1932

Abstract

Because of recent advances in omics methodologies, knowledge of chlorophototrophy (i.e., chlorophyll-based phototrophy) in bacteria has rapidly increased. Chlorophototrophs currently are known to occur in seven bacterial phyla: , , , , , , and . Other organisms that can produce chlorophylls and photochemical reaction centers may still be undiscovered. Here we summarize the current status of the taxonomy and phylogeny of chlorophototrophic bacteria as revealed by genomic methods. In specific cases, we briefly describe important ecophysiological and metabolic insights that have been gained from the application of genomic methods to these bacteria. In the 20 years since the completion of the sp. PCC 6803 genome in 1996, approximately 1,100 genomes have been sequenced, which represents nearly the complete diversity of known chlorophototrophic bacteria. These data are leading to new insights into many important processes, including photosynthesis, nitrogen and carbon fixation, cellular differentiation and development, symbiosis, and ecosystem functionality.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-042817-040500
2018-04-29
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/arplant/69/1/annurev-arplant-042817-040500.html?itemId=/content/journals/10.1146/annurev-arplant-042817-040500&mimeType=html&fmt=ahah

Literature Cited

  1. Albuquerque L, Rainey FA, Nobre MF, da Costa MS. 1.  2008. Elioraea tepidiphila gen. nov., sp. nov., a slightly thermophilic member of the Alphaproteobacteria. Int. J. Syst. Evol. Microbiol 58:773–78 [Google Scholar]
  2. Beatty JT. 2.  2013. Genome Evolution of Photosynthetic Bacteria Advances in Botanical Research 66 Amsterdam: Elsevier
  3. Becraft ED, Wood JM, Rusch DB, Kühl M, Jensen SI. 3.  et al. 2015. The molecular dimension of microbial species. 1. Ecological distinctions among, and homogeneity within, putative ecotypes of Synechococcus inhabiting the cyanobacterial mat of Mushroom Spring, Yellowstone National Park. Front. Microbiol. 6:590 [Google Scholar]
  4. Benzerara K, Skori-Panet F, Li J, Férard C, Gugger M. 4.  et al. 2014. Intracellular Ca-carbonate biomineralization is widespread in cyanobacteria. PNAS 111:10933–38 [Google Scholar]
  5. Biller SJ, Berube PM, Berta-Thompson JW, Kelly L, Roggensack SE. 5.  et al. 2014. Genomes of diverse isolates of the marine cyanobacterium Prochlorococcus. Sci. Data 1:140034 [Google Scholar]
  6. Biller SJ, Berube PM, Lindell D, Chisholm SW. 6.  2015. Prochlorococcus: the structure and function of collective diversity. Nat. Rev. Microbiol. 13:13–27 [Google Scholar]
  7. Bombar D, Heller P, Sanchez-Baracaldo P, Carter BJ, Zehr JP. 7.  2014. Comparative genomics reveals surprising divergence of two closely related strains of uncultivated UCYN-A cyanobacteria. ISME J 8:2530–42 [Google Scholar]
  8. Boomer SM, Noll KL, Geesey GG, Dutton BE. 8.  2009. Formation of multilayered photosynthetic biofilms in an alkaline thermal spring in Yellowstone National Park, Wyoming. Appl. Environ. Microbiol. 75:2464–75 [Google Scholar]
  9. Braakman R, Follows MJ, Chisholm SW. 9.  2017. Metabolic evolution and the self-organization of ecosystems. PNAS 114:E3091–100 [Google Scholar]
  10. Bryant DA, Canniffe DP. 10.  2017. How nature designs antenna proteins. Light-harvesting antenna systems in diverse chlorophototrophic prokaryotes: design principles and functional realization. J. Phys. B 51:033001 [Google Scholar]
  11. Bryant DA, Frigaard N-U. 11.  2006. Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–96 [Google Scholar]
  12. Bryant DA, Garcia Costas AM, Maresca JA, Gomez Maqueo Chew A, Klatt CG. 12.  et al. 2007. Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science 317:523–26 [Google Scholar]
  13. Bryant DA, Liu Z. 13.  2013. Green bacteria: insights into green bacterial evolution through genomic analyses. See Ref. 2 99–150
  14. Bryant DA, Liu Z, Li T, Zhao F, Garcia Costas AM. 14.  et al. 2012. Comparative and functional genomics of anoxygenic green bacteria from the taxa Chlorobi, Chloroflexi, and Acidobacteria. Functional Genomics and Evolution of Photosynthetic Systems Advances in Photosynthesis and Respiration, Vol. 33, ed. R Burnap, W Vermaas 47–102 Dordrecht, Neth.: Springer [Google Scholar]
  15. Camacho A, Walter XA, Picazo A, Zopfi J. 15.  2017. Photoferrotrophy: remains of an ancient photosynthesis in modern environments. Front. Microbiol. 8:323 [Google Scholar]
