1887

Abstract

It is commonly accepted that green filamentous anoxygenic phototrophic (FAP) bacteria are the most ancient representatives of phototrophic micro-organisms. Modern FAPs belonging to the order are divided into two suborders: and . Representatives of lack chlorosomes and synthesize bacteriochlorophyll , whereas those of synthesize bacteriochlorophylls and and utilize chlorosomes for light harvesting. Though they constitute a small number of species, FAPs are quite diverse in their physiology. This bacterial group includes autotrophs and heterotrophs, thermophiles and mesophiles, aerobes and anaerobes, occupying both freshwater and halophilic environments. The anaerobic mesophilic autotroph DG-6 is still not well studied in its physiology, and its evolutionary origin remains unclear. The goals of this study included identification of the reaction centre type of DG-6, reconstruction of its bacteriochlorophyll biosynthesis pathways, and determination of its evolutionary relationships with other FAPs. By enzymic and genomic analysis, the presence of RCII in DG-6 was demonstrated and the complete gene set involved in biosynthesis of bacteriochlorophylls and was established. We found that the bacteriochlorophyll gene sets differed between aerobic and anaerobic FAPs. The aerobic FAP genomes code oxygen-dependent AcsF cyclases, but lack the / genes, which have been associated with adaptation to low light conditions in the anaerobic FAPs. A scenario of evolution of FAPs belonging to the order is proposed.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.082313-0
2015-01-01
2019-11-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/1/120.html?itemId=/content/journal/micro/10.1099/mic.0.082313-0&mimeType=html&fmt=ahah

References

  1. Berg I. A. , Keppen O. I. , Krasil’nikova E. N. , Ugol’kova N. V. , Ivanovskiǐ R. N. . ( 2005; ). [ Carbon metabolism of filamentous anoxygenic phototrophic bacteria of the family Oscillochloridaceae . ]. Mikrobiologiia 74:, 305–312 (in Russian).[PubMed]
    [Google Scholar]
  2. Blankenship R. E. . ( 2010; ). Early evolution of photosynthesis. . Plant Physiol 154:, 434–438. [CrossRef] [PubMed]
    [Google Scholar]
  3. Blankenship R. A. . ( 2014; ). Reaction centers and electron transport pathways in anoxygenic phototrophs. . Molecular Mechanisms of Photosynthesis, , 2nd edn., pp. 89–109. Chichester:: John Wiley & Sons;.
    [Google Scholar]
  4. Bogorov L. V. . ( 1974; ). [ The properties of Thiocapsa roseopersicina, strain BBS, isolated from an estuary of the White Sea. ]. Mikrobiologiia 43:, 326–332 (in Russian).[PubMed]
    [Google Scholar]
  5. Bromham L. , Penny D. . ( 2003; ). The modern molecular clock. . Nat Rev Genet 4:, 216–224. [CrossRef] [PubMed]
    [Google Scholar]
  6. Bryant D. A. , Vassilieva E. V. , Frigaard N. U. , Li H. . ( 2002; ). Selective protein extraction from Chlorobium tepidum chlorosomes using detergents. Evidence that CsmA forms multimers and binds bacteriochlorophyll a . . Biochemistry 41:, 14403–14411. [CrossRef] [PubMed]
    [Google Scholar]
  7. Bryant D. A. , Liu Z. , Li T. , Zhao F. , Costas A. M. G. . ( 2012; ). Comparative and functional genomics of anoxygenic green bacteria from the taxa Chlorobi, Chloroflexi, and Acidobacteria . . In Functional Genomics and Evolution of Photosynthetic Systems (Advances in Photosynthesis and Respiration, vol. 33) , pp. 47–102. Edited by Burnap R. L. , Vermaas W. F. J. . . Dordrecht:: Springer;. [CrossRef]
