. nov., novel aerobic bacteriochlorophyll a-containing bacteria from soil. Int J Syst Evol Microbiol 48: 1043–1047Google Scholar
  50. Schwarze C, Carluccio AV, Venturoli G and Labahn A (2000) Photo-induced cyclic electron transfer involving cytochrome bc 1 complex and reaction center in the obligate aerobic phototroph Roseobacter denitrificans. Europ J Biochem 267: 422–433Google Scholar
  51. Shiba T (1984) Utilization of light energy by the strictly aerobic bacterium Erythrobacter sp. OCh114. J Gen Appl Microbiol 30: 239–244Google Scholar
  52. Shiba T (1987) O2 regulation of bacteriochlorophyll synthesis in the aerobic bacterium Erythrobacter. Plant Cell Physiol 28: 1313–1320Google Scholar
  53. 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
  54. Shiba T and Harashima K (1986) Aerobic photosynthetic bacteria. Microbiol Sci 3: 376–378Google Scholar
  55. Shiba T and Simidu U (1982) Erythrobacter longus gen. nov., sp. nov., an aerobic bacterium which contains bacteriochlorophyll a. Int. J. Syst. Bacteriol. 32: 211–217Google Scholar
  56. Shiba T, Simidu U and Taga N (1979) Distribution of aerobic bacteria which contain bacteriochlorophyll a. Appl Environ Microbiol 38: 43–45Google Scholar
  57. Shiba T, Shioi Y, Takamiya K, Sutton DC and 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
  58. Shimada K (1995) Aerobic anoxygenic phototrophs. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 105–122. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  59. Sorokin DY, Tourova TP, Kuznetsov BB, Bryantseva IA and Gorlenko VM (2000) Roseinatronobacter thioxidans gen. nov., sp. nov., a new alkaliphilic aerobic bacteriochlorophyll a-containing bacterium isolated from a soda lake. Microbiology (New York) 69: 89–97Google Scholar
  60. Suyama T, Shigematsu T, Takaichi S, Nodasaka Y, Fujikawa S, Hosoya H, Tokiwa Y, Kanagawa T and Hanada S (1999) Roseateles depolymerans gen. nov., sp. nov., a new bacteriochlorophyll a-containing obligate aerobe belonging to the β-subclass of the Proteobacteria. Int J Syst Evol Microbiol 49: 449–457Google Scholar
  61. Suzuki T, Muroga Y, Takahama M and Nishimura Y (1999a) Roseivivax halodurans gen. nov., sp. nov. and Roseivivax halotolerans sp. nov., aerobic bacteriochlorophyll-containing bacteria isolated from a saline lake. Int J Syst Bacteriol 49: 629–634Google Scholar
  62. Suzuki T, Muroga Y, Takahama M, Shiba T and Nishimura Y (1999b) Rubrimonas cliftonensis gen. nov., sp. nov., an aerobic bacteriochlorophyll-containing bacterium isolated from a saline lake. Int J Syst Evol Microbiol 49: 201–205Google Scholar
  63. Suzuki T, Muroga Y, Takahama M and Nishimura Y (2000) Roseibium denhamense gen. nov., sp. nov. and Roseibium hamelinense sp. nov., aerobic bacteriochlorophyll-containing bacteria isolated from the east and west coasts of Australia. Int J Syst Evol Microbiol 50: 2151–2156Google Scholar
  64. Wakao N, Yokoi N, Isoyama N, Hiraishi A, Shimada K, Kobayashi M, Kise H, Iwaki M, Itoh S, Takaichi S and Sakurai Y (1996) Discovery of natural photosynthesis using Zn-containing bacteriochlorophyll in an aerobic bacterium Acidiphilium rubrum. Plant Cell Physiol 37: 889–893Google Scholar
  65. Woese CR, Stackebrandt E, Weisburg WG, Paster BJ, Madigan MT, Fowler VJ, Hahn CM, Blanz P, Gupta R, Nealson KH and Fox GE (1984) The phylogeny of purple bacteria: the alpha subdivision. Syst Appl Microbiol 5: 315–326Google Scholar
  66. Yurkov V (2001) Aerobic phototrophic proteobacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H and Stackebrandt E (eds) The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, Springer-Verlag, New York (http://link.springer-ny.com/link/service/books/10125/)Google Scholar
  67. Yurkov V and Beatty JT (1998a) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62: 695–724Google Scholar
  68. Yurkov V and 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: 337–341Google Scholar
  69. Yurkov VV and Csotonyi JT (2003) Aerobic anoxygenic phototrophs and heavy metal reducers from extreme environments. In: Pandalai SG (ed) Recent Research Developments in Bacteriology, Vol 1, pp 247–300. Transworld Research Network, Trivandrum, IndiaGoogle Scholar
  70. Yurkov V and Van Gemerden H (1993) Abundance and salt tolerance of obligately aerobic, phototrophic bacteria in a microbial mat. Neth J Sea Res 31: 57–62Google Scholar
  71. Yurkov V, Krieger S, Stackebrandt E and 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: 4517–4525Google Scholar
  72. Yurkova N, Rathgeber C, Swiderski J, Stackebrandt E, Beatty JT, Hall KJ and Yurkov V (2002) Diversity, distribution and physiology of the aerobic phototrophic bacteria in the mixolimnion of a meromictic lake. FEMS Microbiol Ecol 40: 191–220Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Christopher Rathgeber
    • 1
  • J. Thomas Beatty
    • 2
  • Vladimir Yurkov
    • 1
  1. 1.Department of MicrobiologyUniversity of ManitobaWinnipegCanada
  2. 2.Department of Microbiology and ImmunologyUniversity of British ColumbiaVancouverCanada

Personalised recommendations