  16. Chan CS, Chan K-G, Tay Y-L, Chua Y-H, Goh KM. 16.  2015. Diversity of thermophiles in a Malaysian hot spring determined using 16S rRNA and shotgun metagenomic sequencing. Front. Microbiol. 6:177 [Google Scholar]
  17. Chen M.17.  2014. Chlorophyll modifications and their spectral extension in oxygenic photosynthesis. Annu. Rev. Biochem. 83:317–40 [Google Scholar]
  18. Chisholm SW.18.  2017. Prochlorococcus. Curr. Biol. 27:R447–48
  19. Chisholm SW, Olson RJ, Zettler ER, Goericke R, Waterbury JB, Selschmeyer NA. 19.  1988. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334340–43
  20. Choudhary M, Mackenzie C, Mouncey NJ, Kaplan S. 20.  1999. RsGDB, the Rhodobacter sphaeroides Genome Database. Nucl. Acids Res. 27:61–62 [Google Scholar]
  21. Choudhary M, Zanhua X, Fu YX, Kaplan S. 21.  2007. Genome analyses of three strains of Rhodobacter sphaeroides: evidence of rapid evolution of chromosome II. J. Bacteriol. 189:1914–21 [Google Scholar]
  22. Coleman ML, Sullivan MB, Martiny AC, Steglich C, Barry K. 22.  et al. 2006. Genomic islands and the ecology and evolution of Prochlorococcus. Science 311:1768–70 [Google Scholar]
  23. Coman C, Chiriac CM, Robeson MS, Ionescu C, Dragos N. 23.  et al. 2015. Structure, minerology, and microbial diversity of geothermal spring microbialites associated with a deep oil drilling in Romania. Front. Microbiol. 6:253 [Google Scholar]
  24. Crowe SA, Hahn AS, Morgan-Lang C, Thompson KJ, Simister RL. 24.  et al. 2017. Draft genome sequence of the pelagic photoferrotroph Chlorobium phaeoferrooxidans. Genome Announc 5:4–6 [Google Scholar]
  25. Crowe SA, Jones C, Katsev S, Magen C, O'Neill AH. 25.  et al. 2008. Photoferrotrophs thrive in an Archean Ocean analogue. PNAS 105:15938–43 [Google Scholar]
  26. Csotonyi JT, Swiderski J, Stackebrandt E, Yurkov V. 26.  2009. A new environment for aerobic anoxygenic phototrophic bacteria: biological soil crusts. Environ. Microbiol. Rep. 2:651–66 [Google Scholar]
  27. Csotonyi JT, Stackebrandt E, Swiderski J, Schumann P, Yurkov V. 27.  2011. An alphaproteobacterium capable of both aerobic and anaerobic anoxygenic photosynthesis but incapable of photoautotrophy: Charonomicrobium ambiphototrophicum, gen. nov., sp. nov. Photosynth. Res. 107:257–68 [Google Scholar]
  28. Csotonyi JT, Stackebrandt E, Swiderski J, Schumann P, Yurkov V. 28.  2011. Chromocurvus halotolerans gen. nov., sp. nov., a grammaproteobacterial obligately aerobic anoxygenic phototroph, isolated from a Canadian hypersaline spring. Arch. Microbiol. 193:573–82 [Google Scholar]
  29. Curtis PD.29.  2016. Essential genes predicted in the genome of Rubrivivax gelatinosus. J. Bacteriol 198:2244–50 [Google Scholar]
  30. Dahl C.30.  2017. Sulfur metabolism in phototrophic bacteria. See Ref. 59 27–66
  31. Di Rienzi SC, Sharon I, Wrighton KC, Koren O, Hug LA. 31.  et al. 2013. The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. eLife 2:e01102 [Google Scholar]
  32. Dubinina GA, Gorlenko VM. 32.  1975. New filamentous photosynthetic green bacteria containing gas vacuoles. Mikrobiologiya 44:511–17 [Google Scholar]
  33. Dvořák P, Casamatta D, Hašler, Jahodářová E, Norwich AR, Poulíčková A. 33.  2017. Diversity of cyanobacteria. See Ref. 59 3–46
  34. Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M. 34.  et al. 2002. The complete genome sequence of the green sulfur bacterium Chlorobium tepidum. PNAS 99:9509–14 [Google Scholar]
  35. Fischer WW, Hemp J, Johnson JE. 35.  2016. Evolution of oxygenic photosynthesis. Annu. Rev. Earth Planet. Sci. 44:647–83 [Google Scholar]
  36. Frigaard N-U, Bryant DA. 36.  2001. Chromosomal gene inactivation in the green sulfur bacterium Chlorobium tepidum by natural transformation. Appl. Environ. Microbiol. 67:2538–44 [Google Scholar]
  37. Frigaard N-U, Bryant DA. 37.  2008. Genomic insights into the sulfur metabolism of phototrophic sulfur bacteria. In. Sulfur Metabolism in Phototrophic Organisms Advances in Photosynthesis and Respiration, Vol. 27, ed. R Hell, C Dahl, DB Knaff, T Leustek 343–61 Dordrecht, Neth.: Springer [Google Scholar]
  38. Frigaard N-U, Dahl C. 38.  2009. Sulfur metabolism in phototrophic sulfur bacteria. Adv. Microb. Physiol. 54:103–200 [Google Scholar]
  39. Fuchs G.39.  2011. Alternative pathways of carbon dioxide fixation: insights into the early evolution of life?. Annu. Rev. Microbiol. 65:631–58 [Google Scholar]
  40. Fujita Y, Yamakawa H. 40.  2017. Biochemistry of chlorophyll biosynthesis in photosynthetic prokaryotes. See Ref. 59 67–122
