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Complete nucleotide sequence of the freshwater unicellular cyanobacterium Synechococcus elongatus PCC 6301 chromosome: gene content and organization

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Abstract

The entire genome of the unicellular cyanobacterium Synechococcus elongatus PCC 6301 (formerly Anacystis nidulans Berkeley strain 6301) was sequenced. The genome consisted of a circular chromosome 2,696,255 bp long. A total of 2,525 potential protein-coding genes, two sets of rRNA genes, 45 tRNA genes representing 42 tRNA species, and several genes for small stable RNAs were assigned to the chromosome by similarity searches and computer predictions. The translated products of 56% of the potential protein-coding genes showed sequence similarities to experimentally identified and predicted proteins of known function, and the products of 35% of the genes showed sequence similarities to the translated products of hypothetical genes. The remaining 9% of genes lacked significant similarities to genes for predicted proteins in the public DNA databases. Some 139 genes coding for photosynthesis-related components were identified. Thirty-seven genes for two-component signal transduction systems were also identified. This is the smallest number of such genes identified in cyanobacteria, except for marine cyanobacteria, suggesting that only simple signal transduction systems are found in this strain. The gene arrangement and nucleotide sequence of Synechococcus elongatus PCC 6301 were nearly identical to those of a closely related strain Synechococcus elongatus PCC 7942, except for the presence of a 188.6 kb inversion. The sequences as well as the gene information shown in this paper are available in the Web database, CYORF (http://www.cyano.genome.jp/).

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Abbreviations

PSI:

Photosystem I

PSII:

Photosystem II

HIP1:

Highly iterated palindrome

IS:

Insertion sequence

ORF:

Open reading frame

References

  • Aiba H, Nagaya M, Mizuno T (1993) Sensor and regulator proteins from the cyanobacterium Synechococcus species PCC 7942 that belong to the bacterial signal-transduction protein families: implication in the adaptive response to phosphate limitation. Mol Microbiol 8:81–91

    Article  CAS  PubMed  Google Scholar 

  • Allen MB (1952) The cultivation of Myxophyceae. Arch Mikrobiol 17:34–53

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Scaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Anandan S, Nalty MS, Cogdell DE, Golden SS (1996) Identification of two classes of transcriptional regulator genes in the cyanobacterium Synechococcus sp. strain PCC 7942. Arch Microbiol 166:58–63

    Article  CAS  PubMed  Google Scholar 

  • Banta AB, Haas ES, Brown JW, Pace NR (1992) Sequence of the ribonuclease P RNA gene from the cyanobacterium Anacystis nidulans. Nucleic Acids Res 20:911

    Article  CAS  PubMed  Google Scholar 

  • Bryant DA (ed) (1994) The molecular biology of cyanobacteria. Kluwer Academic Publishers, Dordrecht, Boston, London

  • Delaney SF, Carr NG (1975) Temporal genetic mapping in the blue-green alga Anacystis nidulans using ethyl methanesulphonate. J Gen Microbiol 88:259–268

    CAS  PubMed  Google Scholar 

  • Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, Barbe V, Duprat S, Galperin MY, Koonin EV, Le Gall F, Makarova KS, Ostrowski M, Oztas S, Robert C, Rogozin IB, Scanlan DJ, Tandeau de Marsac N, Weissenbach J, Wincker P, Wolf YI, Hess WR (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Aca Sci USA 100:10020–10025

    Article  CAS  Google Scholar 

  • Fukuta M, Wakasugi T, Sugiura M (1994) Nucleotide sequence of a putative sensory kinase gene from the cyanobacterium, Anacystis nidulans 6301. DNA Res 1:97–98

    Article  CAS  PubMed  Google Scholar 

  • Golden SS, Nalty MS, Cho DSC (1989) Genetic relationship of two highly studied Synechococcus strains designated Anacystis nidulans. J Bacteriol 171:24–29

    CAS  PubMed  Google Scholar 

  • Goto-Seki A, Shirokane M, Masuda S, Tanaka K, Takahashi H (1999) Specificity crosstalk among group 1 and group 2 sigma factors in the cyanobacterium Synechococcus sp. PCC7942: in vitro specificity and a phylogenetic analysis. Mol Microbiol 34:473–484

