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Nitrogen-fixing symbiosis between photosynthetic bacteria and legumes

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Abstract

Rhizobia having photosynthetic systems form nitrogen-fixing nodules on the stem and/or root of some species of the legumes Aeschynomene and Lotononis. This review is focused on the recent knowledge about the physiology, genetics and role of the photosystem in these bacteria. Photosynthetic electron transport seems to involve reaction centers, soluble cytochrome c2 and cytochrome bc1. Anaerobically, the electron transport system becomes over-reduced. The photosynthesis genes have been partially characterized; their organization is classical but their regulation is unusual as it is activated by far-red light via a bacteriophytochrome. This original mechanism of regulation seems well adapted to promote photosynthesis during stem symbiosis. Photosynthesis plays a major role in the efficiency of stem nodulation. It is also observed that infrared light stimulates nitrogen fixation in nodules containing photosynthetic bacteroids, suggesting that photosynthesis may additionally provides energy for nitrogen fixation, allowing for more efficient plant growth. Other aspects of these bacteria are discussed, in particular their taxonomic position and nodulation ability, the role of carotenoids and the potential for application of photosynthetic rhizobia in rice culture.

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References

  • Adebayo A, Watanabe I and Ladha JK (1989) Epiphytic occurrence of Azorhizobium caulinodans and other rhizobia on host and nonhost legumes. Appl Environ Microbiol 55: 2407-2409

    PubMed  Google Scholar 

  • Alazard D (1991) La nodulation caulinaire dans le genre Aeschynomene. PhD thesis, University Claude Bernard-Lyon 1, Lyon, France

    Google Scholar 

  • Alazard D and Becker M (1987) Aeschynomene as green manure for rice. Plant Soil 101: 141-143

    Article  Google Scholar 

  • Alazard D and Duhoux E (1988) Diversity of stem nodulation sites in Aeschynomene spp. J Plant Physiol 132: 123-125

    Google Scholar 

  • Alberti M, Burke DH and Hearst JE (1995) Structure and sequence of the photosynthesis gene cluster. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 775-805. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: the protein subunits. Proc Natl Acad Sci USA 84: 6162-6166

    Article  PubMed  CAS  Google Scholar 

  • Bhoo S-H, Davis SJ, Walker J, Karniol B and Vierstra RD (2001) Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 41: 776-779

    Article  CAS  Google Scholar 

  • Boivin C and Giraud E (1999) Molecular symbiotic characterization of rhizobia: towards a polyphasic approach using Nod factors and nod genes. In: Martinez E and Hernandez G (eds) Highlights of Nitrogen Fixation Research, pp 295-299. Plenum Publishing Corporation, New York

    Google Scholar 

  • Boivin C, Ndoye I, Molouba F, de Lajudie P, Depuy N and Dreyfus B (1997) Stem nodulation in legumes: diversity, mechanisms and unusual characters. Crit Rev Plant Sci 16: 1-30

    CAS  Google Scholar 

  • Chaintreuil C, Giraud E, Prin Y, Lorquin J, Bâ A, Gillis M, de Lajudie P and Dreyfus B (2000) Photosynthetic Bradyrhizobia are natural endophytes of the African wild Rice Oryza brevigulata. Appl Environ Microbiol 182: 3850-3853

    Google Scholar 

  • Chaintreuil C, Boivin C, Dreyfus B and Giraud E (2001) Characterization of the common nodulation genes of the photosynthetic Bradyrhizobium sp. ORS285 reveals the presence of a new insertion sequence upstream of nodA. FEMS Microbiol Lett 194: 83-86

    Article  PubMed  CAS  Google Scholar 

  • Chen WM, Moulin L, Bontemps C, Vandamme P, Bena G and Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J Bacteriol 24: 7266-7272

    Article  CAS  Google Scholar 

  • Choudhary M and Kaplan S (2000) DNA sequence analysis of the photosynthesis region of Rhodobacter sphaeroides 2â4â1T. Nucleic Acids Res 28: 862-867

    Article  PubMed  CAS  Google Scholar 

  • Corpe WA and Rheem S (1989) Ecology of methylotrophic bacteria on living leaf surfaces. FEMS Microbiol Ecol 62: 243-250

    Article  CAS  Google Scholar 

  • Dénarié J, Débellé F and Promé JC (1996) Rhizobium lipochitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Ann Rev Biochem 65: 503-535

    Article  PubMed  Google Scholar 

  • Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 A° resolution. Nature 318: 618-624

    Article  Google Scholar 

  • Deisenhofer J, Epp O, Sinning I and Michel H (1995) Crystallographic refinement at 2.3 A° resolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J Mol Biol 246: 429-457