  41. Gaisin VA, Kalashnikov AM, Grouzdev DS, Sukhacheva MV, Kruznetsov BB, Gorlenko VM. 41.  2017. Chloroflexus islandicus sp. nov., a thermophilic filamentous anoxygenic phototrophic bacterium from geyser Strokkur (Iceland). Int. J. Syst. Evol. Microbiol. 67:1381–86 [Google Scholar]
  42. Gan F, Bryant DA. 42.  2015. Adaptive and acclimative responses of the photosynthetic apparatus in cyanobacteria to far-red light. Environ. Microbiol. 17:3450–65 [Google Scholar]
  43. Gan F, Shen G, Bryant DA. 43.  2015. Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria. Life 5:4–24 [Google Scholar]
  44. Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA. 44.  2014. Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:1312–17 [Google Scholar]
  45. Garcia Costas AM, Liu Z, Tomsho LP, Schuster SC, Ward DM, Bryant DA. 45.  2012. Complete genome of “Candidatus Chloracidobacterium thermophilum,” a chlorophyll-based photoheterotroph belonging to the phylum Acidobacteria. Environ. Microbiol 14:177–90 [Google Scholar]
  46. Garcia Costas AM, Tsukatani Y, Rijpstra WIC, Schouten S, Welander PV. 46.  et al. 2012. Identification of the bacteriochlorophylls, carotenoids, quinones, lipids, and hopanoids of “Candidatus Chloracidobacterium thermophilum.”. J. Bacteriol. 194:1158–68 [Google Scholar]
  47. Garcia Costas AM, Tsukatani Y, Romberger SP, Oostergetel GT, Boekema EJ. 47.  et al. 2011. Ultrastructural analysis and identification of envelope proteins of “Candidatus Chloracidobacterium thermophilum” chlorosomes. J. Bacteriol. 193:6701–11 [Google Scholar]
  48. Gest H, Favinger JL. 48.  1983. Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a “new” form of bacteriochlorophyll. Arch. Microbiol. 136:11–16 [Google Scholar]
  49. Giovannoni SJ.49.  2017. SAR11 bacteria: the most abundant plankton in the oceans. Annu. Rev. Mar. Sci. 9:231–55 [Google Scholar]
  50. Gisriel C, Sarrou I, Ferlez B, Golbeck JH, Redding K, Fromme R. 50.  2017. Structure of a symmetric photosynthetic reaction center–photosystem. Science 27:eaan5611 [Google Scholar]
  51. Gomelsky M, Zeilstra-Ryalls JH. 51.  2013. The living genome of a purple nonsulfur photosynthetic bacterium. See Ref. 2 179–203
  52. Gomez Maqueo Chew A, Bryant DA. 52.  2007. Chlorophyll biosynthesis in bacteria: the origins of structural and functional diversity. Annu. Rev. Microbiol. 61:113–129 [Google Scholar]
  53. Gonzalez-Esquer CR, Smarda J, Rippka R, Axen SD, Guglielmi G. 53.  et al. 2016. Cyanobacterial ultrastructure in light of genomic sequence data. Photosynth. Res. 129:147–57 [Google Scholar]
  54. Gorlenko VM, Bryantseva IA, Kalashnikov AM, Gaisin VA, Sukhacheva MV. 54.  et al. 2014. Candidatus Chloroploca asiatica” gen. nov., sp. nov., a new mesophilic filamentous anoxygenic phototrophic bacterium. Microbiology 83:838–48 [Google Scholar]
  55. Groudev DS, Kuznetsov BB, Keppen OI, Krasil'nikova EN, Lebedeva NV, Ivanovsky RN. 55.  2015. Reconstruction of bacteriochlorophyll biosynthesis pathways in the filamentous anoxygenic phototrophic bacterium Oscillochloris trichoides DG-6 and evolution of anoxygenic phototrophs of the order Chloroflexales. Microbiology 161:120–30 [Google Scholar]
  56. Guiry MD.56.  2012. How many species of algae are there?. J. Phycol. 48:1057–63 [Google Scholar]
  57. Gupta RS, Chander P, George S. 57.  2013. Phylogenetic framework and molecular signatures for the class Chloroflexi and its different clades; proposal for division of the class Chloroflexi class. nov. 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 [Google Scholar]
  58. Ha PT, Lindemann SR, Shi L, Dohnalkova AC, Fredrickson JK. 58.  et al. 2017. Syntrophic anaerobic photosynthesis via direct interspecies electron transfer. Nat. Commun. 8:13924 [Google Scholar]
  59. Hallenbeck PC. 59.  2017. Modern Topics in the Phototrophic Prokaryotes: Environmental and Applied Aspects Berlin: Springer
  60. Hallenbeck PC, Grogger M, Mraz M, Veverka D. 60.  2016. Draft genome sequence of the photoheterotrophic Chloracidobacterium thermophilum strain OC1 found in a mat at Ojo Caliente. Genome Announc 4:e01570–15 [Google Scholar]
  61. Hanada S, Hiraishi A, Shimada K, Matsuura K. 61.  1995. Chloroflexus aggregans sp. nov., a filamentous phototrophic bacterium which forms dense cell aggregates by active gliding movement. Int. J. Syst. Bacteriol. 45:676–81 [Google Scholar]
  62. Hanada S, Takaichi S, Matsuura K, Nakamura K. 62.  2002. Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes. Int. J. Syst. Evol. Microbiol. 52:187–93 [Google Scholar]
  63. Heinnickel M, Golbeck JH. 63.  2007. Heliobacterial photosynthesis. Photosynth. Res. 92:35–53 [Google Scholar]