    Article  CAS  PubMed  Google Scholar 

  • Gupta A, Morby AP, Turner JS, Whitton BA, Robinson NJ (1993) Deletion within the metallothionein locus of cadmium-tolerant Synechococcus PCC 6301 involving a highly iterated palindrome (HIP1). Mol Microbiol 7:189–195

    Article  CAS  PubMed  Google Scholar 

  • Holtman CK, Chen Y, Sandoval P, Gonzales A, Nalty MS, Thomas TL, Youderian P, Golden SS (2005) High-throughput functional analysis of the Synechococcus elongatus PCC 7942 genome. DNA Res 12:103–115

    Article  CAS  PubMed  Google Scholar 

  • Ishiura M, Kutsuna S, Aoki S, Iwasaki H, Andersson CR, Tanabe A, Golden SS, Johnson CH, Kondo T (1998) Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science 281:1519–1523

    Article  CAS  PubMed  Google Scholar 

  • Iwasaki H, Williams SB, Kitayama Y, Ishiura M, Golden SS, Kondo T (2000) A KaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria. Cell 101:223–233

    Article  CAS  PubMed  Google Scholar 

  • Kaneko T, Matsubayashi T, Sugita M, Sugiura M (1996a) Physical and gene maps of the unicellular cyanobacterium Synechococcus sp. strain PCC6301 genome. Plant Mol Biol 31:193–201

    Article  CAS  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996b) 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 3:109–136

    Article  CAS  Google Scholar 

  • Kaneko T, Nakamura Y, Wolk CP, Kuritz T, Sasamoto S, Watanabe A, Iriguchi M, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kohara M, Matsumoto M, Matsuno A, Muraki A, Nakazaki N, Shimpo S, Sugimoto M, Takazawa M, Yamada M, Yasuda M, Tabata S (2001) Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8:205–213

    Article  CAS  PubMed  Google Scholar 

  • Kumano M, Tomioka N, Sugiura M (1983) The complete nucleotide sequence of a 23S rRNA gene from a blue-green alga, Anacystis nidulans. Gene 24:219–225

    Article  CAS  PubMed  Google Scholar 

  • Lau RH, Sapienza C, Doolittle WE (1980) Cyanobacterial plasmids: their widespread occurrence, and existence of regions of homology between plasmids in the same and different species. Mol Gen Genet 178:203–211

    Article  CAS  PubMed  Google Scholar 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  CAS  PubMed  Google Scholar 

  • Maeda S, Sugita C, Sugita M, Omata T (2006a) Latent nitrate transport activity of a novel sulfate permease-like protein of the cyanobacterium Synechococcus elongatus. J Biol Chem 281:5869–5876

    Article  CAS  Google Scholar 

  • Maeda S, Sugita C, Sugita M, Omata T (2006b) A new class of signal transducer in His-Asp phosphorelay systems. J Biol Chem 281:37868–37876

    Article  CAS  Google Scholar 

  • Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P, Atlas R (2001) An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 70:85–106

    Article  CAS  PubMed  Google Scholar 

  • Miller B, Heuser T, Zimmer W (2000) Functional involvement of a deoxy-d-xylulose 5-phosphate reductoisomerase gene harboring locus of Synechococcus leopoliensis in isoprenoid biosynthesis. FEBS Lett 481:221–226

    Article  CAS  PubMed  Google Scholar 

  • Mizuno T, Kaneko T, Tabata S (1996) Compilation of all genes encoding bacterial two-component signal transducers in the genome of the cyanobacterium, Synechocystis sp. strain PCC 6803. DNA Res 3:407–414

    Article  CAS  PubMed  Google Scholar 

  • Nagaya M, Aiba H, Mizuno T (1993) Cloning of a sensory-kinase-encoding gene that belongs to the two-component regulatory family from the cyanobacterium Synechococcus sp. PCC7942. Gene 131:119–124

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Kaneko T, Sato S, Ikeuchi M, Katoh H, Sasamoto S, Watanabe A, Iriguchi M, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2002) Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res 9:123–130

