Aerobic phototrophic bacteria: New evidence for the diversity, ecological importance and applied potential of this previously overlooked group

Photosynthesis Research

Volumn 81, Issue 2, 2004, Pages 113-128

  Rathgeber, Christopher ^a   Beatty, J Thomas ^b   Yurkov, Vladimir ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

aerobic phototrophic bacteria; bacteriochlorophyll; photosynthesis; Roseobacter

Indexed keywords

BACTERIA (MICROORGANISMS); PHOTOBACTERIA; ROSEOBACTER;

EID: 3843152646     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:PRES.0000035036.49977.bc     Document Type: Review

References (72)

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: 198-206
2. Bauer CE, Buggy J and Mosley C (1993) Control of photosystem genes in Rhodobacter capsulatus. Trends Genet Rev 9: 56-60
3. Beatty JT (2002) On the natural selection and evolution of the aerobic phototrophic bacteria. Photosynth Res 73: 109-114
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: 630-633
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: 3924-3930
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: 4662-4672
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: 168-177
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: 1655-1661
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: 554-558
10. Fleischman D and Kramer D (1998) Photosynthetic rhizobia. Biochim Biophys Acta 1364: 17-36
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: 666-673
12. Gest H (1993) Photosynthetic and quasi-photosynthetic bacteria. FEMS Microbiol Lett 112: 1-6
13. Goericke R (2002) Bacteriochlorophyll a in the ocean: is anoxygenic bacterial photosynthesis important? Limnol Oceanogr 47: 290-295
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: 4111-4116
15. Gregor J and Klug G (1999) Regulation of bacterial photosynthesis genes by oxygen and light. FEMS Microbiol Lett 179: 1-9
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: 217-222
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 Physiol 23: 185-193
18. Hiraishi A and Shimada K (2001) Aerobic anoxygenic photosynthetic bacteria with zinc-bacteriochlorophyll. J Gen Appl Microbiol 47: 161-180
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: 1539-1546
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: 45-52
21. Jannasch HW and Jones GE (1959) Bacterial populations in sea water as determined by different methods of enumeration. Limnol Oceanogr 4: 128-139
22. Jones BE, Grant WD, Duckworth AW and Avenson GG (1998) Microbial diversity of soda lakes. Extremophiles 2: 191-200
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 rubrurn. Photomed Photobiol 20: 75-80
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: 88-106
25. Kolber ZS, Van Dover CL, Niederman RA and Falkowski PG (2000) Bacterial photosynthesis in surface waters of the open ocean. Nature 407: 177-179
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: 2492-2495
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: 137-147
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, heliothemial and meromictic antarctic Ekho Lake. Int J Syst Evol Microbiol 50: 303-313
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: 290-296
30. Madigan MT, Martinko JM and Parker J (2003) Brock Biology of Microorganisms. Prentice Hall, Upper Saddle River, New Jersey
31. Mahapatra NR, Ghosh S, Deb C and Banerjee PC (2002) Resistance to cadmium and zinc in Acidiphilium symbioticum KM2 is plasmid mediated. Curr Microbiol 45: 180-186
32. Masuda S and Bauer CE (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110: 613-623
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: 4205-4215
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: 791-800
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 Oceanogr 40: 148-158
36. Nagashima KVP, Shimada K and Matsuura K (1993) Phylogenetic analysis of photosynthetic genes of Rhodocychis gelatinosis: possibility of horizontal gene transfer in purple bacteria. Photosynth Res 36: 185-191
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: 131-136
38. Neumann U, Maier E, Schiltz E, Weckesser J and Benz R (1997) Characterization of porin from Roseobacter denitrificans. Antonie van Leeuwenhoek 72: 135-140
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: 287-296
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: 129-143
41. Oh JI and Kaplan S (2001) Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39: 1116-1123
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: 12-17
43. Ormerod J (2003) 'Every dogma has its day': a personal look at carbon metabolism in photosynthetic bacteria. Photosynth Res 76: 135-143
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 York
45. Rainey FA, Suva 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: 35-41
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 Oceanogr 45: 408-418
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: 537-542
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: 52-59
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: 1043-1047
50. Schwarze C, Carluccio AV, Venturoli G and Labahn A (2000) Photo-induced cyclic electron transfer involving cytochrome bci complex and reaction center in the obligate aerobic phototroph Roseobacter denitrificans. Eur J Biochem 267: 422-433
51. Shiba T (1984) Utilization of light energy by the strictly aerobic bacterium Erythrobacter sp. OCh114. J Gen Appl Microbiol 30: 239-244
52. 2 regulation of bacteriochlorophyll synthesis in the aerobic bacterium Erythrobacter. Plant Cell Physiol 28: 1313-1320
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: 140-145
54. Shiba T and Harashima K (1986) Aerobic photosynthetic bacteria. Microbiol Sci 3: 376-378
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: 211-217
56. Shiba T, Simidu U and Taga N (1979) Distribution of aerobic bacteria which contain bacteriochlorophyll a. Appl Environ Microbiol 38: 43-45
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: 295-300
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 Netherlands
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: 89-97
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 Proleobacleria. Int J Syst Evol Microbiol 49: 449-457
61. Suzuki T, Muroga Y, Takahama M and Nishimura Y (1999a) Roseivivax halodurans gen. nov., sp. nov. and Roseivivax halololerans sp. nov., aerobic bacteriochlorophyll-containing bacteria isolated from a saline lake. Int J Syst Bacteriol 49: 629-634
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: 201-205
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: 2151-2156
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: 889-893
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: 315-326
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/ )
67. Yurkov V and Beatty JT (1998a) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62: 695-724
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: 337-341
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, India
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: 57-62
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: 4517-4525
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: 191-220