  64. Heising S, Richter L, Ludwig W, Schink B. 64.  1999. A phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a “Geospirillum” sp. strain. Arch. Microbiol. 172:116–24 [Google Scholar]
  65. Hemp J, Lücker S, Schott J, Pace LA, Johnson JE. 65.  et al. 2016. Genomics of a phototrophic nitrite oxidizer: insights into the evolution of photosynthesis and nitrification. ISME J 10:2669–78 [Google Scholar]
  66. Hernandez-Maldonado J, Sanchez-Sedillo B, Stoneburner B, Boren A, Miller L. 66.  et al. 2017. The genetic basis of anoxygenic photosynthetic arsenite oxidation. Environ. Microbiol. 19:130–41 [Google Scholar]
  67. Hiras J, Wu Y-W, Eichorst SA, Simmons BA, Singer SW. 67.  2016. Refining the phylum Chlorobi by resolving the phylogeny and metabolic potential of the representative of a deeply branching, uncultivated lineage. ISME J 10:833–45 [Google Scholar]
  68. Hirose S, Matsuura K, Haruta S. 68.  2016. Phylogenetically diverse aerobic anoxygenic phototrophic bacteria isolated from epilithic biofilms in Tama River, Japan. Microbes Environ 31:299–306 [Google Scholar]
  69. Ho M-Y, Gan F, Shen G, Bryant DA. 69.  2017. Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. II. Characterization of phycobiliproteins produced during acclimation to far-red light. Photosynth. Res. 131:187–202 [Google Scholar]
  70. Ho M-Y, Shen G, Canniffe DP, Zhao C, Bryant DA. 70.  2016. Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of Photosystem II. Science 353:aaf9178 [Google Scholar]
  71. Ho M-Y, Soulier NT, Canniffe DP, Shen G, Bryant DA. 71.  2017. Light regulation of cyanobacterial pigment and photosystem biosynthesis. Curr. Opin. Plant Biol. 37:24–33 [Google Scholar]
  72. Hohmann-Marriott MF, Blankenship RE. 72.  2011. Evolution of photosynthesis. Annu. Rev. Plant Biol. 62:515–48 [Google Scholar]
  73. Holo H, Sirevåg R. 73.  1986. Autotrophic growth and CO2 fixation of Chloroflexus aurantiacus. Arch. Microbiol 145:173–80 [Google Scholar]
  74. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ. 74.  et al. 2016. A new view of the tree of life. Nat. Microbiol. 1:16048 [Google Scholar]
  75. Hunter CN, Daldal F, Thurnauer MC, Beatty JT. 75.  2009. The Purple Phototrophic Bacteria Advances in Photosynthesis and Respiration 28 Berlin: Springer
  76. Igarashi N, Harada J, Nagashima S, Matsuura K, Shimada K, Nagashima KV. 76.  2001. Horizontal transfer of the photosynthesis gene cluster and operon rearrangement in purple bacteria. J. Mol. Evol. 52:333–41 [Google Scholar]
  77. Iino T, Mori K, Uchino Y, Nakagawa T, Harayama S, Suzuki K-I. 77.  2010. Ignavibacterium album gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from microbial mats at a terrestrial hot spring and proposal of Ignavibacteria classis nov., for a novel lineage at the periphery of green sulfur bacteria. Int. J. Syst. Evol. Microbiol. 60:1376–82 [Google Scholar]
  78. Imhoff JF.78.  2014. The family Chlorobiaceae. The Prokaryotes: Other Major Lineages of Bacteria and The Archaea E Rosenberg, EF DeLong, S Lory, E Stackebrandt, F Thompson 501–14 Berlin: Springer [Google Scholar]
  79. Imhoff JF.79.  2017. Anoxygenic phototrophic bacteria from extreme environments. See Ref. 59 427–80
  80. Imhoff JF.80.  2017. Diversity of anaerobic anoxygenic phototrophic purple bacteria. See Ref. 59 47–85
  81. Ivanovsky RN, Fal YI, Berg IA, Ugolkova NV, Krasilnikova EN. 81.  et al. 1999. Evidence for the presence of the reductive pentose phosphate cycle in a filamentous anoxygenic photosynthetic bacterium, Oscillochloris trichoides strain DG-6. Microbiology 145:1743–48 [Google Scholar]
  82. Johnson ZI, Zinser ER, Coe A, McNulty NP, Woodward EM, Chisholm SW. 82.  2006. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311:1737–40 [Google Scholar]
  83. Kadnikov VV, Mardanov AV, Podosokorskaya OA, Gavrilov SN, Kublanov IV. 83.  et al. 2013. Genomic analysis of Melioribacter roseus, facultatively anaerobic organotrophic bacterium representing a novel deep lineage within Bacteriodetes/Chlorobi group. PLOS ONE 8:e53047 [Google Scholar]
  84. Kálmán L, Williams JC, Allen JP. 84.  2008. Comparison of bacterial reaction centers and photosystem II. Photosynth. Res. 98:643–55 [Google Scholar]
  85. Kandori H.85.  2015. Ion-pumping microbial rhodopsins. Front. Mol. Biosci. 2:52 [Google Scholar]
  86. Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y. 86.  et al. 1996. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–36 [Google Scholar]