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Kaneko T, Sato S, Mimuro M, Miyashita H, Tsuchiya T, Sasamoto S, Watanabe A, Kawashima K, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shimpo S, Takeuchi C, Yamada M, Tabata S (2003) Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 10:137–145

    Article  CAS  PubMed  Google Scholar 

  • Palenik B, Brahamsha B, Larimer FW, Land M, Hauser L, Chain P, Lamerdin J, Regala W, Allen EE, McCarren J, Paulsen I, Dufresne A, Partensky F, Webb EA, Waterburg J (2003) The genome of a motile marine Synechococcus. Nature 424:1037–1042

    Article  CAS  PubMed  Google Scholar 

  • Palenik B, Ren Q, Dupont CL, Myers GS, Heidelberg JF, Badger JH, Madupu R, Nelson WC, Brinkac LM, Dodson RJ, Durkin AS, Daugherty SC, Sullivan SA, Khouri H, Mohamoud Y, Halpin R, Paulsen IT (2006) Genome sequence of Synechococcus CC9311: Insights into adaptation to a coastal environment. Proc Natl Acad Sci USA 103:13555–13559

    Article  CAS  PubMed  Google Scholar 

  • Paquin B, Kathe SD, Nierzwicki-Bauer SA, Shub DA (1997) Origin and evolution of group I introns in cyanobacterial tRNA genes. J Bacteriol 179:6798–6806

    CAS  PubMed  Google Scholar 

  • Rebière MC, Castets AM, Houmard J, Tandeau de Marsac N (1986) Plasmid distribution among unicellular and filamentous cyanobacteria: occurrence of large and mega-plasmids. FEMS Microbiol Lett 37:269–275

    Article  Google Scholar 

  • Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgrn NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI, Land M, Lindell D, Post AF, Regala W, Shah M, Shaw SL, Steglich C, Sullivan MB, Ting CS, Tolonen A, Webb EA, Zinser ER, Chisholm SW (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042–1047

    Article  CAS  PubMed  Google Scholar 

  • Schmitz O, Katayama M, Williams SB, Kondo T, Golden SS (2000) CikA, a bacteriophytochrome that resets the cyanobacterial circadian clock. Science 289:765–768

    Article  CAS  PubMed  Google Scholar 

  • Schwarz R, Grossman AR (1998) A response regulator of cyanobacteria integrates diverse environmental signals and is critical for survival under extreme conditions. Proc Natl Acad Sci USA 95:11008–11013

    Article  CAS  PubMed  Google Scholar 

  • Shestakov SV, Khyen NT (1970) Evidence for genetic transformation in blue-green alga Anacystis nidulans. Mol Gen Genet 107:372–375

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Tomioka N, Yamada C, Sugiura M (1982) Cloning and characterization of a plasmid DNA from Anacystis nidulans 6301. Gene 19:221–224

    Article  CAS  PubMed  Google Scholar 

  • Sugita M, Luo L, Ohta M, Itadani H, Matsubayashi T, Sugiura M (1995) Genes encoding the group I intron-containing tRNALeu and subunit L of NADH dehydrogenase from the cyanobacterium Synechococcus PCC 6301. DNA Res 2:71–76

    Article  CAS  PubMed  Google Scholar 

  • Sugita M, Tsudzuki T, Sugita C, Ishiura M, Ogata K, Jikuya H, Takano J, Sugiura M (2001) Genome analysis of Synechococcus sp. strain PCC6301. In: PS2001 Proceedings: 12th International Congress on Photosynthesis, S41–009, CSIRO Publishing, Melbourne (CD-ROM)

  • Takai N, Nakajima M, Oyama T, Kito R, Sugita C, Sugita M, Kondo T, Iwasaki H (2006) A KaiC-associating SasA-RpaA two-component regulatory system as a major circadian timing mediator in cyanobacteria. Proc Natl Acad Sci USA 103:12109–12114

    Article  CAS  PubMed  Google Scholar 

  • Thomas C, Andersson CR, Canales SR, Golden SS (2004) PsfR, a factor that stimulates psbAI expression in the cyanobacterium Synechococcus elongatus PCC 7942. Microbiol 150:1031–1040