    [Google Scholar]
  8. Bryantseva I. A. , Gorlenko V. M. , Kompantseva E. I. , Achenbach L. A. , Madigan M. T. . ( 1999; ). Heliorestis daurensis, gen. nov. sp. nov., an alkaliphilic rod-to-coiled-shaped phototrophic heliobacterium from a Siberian soda lake. . Arch Microbiol 172:, 167–174. [CrossRef] [PubMed]
    [Google Scholar]
  9. Chew A. G. , Bryant D. A. . ( 2007; ). Chlorophyll biosynthesis in bacteria: the origins of structural and functional diversity. . Annu Rev Microbiol 61:, 113–129. [CrossRef] [PubMed]
    [Google Scholar]
  10. Chew A. G. M. , Frigaard N.-U. , Bryant D. A. . ( 2007; ). Bacteriochlorophyllide c C-8(2) and C-12(1) methyltransferases are essential for adaptation to low light in Chlorobaculum tepidum . . J Bacteriol 189:, 6176–6184. [CrossRef] [PubMed]
    [Google Scholar]
  11. Collins A. M. , Xin Y. , Blankenship R. E. . ( 2009; ). Pigment organization in the photosynthetic apparatus of Roseiflexus castenholzii . . Biochim Biophys Acta 1787:, 1050–1056. [CrossRef] [PubMed]
    [Google Scholar]
  12. Collins A. M. , Qian P. , Tang Q. , Bocian D. F. , Hunter C. N. , Blankenship R. E. . ( 2010; ). Light-harvesting antenna system from the phototrophic bacterium Roseiflexus castenholzii . . Biochemistry 49:, 7524–7531. [CrossRef] [PubMed]
    [Google Scholar]
  13. Elcock A. H. , McCammon J. A. . ( 1998; ). Electrostatic contributions to the stability of halophilic proteins. . J Mol Biol 280:, 731–748. [CrossRef] [PubMed]
    [Google Scholar]
  14. Felsenstein J. . ( 1996; ). Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. . Methods Enzymol 266:, 418–427. [CrossRef] [PubMed]
    [Google Scholar]
  15. Frigaard N. U. , Bryant D. A. . ( 2004; ). Seeing green bacteria in a new light: genomics-enabled studies of the photosynthetic apparatus in green sulfur bacteria and filamentous anoxygenic phototrophic bacteria. . Arch Microbiol 182:, 265–276. [CrossRef] [PubMed]
    [Google Scholar]
  16. Frigaard N. U. , Chew A. G. , Li H. , Maresca J. A. , Bryant D. A. . ( 2003; ). Chlorobium tepidum: insights into the structure, physiology, and metabolism of a green sulfur bacterium derived from the complete genome sequence. . Photosynth Res 78:, 93–117. [CrossRef] [PubMed]
    [Google Scholar]
  17. Ganapathy S. , Oostergetel G. T. , Reus M. , Tsukatani Y. , Chew A. G. M. , Buda F. , Bryant D. A. , Holzwarth A. R. , de Groot H. J. . ( 2012; ). Structural variability in wild-type and bchQ bchR mutant chlorosomes of the green sulfur bacterium Chlorobaculum tepidum . . Biochemistry 51:, 4488–4498. [CrossRef] [PubMed]
    [Google Scholar]
  18. Gupta R. S. . ( 2003; ). Evolutionary relationships among photosynthetic bacteria. . Photosynth Res 76:, 173–183. [CrossRef] [PubMed]
    [Google Scholar]
  19. Gupta R. S. , Chander P. , George S. . ( 2013; ). Phylogenetic framework and molecular signatures for the class Chloroflexi and its different clades; proposal for division of the class Chloroflexi class. nov. [corrected] into the suborder Chloroflexineae subord. nov., consisting of the emended family Oscillochloridaceae and the family Chloroflexaceae fam. nov., and the suborder Roseiflexineae subord. nov., containing the family Roseiflexaceae fam. nov. . Antonie van Leeuwenhoek 103:, 99–119. [CrossRef] [PubMed]