  87. Kaschner M, Loeschcke A, Krause J, Minh BQ, Heck A. 87.  et al. 2014. Discovery of the first light-dependent protochlorophyllide oxidoreductase in anoxygenic phototrophic bacteria. Mol. Microbiol. 93:1066–78 [Google Scholar]
  88. Kashtan N, Roggensack SE, Rodrigue S, Thompson JW, Biller SJ. 88.  et al. 2014. Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344:416–20 [Google Scholar]
  89. Keppen OI, Krasil'nikova EN, Lebedeva NV, Ivanovskiĭ RN. 89.  2013. Comparative study of metabolism of the purple photosynthetic bacteria grown in the light and in the dark under anaerobic and aerobic conditions. Microbiology 82:547–53 [Google Scholar]
  90. Keppen OI, Tourova TP, Kuznetsov BB, Ivanovsky RN, Gorlenko VM. 90.  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. 50:1529–37 [Google Scholar]
  91. Klappenbach JA, Pierson BK. 91.  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 [Google Scholar]
  92. Klatt CG, Bryant DA, Ward DM. 92.  2007. Comparative genomics provides evidence for the 3-hydroxypropionate autotrophic pathway in filamentous anoxygenic phototrophic bacteria and in hot spring microbial mats. Environ. Microbiol. 9:2067–78 [Google Scholar]
  93. Klatt CG, Liu Z, Ludwig M, Kühl M, Jensen SI. 93.  et al. 2013. Temporal metatranscriptomic patterning in phototrophic Chloroflexi inhabiting microbial mat in a geothermal spring. ISME J 7:1775–89 [Google Scholar]
  94. Klatt CG, Wood JM, Rusch DB, Bateson MM, Hamamura N. 94.  et al. 2011. Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential. ISME J 5:1262–78 [Google Scholar]
  95. Koblížek M.95.  2015. Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiol. Rev. 39:854–70 [Google Scholar]
  96. Koblížek M, Zeng Y, Horák A, Oborník M. 96.  2013. Regressive evolution of photosynthesis in the Roseobacter clade. See Ref. 2 385–405
  97. Komárek J.97.  2016. A polyphasic approach for the taxonomy of cyanobacteria: principles and applications. Eur J. Phycol. 51:346–53 [Google Scholar]
  98. Kopejtka K, Tomasch J, Zeng Y, Tichý M, Sorokin DY, Koblížek M. 98.  2017. Genomic analysis of the evolution of phototrophy among haloalkaliphilic Rhodobacterales. Gen. Biol. Evol 9:1950–62 [Google Scholar]
  99. Kuznetsov BB, Ivanovsky RN, Keppen OI, Sukhacheva MV, Bumazhkin BK. 99.  et al. 2011. Draft genome sequence of the anoxygenic filamentous phototrophic bacterium Oscillochloris trichoides subsp. DG-6. J. Bacteriol. 193:321–22 [Google Scholar]
  100. Lanyi JK.100.  2006. Proton transfers in the bacteriorhodopsin photocycle. Biochim. Biophys. Acta 1757:1012–18 [Google Scholar]
  101. Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S. 101.  et al. 2004. Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat. Biotechnol 22:55–61 [Google Scholar]
  102. Liu Z, Frigaard N-U, Vogl K, Iino T, Ohkuma M, Overmann J. 102.  et al. 2012. Complete genome of Ignavibacterium album, a metabolically versatile, flagellated, facultative anaerobe from the phylum Chlorobi. Front. Microbiol 3:185 [Google Scholar]
  103. Liu Z, Müller J, Li T, Alvey RM, Vogl K. 103.  et al. 2013. Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium “Chlorochromatium aggregatum.”. Genome Biol 14:R127 [Google Scholar]
  104. Liu Z, Klatt CG, Ludwig M, Rusch DB, Jensen SI. 104.  et al. 2012. Candidatus Thermochlorobacter aerophilum”: an aerobic chlorophotoheterotrophic member of the phylum Chlorobi defined by metagenomics and metatranscriptomics. ISME J 6:1869–82 [Google Scholar]
  105. Llirós M, García-Armisen T, Darchambeau F, Morana C, Triadó-Margarit X. 105.  et al. 2015. Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin. Sci. Rep. 5:13803 [Google Scholar]
  106. Llorens-Marès T, Liu Z, Allen LZ, Rusch DB, Craig MT. 106.  et al. 2016. Speciation and ecological success in dimly lit waters: horizontal gene transfer in a green sulfur bacteria bloom unveiled by metagenomic assembly. ISME J 11:201–11 [Google Scholar]
  107. López-López O, Knapik K, Cerdán M-E, González-Siso M-I. 107.  2015. Metagenomics of an alkaline hot spring in Galicia (Spain): microbial diversity analysis and screening for novel lipolytic enzymes. Front. Microbiol. 6:1291 [Google Scholar]
  108. Luo H, Moran MA. 108.  2014. Evolutionary ecology of the marine Roseobacter clade. Microbiol. Mol. Biol. Rev. 78:573–87 [Google Scholar]
  109. Madigan MT, Euzéby JP, Asao M. 109.  2010. Proposal of Heliobacteriaceae fam. nov. Int. J. Syst. Evol. Microbiol. 60:1709–10 [Google Scholar]
  110. Madigan MT, Vander Schaaf NA, Sattley WM. 110.  2017. The Chlorobiaceae, Chloroflexaceae and Heliobacteriaceae. See Ref. 59 139–61