    Article  CAS  Google Scholar 

  • Tomioka N (1983) Effect of culture conditions on hydrogenase activity and H2-supported nitrogenase activity in some blue-green algae. J Sci Hiroshima Univ Ser B, Div 2 (Bot) 18:173–190

    Google Scholar 

  • Tomioka N, Shinozaki K, Sugiura M (1981) Molecular cloning and characterization of ribosomal RNA genes from a blue-green alga, Anacystis nidulans. Mol Gen Genet 184:359–363

    Article  CAS  Google Scholar 

  • Tomioka N, Sugiura M (1983) The complete nucleotide sequence of a 16S ribosomal RNA gene from a blue-green alga, Anacystis nidulans. Mol Gen Genet 191:46–50

    Article  CAS  PubMed  Google Scholar 

  • Van der Plas J, Oosterhoff-Teertstra R, Borrias M, Weisbeek P (1992) Identification of replication and stability functions in the complete nucleotide sequence of plasmid pUH24 from the cyanobacterium Synechococcus sp. PCC 7942. Mol Microbiol 6:653–664

    Article  PubMed  Google Scholar 

  • van Waasbergen LG, Dolganov N, Grossman AR (2002) nblS, a gene involved in controlling photosynthesis-related gene expression during high light and nutrient stress in Synechococcus elongatus PCC 7942. J Bacteriol 184:2481–2490

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T, Sugiura M, Sugita M (1997) A novel small stable RNA, 6Sa RNA, from the cyanobacterium Synechococcus sp. strain PCC6301. FEBS Lett 416:302–306

    Article  CAS  PubMed  Google Scholar 

  • Watanabe T, Sugita M, Sugiura M (1998) Identification of 10Sa RNA (tmRNA) homologues from the cyanobacterium Synechococcus sp. strain PCC6301 and related organisms. Biochim Biophys Acta 1396:97–104

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by Grant-in-Aid for Scientific Research on Priority Area “Genome Biology” (13206027 to MS) of the Ministry of Education, Sports, Science, Culture and Technology, Japan. We thank Tohru Matsubayashi, Takakazu Kaneko and Takahiko Tsudzuki, for valuable advises, and Nikolay Tzverkov, Makoto Suzuki, Tsuneo Fujishiro, Atsuko Tubai, Misato Ogura, Harumi Yokota, Yuriko Hara for technical assistance. We also thank Dr. Kan Tanaka, Prof. Masahiko Ikeuchi (The University of Tokyo), Prof. Ken Nishikawa, Dr. Yoshiaki Minesaki (National Institute of Genetics, Mishima), Dr. Shin-ichi Maeda, Prof. Takao Kondo (Nagoya University), Dr. Hideo Iwasaki (Wasada University) for annotation of protein-encoding genes, and an anonymous referee for valuable comments on the manuscript.

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Authors and Affiliations

  1. Center for Gene Research, Nagoya University, Chikusa, Nagoya, 464-8602, Japan

    Chieko Sugita & Mamoru Sugita

  2. Life Science Business Unit, Shimadzu Co., Nakagyo-ku, Kyoto, 604-8511, Japan

    Koretsugu Ogata, Masamitsu Shikata & Jun Takano

  3. Bio-Architecture Center, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka, 812-8581, Japan

    Hiroyuki Jikuya

  4. Bioinformatics Center, Institute for Chemical Research, Kyoto University, Uji, Kyoto, 611-0011, Japan

    Miho Furumichi & Minoru Kanehisa

  5. Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, 464-8601, Japan

    Tatsuo Omata

  6. Graduate School of Natural Sciences, Nagoya City University, Nagoya, 467-8501, Japan

    Masahiro Sugiura

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  1. Chieko Sugita
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  2. Koretsugu Ogata
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  3. Masamitsu Shikata
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  10. Mamoru Sugita
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Correspondence to Mamoru Sugita.

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Sugita, C., Ogata, K., Shikata, M. et al. Complete nucleotide sequence of the freshwater unicellular cyanobacterium Synechococcus elongatus PCC 6301 chromosome: gene content and organization. Photosynth Res 93, 55–67 (2007). https://doi.org/10.1007/s11120-006-9122-4

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  • DOI: https://doi.org/10.1007/s11120-006-9122-4

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