    Article  PubMed  CAS  Google Scholar 

  • Duhoux E (1984) Ontogé nèse des nodules caulinaires du Sesbania rostrata (lé gumineuses). Can J Bot 62: 982-994

    Article  Google Scholar 

  • Eaglesham ARJ, Ellis JM, Evans WR, Fleischman DE, Hungria M and Hardy RWF (1990) The first photosynthetic N2 fixing rhizobium: characteristics. In: Greshoff PM, Roth LE, Stacey G and Newton WE (eds) Nitrogen Fixation: Achievements and Objectives, pp 805-811. Chapman & Hall, New York

    Google Scholar 

  • Eardly BD and Eaglesham ARJ (1985) Fixation of nitrogen and carbon by legume stem nodules. In: Evans HJ, Bottomley PJ and Newton WE (eds) Nitrogen Fixation Research Progress, p 324. Martinus Nijhoff, The Hague, The Netherlands

    Google Scholar 

  • Elsen S, Ponnampalam SN and Bauer CE (1998) CrtJ bound to distant binding sites interacts cooperatively to aerobically repress photopigment biosynthesis and light harvesting II gene expression in Rhodobacter capsulatus. J Biol Chem 273: 30762-30769

    Article  PubMed  CAS  Google Scholar 

  • Evans WR, Fleischman DE, Calvert HE, Pyati PV, Alter GM and Subba Rao NS (1990) Bacteriochlorophyll and photosynthetic reaction centers in Rhizobium strain BTAi 1. Appl Environ Microbiol 56: 3445-3449

    PubMed  CAS  Google Scholar 

  • Fleischman DE and Forquer I (2001) Regulation of formation of the photosynthetic system in a photosynthetic rhizobium. In: PS 2001 Proceedings: 12th International Congress on Photosynthesis, S4-023. CSIRO Publishing, Melbourne, Australia

    Google Scholar 

  • Fleischman D and Kramer DM (1998) Photosynthetic rhizobia. Biochim Biophys Acta 1364: 17-36

    Article  PubMed  CAS  Google Scholar 

  • Fleischman DE, Evans WR, Eaglesham ARJ, Calvert HE, Dolan Jr E, Subba Rao NS and Shanmugasundaram S (1991) Photosynthetic properties of stem nodule rhizobia. In: Dutta SK and Sloger C (eds) Biological Nitrogen Fixation Associated with Rice Production, pp 39-46. Oxford and IBH Publishing Company, New Delhi

    Google Scholar 

  • Fleischman DE, Evans WR and Miller IM (1995) Bacteriochlorophyll-containing Rhizobium species. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 123-136. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Fraser NJ, Hashimoto H and Cogdell RJ (2001) Carotenoids and bacterial photosynthesis: the story so far. Photosynth Res 70: 249-256

    Article  PubMed  CAS  Google Scholar 

  • Geurts R and Bisseling T (2002) Rhizobium Nod factor perception and signalling. Plant Cell 14: S239-S249

    PubMed  CAS  Google Scholar 

  • Giraud E, Hannibal L, Fardoux J, Verméglio A and Dreyfus B (2000) Effect of Bradyrhizobium photosynthesis on stem nodulation of Aeschynomene sensitiva. Proc Natl Acad Sci USA 97: 14795-14800

    Article  PubMed  CAS  Google Scholar 

  • Giraud E, Fardoux J, Fourrier N, Hannibal L, Genty B, Bouyer P, Dreyfus B and Verméglio A (2002) Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 417: 202-205

    Article  PubMed  CAS  Google Scholar 

  • Giraud E, Hannibal L, Fardoux J, Jaubert M, Jourand P, Dreyfus B, Sturgis JN and Verméglio A (2004a) Two distinct crt gene clusters for two different functional classes of carotenoid in Bradyrhizobium. J Biol Chem (in press)

  • Giraud E, Zappa S, Jaubert M, Hannibal L, Fardoux J, Adriano JM, Bouyer P, Genty B, Pignol D and Verméglio A (2004b) Bacteriophytochrome and regulation of synthesis of the photosynthetic apparatus in Rhodopseudomonas palustris: pitfalls of using laboratory strains. Photochem Photobiol Sci 3: 587-591

    Article  PubMed  CAS  Google Scholar 

  • Gomelsky M and Kaplan S (1995) Genetic evidence that PpsR from Rhodobacter sphaeroides 2.4.1 functions as a repressor of puc and bchF expression. J Bacteriol 177: 1634-1637