  111. Martin WF, Bryant DA, Beatty JT. 111.  2017. A physiological perspective on the origin and evolution of photosynthesis. FEMS Microbiol. Rev. doi: 10.1093/femsre/fux056 [Google Scholar]
  112. Martínez-Pérez C, Mohr W, Löscher CR, Dekaezemacker J, Littmann S. 112.  et al. 2016. The small unicellular diazotrophic symbiont, UCYN-A, is a key player in the marine nitrogen cycle. Nat. Microbiol. 116163
  113. Miller SR, Strong AL, Jones KL, Ungerer MC. 113.  2009. Bar-coded pyrosequencing reveals shared bacterial community properties along the temperature gradients of two alkaline hot springs in Yellowstone National Park. Appl. Environ. Microbiol. 75:4565–72 [Google Scholar]
  114. Nabout JC, da Silva Rocha B, Carneiro FM, Sant'Anna CL. 114.  2013. How many species of Cyanobacteria are there? Using a discovery curve to predict the species number. Biodivers. Conserv. 22:2907–18 [Google Scholar]
  115. Nadson GA.115.  1906. The morphology of inferior algae. III. Chlorobium limicola Nads., the green chlorophyll bearing microbe. Bull. Jard. Bot. St. Petersb. 6:190 [Google Scholar]
  116. Nagashima S, Nagashima KVP. 116.  2013. Comparison of photosynthesis gene clusters retrieved from total genome sequences of purple bacteria. See Ref. 2 151–78
  117. Nakamura Y, Itoh T, Matsuda H, Gojobori T. 117.  2004. Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat. Genet. 36:760–66 [Google Scholar]
  118. Nowack E, Melkonian M, Glöckner G. 118.  2008. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr. Biol. 18:410–18 [Google Scholar]
  119. Oda Y, Larimer FW, Chain PSG, Malfatti S, Shin MV Vergez LM. 119.  et al. 2008. Multiple genome sequences reveal adaptations of a phototrophic bacterium to sediment microenvironments. PNAS 105:18543–48 [Google Scholar]
  120. Ohkubo S, Miyashita H. 120.  2017. A niche for cyanobacteria producing chlorophyll f within a microbial mat. ISME J 11:2368–78 [Google Scholar]
  121. Olsen MT, Nowack S, Wood JM, Becraft ED, LaButti K. 121.  et al. 2015. The molecular dimension of microbial species. 3. Comparative genomics of Synechococcus strains with different light responses and in situ diel transcription patterns of associated putative ecotypes in the Mushroom Spring microbial mat. Front. Microbiol. 6:604 [Google Scholar]
  122. Overmann J.122.  2006. The family Chlorobiaceae. The Prokaryotes M Dworkin, S Falkow, E Rosenberg, K-H Schleifer, E Stackebrandt 359–78 Berlin: Springer [Google Scholar]
  123. Overmann J.123.  2010. The phototrophic consortium “Chlorochromatium aggregatum”—a model for bacterial heterologous multicellularity. Adv. Exp. Med. Biol. 675:15–29 [Google Scholar]
  124. Overmann J, Garcia-Pichel F. 124.  2013. The phototrophic way of life. The Prokaryotes: Prokaryotic Communities and Ecophysiology E Rosenberg, EF DeLong, S Lory, E Stackebrandt, F Thompson 80–136 Berlin: Springer [Google Scholar]
  125. Pechter KB, Gallagher L, Pyles H, Manoil CS, Harwood CS. 125.  2016. Essential genome of the metabolically versatile alphaproteobacterium Rhodopseudomonas palustris. J. Bacteriol 198:867–76 [Google Scholar]
  126. Petersen J, Brinkmann H, Bunk B, Michael V, Päuker O, Pradalla S. 126.  2012. Think pink: photosynthesis, plasmids, and the Roseobacter clade. Environ. Microbiol. 14:2661–72 [Google Scholar]
  127. Pierson BK, Castenholz RW. 127.  1974. A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov. Arch. Microbiol. 100:5–24 [Google Scholar]
  128. Pierson BK, Giovannoni SJ, Stahl DA, Castenholz RW. 128.  1985. Heliothrix oregonensis, gen. nov., sp. nov., a phototrophic filamentous gliding bacterium containing bacteriochlorophyll a. Arch. Microbiol 142:164–67 [Google Scholar]
  129. Pinhassi J, DeLong EF, Béjà O, González JM, Pedrós-Alió C. 129.  2016. Marine bacterial and archaeal ion-pumping rhodopsins: genetic diversity, physiology, and ecology. Microbiol. Mol. Biol. Rev. 80:929–54 [Google Scholar]
  130. Podosokorskaya OA, Kadnikov VV, Gavrilov SN, Mardanov AV, Merkel AY. 130.  et al. 2013. Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae. Environ. Microbiol 15:1759–71 [Google Scholar]
  131. Pujalte MJ, Lucena T, Ruvira MA, Arahal DR, Macian MC. 131.  2014. The family Rhodobacteraceae. The Prokaryotes: Alphaproteobacteria and Betaproteobacteria E Rosenberg, EF DeLong, S Lory, E Stackebrandt, FL Thompson 439–512 Berlin: Springer [Google Scholar]
  132. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY. 132.  1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111:1–61 [Google Scholar]
