The Primitive Thylakoid-Less Cyanobacterium Gloeobacter Is a Common Rock-Dwelling Organism

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Mareš, Jan ^a,b   Hrouzek, Pavel ^c   Kaňa, Radek ^c   Ventura, Stefano ^d   Strunecký, Otakar ^a,b   Komárek, Jiří ^a,b  

^a INSTITUTE OF BOTANY   (Czech Republic)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^c INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^d Sezione di Firenze   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPHYCOCYANIN; PHYCOBILIPROTEIN; PHYCOCYANIN; RIBOSOME RNA;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CYANOBACTERIUM; GENETIC VARIABILITY; GLOEOBACTER VIOLACEUS; MICROBIAL MORPHOLOGY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC PLASTICITY; PHYLOGENY; PROKARYOTES BY HABITAT; ROCK DWELLING CYANOBACTERIUM; SEQUENCE ALIGNMENT; SPECIES DISTRIBUTION; SPECIES HABITAT; THYLAKOID; UNINDEXED SEQUENCE; CLASSIFICATION; GENETICS; METABOLISM;

ALGAE; APHANOTHECE; CYANOBACTERIA; GLOEOBACTER; GLOEOBACTER VIOLACEUS; PROKARYOTA;

CYANOBACTERIA; PHYLOGENY; RNA, RIBOSOMAL; THYLAKOIDS;

EID: 84879145007     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066323     Document Type: Article

References (62)