    [Google Scholar]
  20. Hanada S. , Pierson B. K. . ( 2006; ). The family Chloroflexaceae . . In Proteobacteria: Delta, Epsilon Subclass ( The Prokaryotes , vol. 7), ch. 10.1, pp. 815–842. Edited by Dworkin M. , Falkow S. , Rosenberg E. , Schleifer K.-H. , Stackebrandt E. . . New York:: Springer;. [CrossRef]
    [Google Scholar]
  21. Hanada S. , Takaichi S. , Matsuura K. , Nakamura K. . ( 2002; ). Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes. . Int J Syst Evol Microbiol 52:, 187–193.[PubMed] [CrossRef]
    [Google Scholar]
  22. Herter S. , Fuchs G. , Bacher A. , Eisenreich W. . ( 2002; ). A bicyclic autotrophic CO2 fixation pathway in Chloroflexus aurantiacus . . J Biol Chem 277:, 20277–20283. [CrossRef] [PubMed]
    [Google Scholar]
  23. Hillier W. , Babcock G. T. . ( 2001; ). Photosynthetic reaction centers. . Plant Physiol 125:, 33–37. [CrossRef] [PubMed]
    [Google Scholar]
  24. House C. H. . ( 2009; ). The tree of life viewed through the contents of genomes. . Methods Mol Biol 532:, 141–161. [CrossRef] [PubMed]
    [Google Scholar]
  25. Ivanovsky R. N. , Fal Y. I. , Berg I. A. , Ugolkova N. V. , Krasilnikova E. N. , Keppen O. I. , Zakharchuc L. M. , Zyakun A. M. . ( 1999; ). Evidence for the presence of the reductive pentose phosphate cycle in a filamentous anoxygenic photosynthetic bacterium, Oscillochloris trichoides strain DG-6. . Microbiology 145:, 1743–1748. [CrossRef] [PubMed]
    [Google Scholar]
  26. Kennedy S. P. , Ng W. V. , Salzberg S. L. , Hood L. , DasSarma S. . ( 2001; ). Understanding the adaptation of Halobacterium species NRC-1 to its extreme environment through computational analysis of its genome sequence. . Genome Res 11:, 1641–1650. [CrossRef] [PubMed]
    [Google Scholar]
  27. Keppen O. I. , Baulina O. I. , Kondratieva E. N. . ( 1994; ). Oscillochloris trichoides neotype strain DG-6. . Photosynth Res 41:, 29–33. [CrossRef] [PubMed]
    [Google Scholar]
  28. Keppen O. I. , Tourova T. P. , Kuznetsov B. B. , Ivanovsky R. N. , Gorlenko V. M. . ( 2000; ). Proposal of Oscillochloridaceae fam. nov. on the basis of a phylogenetic analysis of the filamentous anoxygenic phototrophic bacteria, and emended description of Oscillochloris and Oscillochloris trichoides in comparison with further new isolates. . Int J Syst Evol Microbiol 50:, 1529–1537. [CrossRef] [PubMed]
    [Google Scholar]
  29. Klappenbach J. A. , Pierson B. K. . ( 2004; ). Phylogenetic and physiological characterization of a filamentous anoxygenic photoautotrophic bacterium ‘Candidatus Chlorothrix halophila’ gen. nov., sp. nov., recovered from hypersaline microbial mats. . Arch Microbiol 181:, 17–25. [CrossRef] [PubMed]
    [Google Scholar]
  30. Kratz W. A. , Myers J. . ( 1955; ). Nutrition and growth of several blue-green algae. . Am J Bot 42:, 282–287. [CrossRef]
    [Google Scholar]
  31. Kuznetsov B. B. , Ivanovsky R. N. , Keppen O. I. , Sukhacheva M. V. , Bumazhkin B. K. , Patutina E. O. , Beletsky A. V. , Mardanov A. V. , Baslerov R. V. . & other authors ( 2011; ). Draft genome sequence of the anoxygenic filamentous phototrophic bacterium Oscillochloris trichoides subsp. DG-6. . J Bacteriol 193:, 321–322. [CrossRef] [PubMed]