    PubMed  CAS  Google Scholar 

  • Gregor J and Klug G (1999) Regulation of bacterial photosynthesis genes by oxygen and light. FEMS Microbiol Lett 179: 1-9

    Article  PubMed  CAS  Google Scholar 

  • Hannibal L, Lorquin J, Angles d'Ortoli N, Garcia N, Chaintreuil C, Masson-Boivin C, Dreyfus B and Giraud E (2000) Isolation and characterization of canthaxanthin biosynthesis genes from the photosynthetic bacterium Bradyrhizobium sp. Strain ORS278. J Bacteriol 182: 3850-3853

    Article  PubMed  CAS  Google Scholar 

  • Harashima K, Kawazoe K, Yoshida I and Kamata H (1987) Light-stimulated growth of Erythrobacter species OCh 114. Plant Cell Physiol 28: 365-374

    CAS  Google Scholar 

  • Holland MA (1997) Methylobacterium and plants. Recent Res Devel Plant Physiol 1: 207-213

    Google Scholar 

  • Höxer A (1993) Phylogenetische Untersuchung an einer nodulierenden Methylobacterium und an verschiedenen Vertretern der fu¨ nf Klassen der Rhizobiaceae. Diplomatarbeit, Erlangen

    Google Scholar 

  • Hughes J, Lamparter T, Mittmann F, Hartmann E, Gärtner W, Wilde A and Börner T (1997) A prokaryotic phytochrome. Nature 386: 663

    Google Scholar 

  • Hungria M, Ellis JM, Hardy RWF and Eaglesham ARJ (1993) Light-stimulated 14CO2 uptake and acetylene reduction by bacteriochlorophyll-containing stem nodule isolate BTAi 1. Biol Fertil Soils 15: 1-7

    Article  Google Scholar 

  • Igarashi N, Harada J, Nagashima S, Matsuura K, Shimada K and Nagashima KV (2001) Horizontal transfer of the photosynthesis gene cluster and operon rearrangement in purple bacteria. J Mol Evol 52: 333-341

    PubMed  CAS  Google Scholar 

  • Ingham R (1996) 32P nuclear magnetic resonance studies of energy transduction and photophosphorylation of the aerobic photosynthetic rhizobium BTAi 1. MS thesis, Wright State University, Dayton, Ohio

    Google Scholar 

  • Jaftha JB, Strijdom RW and Steyn PL (2002) Characterization of pigmented methylotrophic bacteria which nodulate Lotononis bainesii. Sys Appl Microbiol 25: 440-449

    Article  CAS  Google Scholar 

  • Kaplan S (2002) Photosynthesis genes and their expression in Rhodobacter sphaeroides 2.4.1: a tribute to my students and associates. Photosynth Res 73: 95-108

    Article  PubMed  CAS  Google Scholar 

  • Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, VanDover CL, Vetriani CI, Koblizek M, Rathgeber C and Falkowski PG (2001) Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292: 2492-2495

    Article  PubMed  CAS  Google Scholar 

  • Kramer DM, Kanazawa A and Fleischman D (1997) Oxygen dependence of photosynthetic electron transport in a bacteriochlorophyll-containing rhizobium. FEBS Lett 417: 275-278

    Article  PubMed  CAS  Google Scholar 

  • Ladha JK and So RB (1994) Numerical taxonomy of phototrophic rhizobia nodulating Aeschynomene species. Int J Syst Bacteriol 44: 62-73

    Article  Google Scholar 

  • Ladha JK, Pareek RP and Becker M (1992) Stem-nodulating legume-Rhizobium symbiosis and its agronomic use in lowland rice. Adv Soil Sci 20: 147-192

    Google Scholar 

  • Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S, Do L, Land ML, Pelletier DA, Beatty JT, Lang AS, Tabita FR, Gibson JL, Hanson TE, Bobst C, Torres JL, Peres C, Harrison FH, Gibson J and Harwood CS (2004) Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotechnol 22: 55-61

    Article  PubMed  CAS  Google Scholar 

  • Lorquin J, Molouba F and Dreyfus BL (1997) Identification of the carotenoid canthaxanthin from photosynthetic Bradyrhizobium strains. Appl Environ Microbiol 63: 1151-1154

    PubMed  CAS  Google Scholar 

  • Masuda S and Bauer CE (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110: 613-623

    Article  PubMed  CAS  Google Scholar 

  • Misawa N, Satomi Y, Kondo K, Yokoyama A, Kajiwara S, Saito T, Ohtani T and Miki W (1995) Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level. J Bacteriol 177: 6575-6584