1. Tomitani A, Knoll AH, Cavanaugh CM, Ohno T, (2006) The evolutionary diversification of cyanobacteria: Molecular-phylogenetic and paleontological perspectives. Proc Natl Acad Sci U S A 103: 5442-5447.
2. Blank CE, Sanchez-Baracaldo P, (2010) Timing of morphological and ecological innovations in the cyanobacteria- a key to understanding the rise in atmospheric oxygen. Geobiology 8: 1-23.
3. Koksharova OA, (2010) Application of molecular genetic and microbiological techniques in ecology and biotechnology of cyanobacteria. Microbiology 79: 721-734.
4. Schirrmeister BE, Antonelli A, Bagheri HC, (2011) The origin of multicellularity in cyanobacteria. BMC Evol Biol 11: 45.
5. Beck C, Knoop H, Axmann IM, Steuer R, (2012) The diversity of cyanobacterial metabolism: genome analysis of multiple phototrophic microorganisms. BMC Genomics 13: 56.
6. Rippka R, Waterbury J, Cohen-Bazire G, (1974) Cyanobacterium which lacks thylakoids. Arch Microbiol 100: 419-436.
7. Guglielmi G, Cohen-Bazire G, Bryant DA, (1981) The structure of Gloeobacter violaceus and its phycobilisomes. Arch Microbiol 129: 181-189.
8. Bryant DA, Cohen-Bazire G, Glazer AN, (1981) Characterization of the biliproteins of Gloeobacter violaceus chromophore content of a cyanobacterial phycoerythrin carrying phycourobilin chromophore. Arch Microbiol 129: 190-198.
9. Seo PS, Yokota A, (2003) The phylogenetic relationships of cyanobacteria inferred from 16S rRNA, gyrB, rpoC1 and rpoD1 gene sequences. J Gen Appl Microbiol 49: 191-203.
10. Hoffmann L, Kaštovský J, Komárek J, (2005) System of cyanoprokaryotes (cyanobacteria) - state in 2004. Arch Hydrobiol Suppl Algol Stud 117: 21.
11. Gupta RS, Mathews DW (2010) Signature proteins for the major clades of Cyanobacteria. BMC Evol Biol 10.
12. Criscuolo A, Gribaldo S, (2011) Large-Scale Phylogenomic Analyses Indicate a Deep Origin of Primary Plastids within Cyanobacteria. Mol Biol Evol 28: 3019-3032.
13. Turner S, Pryer KM, Miao VPW, Palmer JD, (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small submit rRNA sequence analysis. J Eukaryot Microbiol 46: 327-338.
14. Zhaxybayeva O, Gogarten JP, Charlebois RL, Doolittle WF, Papke RT, (2006) Phylogenetic analyses of cyanobacterial genomes: Quantification of horizontal gene transfer events. Genome Res 16: 1099-1108.
15. Gupta RS, (2009) Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. Int J Syst Evol Microbiol 59: 2510-2526.
16. Tsuchiya T, Takaichi S, Misawa N, Maoka T, Miyashita H, et al. (2005) The cyanobacterium Gloeobacter violaceus PCC 7421 uses bacterial-type phytoene desaturase in carotenoid biosynthesis. Febs Letters 579: 2125-2129.
17. Mimuro M, Tomo T, Tsuchiya T, (2008) Two unique cyanobacteria lead to a traceable approach of the first appearance of oxygenic photosynthesis. Photosynth Res 97: 167-176.
18. Williamson A, Conlan B, Hillier W, Wydrzynski T, (2011) The evolution of Photosystem II: insights into the past and future. Photosynth Res 107: 71-86.
19. Nakamura Y, Kaneko T, Sato S, Mimuro M, Miyashita H, et al. (2003) Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 10: 137-145.
20. Bernat G, Schreiber U, Sendtko E, Stadnichuk IN, Rexroth S, et al. (2012) Unique properties vs. common themes: The atypical cyanobacterium Gloeobacter violaceus PCC 7421 is capable of state transitions and blue-light-induced fluorescence quenching. Plant Cell Physiol 53: 528-542.
21. Inoue H, Tsuchiya T, Satoh S, Miyashita H, Kaneko T, et al. (2004) Unique constitution of photosystem I with a novel subunit in the cyanobacterium Gloeobacter violaceus PCC 7421. Febs Letters 578: 275-279.
22. Dreher C, Hielscher R, Prodohl A, Hellwig P, Schneider D, (2010) Characterization of two cytochrome b(6) proteins from the cyanobacterium Gloeobacter violaceus PCC 7421. J Bioenerg Biomembr 42: 517-526.
23. Mimuro M, Yokono M, Akimoto S, (2010) Variations in photosystem I properties in the primordial cyanobacterium Gloeobacter violaceus PCC 7421. Photochem Photobiol 86: 62-69.
24. Krogmann DW, Perez-Gomez B, Gutierrez-Cirlos EB, Chagolla-Lopez A, de la Vara LG, et al. (2007) The presence of multidomain linkers determines the bundle-shape structure of the phycobilisome of the cyanobacterium Gloeobacter violaceus PCC 7421. Photosynt Res 93: 27-43.
25. Yokono M, Akimoto S, Koyama K, Tsuchiya T, Mimuro M, (2008) Energy transfer processes in Gloeobacter violaceus PCC 7421 that possesses phycobilisomes with a unique morphology. Biochim Biophys Acta Bioenergetics1777: 55-65.
26. Bocquet N, Nury H, Baaden M, Le Poupon C, Changeux JP, et al. (2009) X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature 457: 111-114.
27. Weng Y, Yang LY, Corringer PJ, Sonner JM, (2010) Anesthetic sensitivity of the Gloeobacter violaceus proton-gated ion channel. Anesth Analg 110: 59-63.
28. Nury H, Van Renterghem C, Weng Y, Tran A, Baaden M, et al. (2011) X-ray structures of general anaesthetics bound to a pentameric ligand-gated ion channel. Nature 469: 428-431.
29. Cuzman OA, Ventura S, Sili C, Mascalchi C, Turchetti T, et al. (2010) Biodiversity of phototrophic biofilms dwelling on monumental fountains. Microb Ecol 60: 81-95.
30. Geitler L, (1927) Neue Blaualgen aus Lunz. Archiv für Protistenkunde 60: 440-448.