    [Google Scholar]
  32. Lanyi J. K. . ( 1974; ). Salt-dependent properties of proteins from extremely halophilic bacteria. . Bacteriol Rev 38:, 272–290.[PubMed]
    [Google Scholar]
  33. Larkum A. W. D. . ( 2006; ). Evolution of chlorophylls and photosynthesis. . In Chlorophylls and Bacteriochlorophylls (Advances in Photosynthesis and Respiration, vol. 25), ch. 18 , pp. 261–282. Edited by Grimm B. , Porra R. J. , Rüdiger W. , Scheer H. . . Dordrecht:: Springer;. [CrossRef]
    [Google Scholar]
  34. Larsen H. . ( 1952; ). On the culture and general physiology of the green sulfur bacteria. . J Bacteriol 64:, 187–196.[PubMed]
    [Google Scholar]
  35. Liu Z. , Bryant D. A. . ( 2011; ). Multiple types of 8-vinyl reductases for (bacterio)chlorophyll biosynthesis occur in many green sulfur bacteria. . J Bacteriol 193:, 4996–4998. [CrossRef] [PubMed]
    [Google Scholar]
  36. Madigan M. T. , Petersen S. R. , Brock T. D. . ( 1974; ). Nutritional studies on Chloroflexus, a filamentous photosynthetic, gliding bacterium. . Arch Microbiol 100:, 97–103. [CrossRef]
    [Google Scholar]
  37. Markowitz V. M. , Chen I. M. , Palaniappan K. , Chu K. , Szeto E. , Grechkin Y. , Ratner A. , Jacob B. , Huang J. . & other authors ( 2012; ). IMG: the Integrated Microbial Genomes database and comparative analysis system. . Nucleic Acids Res 40: (Database issue), D115–D122. [CrossRef] [PubMed]
    [Google Scholar]
  38. Montaño G. A. , Wu H. M. , Lin S. , Brune D. C. , Blankenship R. E. . ( 2003; ). Isolation and characterization of the B798 light-harvesting baseplate from the chlorosomes of Chloroflexus aurantiacus . . Biochemistry 42:, 10246–10251. [CrossRef] [PubMed]
    [Google Scholar]
  39. Orf G. S. , Blankenship R. E. . ( 2013; ). Chlorosome antenna complexes from green photosynthetic bacteria. . Photosynth Res 116:, 315–331. [CrossRef] [PubMed]
    [Google Scholar]
  40. Paul S. , Bag S. K. , Das S. , Harvill E. T. , Dutta C. . ( 2008; ). Molecular signature of hypersaline adaptation: insights from genome and proteome composition of halophilic prokaryotes. . Genome Biol 9:, R70. [CrossRef] [PubMed]
    [Google Scholar]
  41. Pedersen M. O. , Underhaug J. , Dittmer J. , Miller M. , Nielsen N. C. . ( 2008; ). The three-dimensional structure of CsmA: a small antenna protein from the green sulfur bacterium Chlorobium tepidum . . FEBS Lett 582:, 2869–2874. [CrossRef] [PubMed]
    [Google Scholar]
  42. Pedersen M. O. , Linnanto J. , Frigaard N. U. , Nielsen N. C. , Miller M. . ( 2010; ). A model of the protein-pigment baseplate complex in chlorosomes of photosynthetic green bacteria. . Photosynth Res 104:, 233–243. [CrossRef] [PubMed]
    [Google Scholar]
  43. Reid J. D. , Hunter C. N. . ( 2004; ). Magnesium-dependent ATPase activity and cooperativity of magnesium chelatase from Synechocystis sp. PCC6803. . J Biol Chem 279:, 26893–26899. [CrossRef] [PubMed]
    [Google Scholar]
  44. Sousa F. L. , Shavit-Grievink L. , Allen J. F. , Martin W. F. . ( 2013; ). Chlorophyll biosynthesis gene evolution indicates photosystem gene duplication, not photosystem merger, at the origin of oxygenic photosynthesis. . Genome Biol Evol 5:, 200–216. [CrossRef] [PubMed]
    [Google Scholar]