  133. Sattley WM, Swingley WD. 133.  2013. Properties and evolutionary implications of the heliobacterial genome. See Ref. 2 67–97
  134. Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L. 134.  et al. 2009. Ecological genomics of marine picocyanobacteria. Microbiol. Mol. Biol. Rev. 73:249–99 [Google Scholar]
  135. Shiba T.135.  1991. Roseobacter litoralis gen. nov., sp. nov., and Roseobacter denitrificans sp. nov., aerobic pink-pigmented bacteria which contain bacteriochlorophyll a. Syst. Appl. Microbiol 14:140–45 [Google Scholar]
  136. Shiba T, Simidu U. 136.  1982. Erythrobacter longus gen. nov., sp. nov., an aerobic bacterium which contains bacteriochlorophyll a. Int. J. Syst. Evol. Microbiol 32:211–17 [Google Scholar]
  137. Shiba T, Simidu U, Taga N. 137.  1979. Distribution of aerobic bacteria which contain bacteriochlorophyll a. Appl. Environ. Microbiol 38:43–45 [Google Scholar]
  138. Shih PM, Hemp J, Ward LM, Matzke NJ, Fischer WW. 138.  2017. Crown group Oxyphotobacteria postdate the rise of oxygen. Geobiology 15:19–29 [Google Scholar]
  139. Shih PM, Wu D, Latifi A, Axen SD, Fewer DP. 139.  et al. 2013. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. PNAS 110:1053–58 [Google Scholar]
  140. Simmons SS, Isokpehi RD, Brown SD, McAllister DL, Hall CC. 140.  et al. 2011. Functional annotation analytics of Rhodopseudomonas palustris genomes. Bioinform. Biol. Insights 5:115–29 [Google Scholar]
  141. Simon M, Scheuner C, Meier-Kolthoff JP, Brinkhoff T, Wagner-Döbler I. 141.  et al. 2017. Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. ISME J 11:1483–99 [Google Scholar]
  142. Soo RM, Hemp J, Parks DH, Fischer WW, Hugenholtz P. 142.  2017. On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria. Science 355:1436–40 [Google Scholar]
  143. Soo RM, Skennerton CT, Sekiguchi Y, Imelfort M, Paech SJ. 143.  et al. 2014. An expanded genomic representation of the phylum Cyanobacteria. Genome Biol. Evol. 6:1031–45 [Google Scholar]
  144. Stirewalt VL, Michalowski CB, Löffelhardt W, Bohnert HJ. 144.  Bryant DA 1995. Nucleotide sequence of the cyanelle DNA from Cyanophora paradoxa. Plant Mol. Biol. Rep 13:327–32 [Google Scholar]
  145. Storelli N, Saad MM, Frigaard N-U, Perret X, Tonolla M. 145.  2014. Proteomic analysis of the purple sulfur bacterium “Candidatus Thiodictyon syntrophicum” strain Cad16T isolated from Lake Cadagno. EuPA Open Proteom 2:17–30 [Google Scholar]
  146. Swingley WD, Blankenship RE, Raymond J. 146.  2009. Evolutionary relationships among purple photosynthetic bacteria and the origin of proteobacterial photosynthetic systems. See Ref. 75 17–29
  147. Tahon G, Willems A. 147.  2017. Isolation and characterization of aerobic anoxygenic phototrophs from exposed soils from the Sør Rondane Mountains, East Antarctica. Syst. Appl. Microbiol. 40:357–69 [Google Scholar]
  148. Takaichi S.148.  2009. Distribution and biosynthesis of carotenoids. See Ref. 75 97–117
  149. Tang K-H, Barry K, Chertkov O, Dalin E, Han CS. 149.  et al. 2011. Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus. BMC Genom 12:334 [Google Scholar]
  150. Tang K-H, Tang Y-J, Blankenship RE. 150.  2011. Carbon metabolic pathways in phototrophic bacteria and their broader evolutionary implications. Front. Microbiol. 2:165 [Google Scholar]
  151. Tank M, Bryant DA. 151.  2015. Chloracidobacterium thermophilum gen. nov., sp. nov.: an anoxygenic microaerophilic chlorophotoheterotrophic acidobacterium. Int. J. Syst. Evol. Microbiol. 65:1426–30 [Google Scholar]
  152. Tank M, Bryant DA. 152.  2015. Nutrient requirements and growth physiology of the photoheterotrophic acidobacterium, Chloracidobacterium thermophilum. Front. Microbiol. 6:226 [Google Scholar]
  153. Tank M, Thiel V, Imhoff JF. 153.  2009. Phylogenetic relationship of phototrophic purple sulfur bacteria according to pufL and pufM genes. Int. Microbiol. 12:175–85 [Google Scholar]
  154. Tank M, Thiel V, Ward DM, Bryant DA. 154.  2017. A panoply of phototrophs: a photomicrographic overview of the thermophilic chlorophototrophs of the microbial mats of alkaline siliceous hots springs in Yellowstone National Park, WY, USA. See Ref. 59 87–137
  155. Thiel V, Drautz-Moses DI, Purbojati RW, Schuster SC, Lindemann S, Bryant DA. 155.  2017. Genome sequence of Prosthecochloris sp. strain HL-130-GSB, from the phylum Chlorobi. Genome Announc 5:e00538–17 [Google Scholar]
  156. Thiel V, Hamilton TL, Tomsho LP, Burhans R, Gay SC. 156.  et al. 2014. Draft genome sequence of a sulfide-oxidizing, autotrophic filamentous anoxygenic phototrophic bacterium, Chloroflexus sp. strain MS-G (Chloroflexi). Genome Announc 2:e00872–14 [Google Scholar]