31. Golubic S, Campbell SE, (1979) Analogous microbial forms in recent subaerial habitats and in precambrian cherts - Gloeothece coerulea Geitler and Eosynechococcus moorei Hofmann. Precambrian Res 8: 201-217.
32. Hansgirg A, (1892) Prodromus der Algenflora von Böhmen. 2. Arch Naturwiss Landesdurchforsch Böhmen 8: 1-268.
33. Komárek J, Anagnostidis K (1999) Cyanoprokaryota. 1. Teil: Chroococcales. Süsswasserflora von Mitteleuropa. Heidelberg, Berlin: Spektrum Akademischer Verlag GmbH. 548.
34. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY, (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111: 1-61.
35. Statsoft Inc. (2012) STATISTICA (data analysis software system), version 9.1. www.statsoft.com.
36. Spurr AR, (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26: 31-43.
37. Yilmaz M, Phlips EJ, Tillett D, (2009) Improved methods for the isolation of cyanobacterial DNA from environmental samples. J Phycol 45: 517-521.
38. Wilmotte A, Van der Auwera G, Dewachter R, (1993) Structure of the 16S ribosomal-RNA of the thermophilic cyanobacterium Chlorogloeopsis HTF (Mastigocladus laminosus HTF) strain PCC7518, and phylogenetic analysis. FEBS Letters 317: 96-100.
39. Nübel U, Garcia-Pichel F, Muyzer G, (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Env Microbiol 63: 3327-3332.
40. Katoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT. In: Posada D, editor. Bioinformatics for DNA Sequence Analysis. Totowa, New Jersey: Humana Press. 39-64.
41. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
42. Stamatakis A, (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
43. Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sunderland, Massachusetts: Sinauer Associates.
44. Kaňa R, Prášil O, Komárek O, Papageorgiou GC, (2009) Govindjee (2009) Spectral characteristic of fluorescence induction in a model cyanobacterium, Synechococcus sp. (PCC 7942). Biochim Biophys Acta Bioenergetics 1787: 1170-1178.
45. Hauer T, (2008) Epilithic cyanobacterial flora of Mohelenská hadcová steppe Nature Reserve (western Moravia, Czech Republic) 70 years ago and now. Fottea 8: 129-132.
46. Halda J, Hauer T, Kociánová M, Mühlsteinová R, Řeháková K, et al. (2011) Biodiverzita cévnatých rostlin, lišejníků, sinic a řas na skalách s ledopády v Labském dole. Opera Corcontica 48: 45-67.
47. Johansen JR, Lowe RL, Carty S, Fučíková K, Olsen CE, et al. (2007) New algal species records for Great Smoky Mountains National Park, with an annotated checklist of all reported algal taxa for the park. Southeast Nat 6: 99-134.
48. Lamprinou V, Danielidis DB, Economou-Amilli A, Pantazidou A, (2012) Distribution survey of Cyanobacteria in three Greek caves of Peloponnese. Int J Speleol 41: 267-273.
49. Matuła J, Pietryka M, Richter D, Wojtuń B, (2007) Cyanoprokaryota and algae of Arctic terrestrial ecosystems in the Hornsund area, Spitsbergen. Pol Polar Res 28: 283-315.
50. Uher B, Kováčik L, (2002) Epilithic cyanobacteria of subaerial habitats in National Park Slovak Paradise (1998-2000). Bull Slov Bot Spoločn, Bratislava 24: 25-29.
51. Alvarez-Cobelas M, Gallardo T, (1988) Catalogo de las algas continentales Españolas v. Cyanophyceae Schaffner 1909. Acta Bot Malacit 13: 53-76.
52. Singh SM, Singh P, Thajuddin N, (2008) Biodiversity and distribution of cyanobacteria at Dronning Maud Land, East Antarctica. Acta Bot Malacit 33: 17-28.
53. Skinner S, Entwisle TJ, (2001) Non-marine algae of Australia: 1. Survey of colonial gelatinous blue-green macroalgae (Cyanobacteria). Telopea 9: 573-599.
54. Gutierrez-Cirlos EB, Perez-Gomez B, Krogmann DW, Gomez-Lojero C, (2006) The phycocyanin-associated rod linker proteins of the phycobilisome of Gloeobacter violaceus PCC 7421 contain unusually located rod-capping domains. Biochim Biophys Acta Bioenergetics 1757: 130-134.
55. Kondo K, Ochiai Y, Katayama M, Ikeuchi M, (2007) The membrane-associated CpcG2-phycobilisome in Synechocystis: A new photosystem I antenna. Plant Physiol 144: 1200-1210.
56. Takaichi S, Maoka T, Takasaki K, Hanada S, (2010) Carotenoids of Gemmatimonas aurantiaca (Gemmatimonadetes): identification of a novel carotenoid, deoxyoscillol 2-rhamnoside, and proposed biosynthetic pathway of oscillol 2,2-dirhamnoside. Microbiology 156: 757-763.
57. Foss P, Skulberg OM, Kilaas L, Liaaen-Jensen S, (1986) The carbohydrate moieties bound to the carotenoids myxol and oscillol and their chemosystematic applications. Phytochemistry 25: 1127-1132.
58. Rexroth S, Mullineaux CW, Ellinger D, Sendtko E, Rogner M, et al. (2011) The plasma membrane of the cyanobacterium Gloeobacter violaceus contains segregated bioenergetic domains. Plant Cell 23: 2379-2390.
59. Herrero A, Flores E (2008) The Cyanobacteria: Molecular biology, genomics and evolution. Wymondham, Norfolk, UK: Caister Academic. 484 p.
60. Wu DY, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, et al. (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462: 1056-1060.
61. Couradeau E, Benzerara K, Gerard E, Moreira D, Bernard S, et al. (2012) An early-branching microbialite cyanobacterium forms intracellular carbonates. Science 336: 459-462.
62. Cavalier-Smith T, (2002) The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int J Syst Evol Microbiol 52: 7-76.