  45. Taisova A. S. , Keppen O. I. , Lukashev E. P. , Arutyunyan A. M. , Fetisova Z. G. . ( 2002; ). Study of the chlorosomal antenna of the green mesophilic filamentous bacterium Oscillochloris trichoides . . Photosynth Res 74:, 73–85. [CrossRef] [PubMed]
    [Google Scholar]
  46. Tamura K. , Dudley J. , Nei M. , Kumar S. . ( 2007; ). MEGA4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. . Mol Biol Evol 24:, 1596–1599. [CrossRef] [PubMed]
    [Google Scholar]
  47. Tang K. H. , Wen J. , Li X. , Blankenship R. E. . ( 2009; ). Role of the AcsF protein in Chloroflexus aurantiacus . . J Bacteriol 191:, 3580–3587. [CrossRef] [PubMed]
    [Google Scholar]
  48. Tang K. H. , Barry K. , Chertkov O. , Dalin E. , Han C. S. , Hauser L. J. , Honchak B. M. , Karbach L. E. , Land M. L. . & other authors ( 2011; ). Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus . . BMC Genomics 12:, 334. [CrossRef] [PubMed]
    [Google Scholar]
  49. Turova T. P. , Spiridonova E. M. , Slobodova N. V. , Bulygina E. S. , Keppen O. I. , Kuznetsov B. B. , Ivanovskiǐ R. N. . ( 2006; ). [ Phylogeny of anoxygenic filamentous phototrophic bacteria of the family Oscillochloridaceae as inferred from comparative analyses of the rrs, cbbL, and nifH genes. ]. Mikrobiologiia 75:, 235–244 (in Russian). [PubMed]
    [Google Scholar]
  50. van der Meer M. T. J. , Schouten S. , Bateson M. M. , Nübel U. , Wieland A. , Kühl M. , de Leeuw J. W. , Sinninghe Damsté J. S. , Ward D. M. . ( 2005; ). Diel variations in carbon metabolism by green nonsulfur-like bacteria in alkaline siliceous hot spring microbial mats from Yellowstone National Park. . Appl Environ Microbiol 71:, 3978–3986. [CrossRef] [PubMed]
    [Google Scholar]
  51. van der Meer M. T. J. , Klatt C. G. , Wood J. , Bryant D. A. , Bateson M. M. , Lammerts L. , Schouten S. , Damsté J. S. S. , Madigan M. T. , Ward D. M. . ( 2010; ). Cultivation and genomic, nutritional, and lipid biomarker characterization of Roseiflexus strains closely related to predominant in situ populations inhabiting Yellowstone hot spring microbial mats. . J Bacteriol 192:, 3033–3042. [CrossRef] [PubMed]
    [Google Scholar]
  52. Ward J. H. Jr . ( 1963; ). Hierarchical grouping to optimize an objective function. . J Am Stat Assoc 58:, 236–244. [CrossRef]
    [Google Scholar]
  53. Xiong J. , Fischer W. M. , Inoue K. , Nakahara M. , Bauer C. E. . ( 2000; ). Molecular evidence for the early evolution of photosynthesis. . Science 289:, 1724–1730. [CrossRef] [PubMed]
    [Google Scholar]
  54. Zarzycki J. , Brecht V. , Müller M. , Fuchs G. . ( 2009; ). Identifying the missing steps of the autotrophic 3-hydroxypropionate CO2 fixation cycle in Chloroflexus aurantiacus . . Proc Natl Acad Sci U S A 106:, 21317–21322. [CrossRef] [PubMed]
    [Google Scholar]
  55. Zobova A. , Taisova A. , Lukashev E. , Fedorova N. , Baratova L. , Fetisova Z. . ( 2011; ). CsmA protein is associated with BChl a in the baseplate subantenna of chlorosomes of the photosynthetic green filamentous bacterium Oscillochloris trichoides belonging to the family Oscillochloridaceae . . J Biophys 2011:, 860382. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.082313-0
Loading
/content/journal/micro/10.1099/mic.0.082313-0
Loading

Data & Media loading...

Supplements

Supplementary Data



PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error