    PubMed  CAS  Google Scholar 

  • Molouba F, Lorquin J, Willems A, Hoste B, Giraud E, Dreyfus B, Gillis M, de Lajudie P and Masson-Boivin C (1999) Photosynthetic Bradyrhizobia from Aeschynomene spp. are specific to stem nodulated species and form a separate 16S ribosomal DNA restriction fragment length polymorphism group. Appl Environ Microbiol 6: 3084-3094

    Google Scholar 

  • Montecchia M, Kerber N, Pucheu N, Perticari A and Garcia AF (2002) Analysis of genome diversity among photosynthetic stem-nodulating rhizobial strains from northeast Argentina. Syst Appl Microbiol 25: 423-433

    Article  PubMed  CAS  Google Scholar 

  • Montgomery BL and Lagarias JC (2002) Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci 7: 357-366

    Article  PubMed  CAS  Google Scholar 

  • Moulin L, Munive A, Dreyfus B and Boivin-Masson C (2001) Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411: 948-950

    Article  PubMed  CAS  Google Scholar 

  • Nagashima KV, 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

    Article  PubMed  CAS  Google Scholar 

  • Ndoye I, Dreyfus B and Becker M (1996) Sesbania rostrata as green manure for lowland rice in Casamance (Senegal). Tropic Agric 73: 234-237

    Google Scholar 

  • Norris DO (1958) A red strain of Rhizobium from Lotononis bainesii Baker. Aust J Agric Res 9: 629-632

    Article  Google Scholar 

  • Ochman H and Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26: 74-86

    Article  PubMed  CAS  Google Scholar 

  • Penfold RJ and Pemberton JM (1994) Sequencing, chromosomal inactivation, and functional expression of ppsR, a gene which represses carotenoid and bacteriochlorophyll synthesis in Rhodobacter sphaeroides. J Bacteriol 176: 2869-2876

    PubMed  CAS  Google Scholar 

  • Perret X, Staehelin C and Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64: 180-201

    Article  PubMed  CAS  Google Scholar 

  • Ponnampalam SN and Bauer CE (1997) DNA binding characteristics of CrtJ. A redox-responding repressor of bacteriochlorophyll, carotenoid, and light harvesting-II gene expression in Rhodobacter capsulatus. J Biol Chem 272: 18391-18396

    Article  PubMed  CAS  Google Scholar 

  • Ponnampalam SN, Buggy JJ and Bauer CE (1995) Characterization of an aerobic repressor that coordinately regulates bacteriochlorophyll, carotenoid, and light harvesting-II expression in Rhodobacter capsulatus. J Bacteriol 177: 2990-2997

    PubMed  CAS  Google Scholar 

  • Preisig O, Zufferey R, Thony-Meyer L, Appleby CA and Hennecke H (1996) A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol 178: 1532-1538

    PubMed  CAS  Google Scholar 

  • Quail PH, Boylan MT, Parks BM, Short TW, Xu Y and Wagner D (1995) Phytochromes: photosensory perception and signal transduction. Science 268: 675-680

    PubMed  CAS  Google Scholar 

  • Roche P, Maillet F, Plazanet C, Debelle F, Ferro M, Truchet G, Prome JC and Denarie J (1996) The common nodABC genes of Rhizobium meliloti are host-range determinants. Proc Natl Acad Sci USA 93: 15305-15310

    Article  PubMed  CAS  Google Scholar 

  • Schwarze C, Carluccio AV, Venturoli G and Labahn A (2000) Photo-induced cyclic electron transfer involving cytochrome bc1 complex and reaction center in the obligate aerobic phototroph Roseobacter denitrificans. Eur J Biochem 267: 422-433

    Article  PubMed  CAS  Google Scholar 

  • Shimada K (1995) Aerobic anoxygenic bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 105-122. Kluwer Academic Publishers, Dordrecht, The Netherlands

  • Smith H (2000) Phytochromes and light signal perception by plants-an emerging synthesis. Nature 407: 585-591

    Article  PubMed  CAS  Google Scholar 

  • Stowers MD and Eaglesham ARJ (1983) A stem-nodulating Rhizobium with physiological characteristics of both fast and slow growers. J Gen Microbiol 129: 3651-3655

    CAS  Google Scholar 

  • Suominen L, Roos C, Lortet G, Paulin L and Lindstrom K (2001) Identification and structure of the Rhizobium galegae common nodulation genes: evidence for horizontal gene transfer. Mol Biol Evol 18: 907-916