  157. Thiel V, Hügler M, Ward DM, Bryant DA. 157.  2017. The dark side of the Mushroom Spring microbial mat: life in the shadow of chlorophototrophs. II. Metabolic functions of abundant community members predicted from metagenomics analyses. Front. Microbiol. 8:943 [Google Scholar]
  158. Thiel V, Tank M, Neulinger SC, Gehrmann L, Dorador C, Imhoff JF. 158.  2010. Unique communities of anoxygenic phototrophic bacteria in saline lakes of Salar de Atacama (Chile): evidence for a new phylogenetic lineage of phototrophic Gammaproteobacteria from pufLM gene analyses. FEMS Microbiol. Ecol. 74:510–22 [Google Scholar]
  159. Thiel V, Wood JM, Olsen MT, Tank M, Klatt CG. 159.  et al. 2016. The dark side of the Mushroom Spring microbial mat: life in the shadow of chlorophototrophs. I. Microbial diversity based on 16S rRNA amplicon and metagenome sequencing. Front. Microbiol. 7:919 [Google Scholar]
  160. Thompson AW, Foster RA, Krupke A, Carter BJ, Musat N. 160.  et al. 2012. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337:1546–50 [Google Scholar]
  161. Tsukatani Y, Romberger SP, Golbeck JH, Bryant DA. 161.  2012. Characterization of the oxygen-tolerant, homodimeric type-1 reaction centers of “Candidatus Chloracidobacterium thermophilum.”. J. Biol. Chem. 287:5720–32 [Google Scholar]
  162. van der Meer MTJ, Klatt CG, Wood J, Bryant DA, Bateson MM. 162.  et al. 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. 192:3033–42 [Google Scholar]
  163. van Gemerden H, Mas J. 163.  1995. Ecology of phototrophic sulfur bacteria. Anoxygenic Photosynthetic Bacteria Advances in Photosynthesis and Respiration, Vol. 2, ed. RE Blankenship, MT Madigan, CE Bauer 49–85 Dordrecht, Neth.: Kluwer [Google Scholar]
  164. Vogl K, Glaeser J, Pfannes KR, Wanner G, Overmann J. 164.  2006. Chlorobium chlorochromatii sp. nov., a symbiotic green sulfur bacterium isolated from the phototrophic consortium “Chlorochromatium aggregatum.”. Arch. Microbiol. 185:363–72 [Google Scholar]
  165. Wahlund TM, Woese CR, Castenholz RW. 165.  Madigan MT. 1991. A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov. Arch. Microbiol 156:81–90 [Google Scholar]
  166. Ward LM, Hemp J, Shih PM, McGlynn SE, Fischer WW.166.  2018. Evolution of phototrophy in the Chloroflexi phylum driven by horizontal gene transfer. Front. Microbiol 9:260 [Google Scholar]
  167. Weissgerber T, Dobler N, Polen T, Latus J, Stockdreher Y, Dahl C. 167.  2013. Genome-wide transcriptional profiling of the purple sulfur bacterium Allochromatium vinosum DSM 180T during growth on different reduced sulfur compounds. J. Bacteriol. 195:4231–45 [Google Scholar]
  168. Yurkov V, Hughes E. 168.  2013. Genes associated with the peculiar phenotypes of the aerobic anoxygenic phototrophs. See Ref. 2 327–58
  169. Yurkov V, Hughes E. 169.  2017. Aerobic anoxygenic phototrophs: four decades of mystery. See Ref. 59 193–214
  170. Zehr JP, Shilova IN, Farnelid HM, Carmen Muñoz-Marin M, Turk-Kubo KA. 170.  2016. Unusual marine unicellular symbiosis with the nitrogen-fixing cyanobacterium UCYN-A. Nat. Microbiol. 2:16214 [Google Scholar]
  171. Zeng Y, Baumbach J, Barbosa EGV, Azevedo V, Zhang C, Koblížek M. 171.  2016. Metagenomic evidence for the presence of phototrophic Gemmatimonadetes bacteria in diverse environments. Environ. Microbiol. Rep. 8:139–49 [Google Scholar]
  172. Zeng Y, Feng F, Medová H, Dean J, Koblížek M. 172.  2014. Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. PNAS 111:7795–800 [Google Scholar]
  173. Zeng Y, Koblížek M. 173.  2017. Phototrophic Gemmatimonadetes: a new “purple” branch on the Bacterial Tree of Life. See Ref. 59 163–92
  174. Zeng Y, Selyanin V, Lukes M, Dean J, Kaftan D. 174.  et al. 2015. Characterization of the microaerophilic, bacteriochlorophyll a-containing bacterium Gemmatimonas phototrophica sp. nov., and emended descriptions of the genus Gemmatimonas and Gemmatimonas aurantiaca. Int. J. Syst. Evol. Microbiol 65:2410–19 [Google Scholar]
  175. Zheng Q, Zhang R, Fogg PCM, Beatty JT, Wang Y, Jiao N. 175.  2012. Gain and loss of phototrophic genes revealed by comparison of two Citromicrobium bacterial genomes. PLOS ONE 7:e25790 [Google Scholar]
/content/journals/10.1146/annurev-arplant-042817-040500
Loading
/content/journals/10.1146/annurev-arplant-042817-040500
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
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