    PubMed  CAS  Google Scholar 

  • Suyama T, Shigematsu T, Suzuki T, Tokiwa Y, Kanagawa T, Nagashima KVP and Hanada S (2002) Photosynthetic apparatus in Roseateles depolymerans 61A is transcriptionally induced by carbon limitation. Appl Environ Microbiol 68: 1665-1673

    Article  PubMed  CAS  Google Scholar 

  • Sy A, Giraud E, Jourand P, Garcia N, Willems A, De Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C and Dreyfus B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183: 214-220

    Article  PubMed  CAS  Google Scholar 

  • Takaichi S (1999) Carotenoids and carotenogenesis in anoxygenic photosynthetic bacteria. In: Frank HA, Young AJ, Britton G and Cogdell RJ (eds) The Photochemistry of Carotenoids, pp 40-69. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Van Berkum P and Eardly BD (1998) Molecular Evolutionary Systematics of the Rhizobiaceae. In: Spaink HP, Kondorosi A and Hooykaas PJ (eds) The Rhizobiaceae; Molecular Biology of Model Plant-Associated Bacteria, pp 1-24. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Van Berkum P and Eardly BD (2002) The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. Appl Environ Microbiol 68: 1132-1136

    Article  PubMed  CAS  Google Scholar 

  • Van Berkum P, Tully RE and Keister DL (1995) Nonpigmented and bacteriochlorophyll-containing Bradyrhizobia isolated from Aeschynomene indica. Appl Environ Microbiol 61: 623-629

    PubMed  CAS  Google Scholar 

  • Van Rhijn P and Vanderleyden J (1995) The Rhizobium-plant symbiosis. Microbiol Rev 59: 124-142

    PubMed  CAS  Google Scholar 

  • Wettlaufer SH and Hardy RWF (1992) Effect of light and organic acids on oxygen uptake by BTAi 1, a photosynthetic rhizobium. Appl Environ Microbiol 58: 3830-3833

    PubMed  CAS  Google Scholar 

  • Wettlaufer SH and Hardy RWF (1995) Effect of oxygen and light on the accumulation of bacteriochlorophyll in the rhizobial strain BTAi1. Plant Cell Physiol 36: 391-396

    CAS  Google Scholar 

  • Willems A, Doignon-Bourcier F, Coopman R, Hoste B, de Lajudie P and Gillis M (2000) AFLP fingerprint analysis of Bradyrhizobium strains isolated from Faidherbia albida and Aeschynomene species. Syst Appl Microbiol 23: 137-47

    PubMed  CAS  Google Scholar 

  • Willems A, Doignon-Bourcier F, Goris J, Coopman R, de Lajudie P, De Vos P and Gillis M (2001) DNA-DNA hybridization study of Bradyrhizobium strains. Int J Syst Evol Microbiol 51: 1315-22

    PubMed  CAS  Google Scholar 

  • Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, De Bruijn F, Stolzfus J, Buckley D, Schimdt TM, Mateos PF, Ladha JK and Dazzo FB (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194: 99-114

    Article  CAS  Google Scholar 

  • Yen HC and Marrs B (1976) Map of genes for carotenoid and bacteriochlorophyll biosynthesis in Rhodopseudomonas capsulata. J Bacteriol 126: 619-629

    PubMed  CAS  Google Scholar 

  • Yildiz FH, Gest H and Bauer CE (1992) Conservation of the photosynthesis gene cluster in Rhodospirillum centenum. Mol Microbiol 6: 2683-2691

    PubMed  CAS  Google Scholar 

  • Young JPW, Downer HL and Eardly BD (1991) Phylogeny of the phototropic rhizobium strain BTAi 1 by polymerase chain reaction-based sequencing of a 16S rRNA gene segment. J Bacteriol 173: 2271-2277

    PubMed  CAS  Google Scholar 

  • Yurkov VV and Beatty JT (1998) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62: 695-724

    PubMed  CAS  Google Scholar 

  • Yurkov VB, Schoepp B and Verméglio A (1995) Electron transport carriers in obligately aerobic photosynthetic bacteria from genera Roseococcus and Erythromicrobium. In: Mathis P (ed) Photosynthesis: from Light to Biosphere, pp 543-546. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Zucconi AP and Beatty JT (1988) Posttranscriptional regulation by light of the steady-state levels of mature B800-850 light-harvesting complexes in Rhodobacter capsulatus. J Bacteriol 170: 877-882

    PubMed  CAS  Google Scholar 

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Giraud, E., Fleischman, D. Nitrogen-fixing symbiosis between photosynthetic bacteria and legumes. Photosynthesis Research 82, 115–130 (2004). https://doi.org/10.1007/s11120-004-1768-1

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