Open access
Announcement
30 April 2015

Complete Genome Sequence of Cyanobacterium Geminocystis sp. Strain NIES-3709, Which Harbors a Phycoerythrin-Rich Phycobilisome

ABSTRACT

The cyanobacterium Geminocystis sp. strain NIES-3709 accumulates a larger amount of phycoerythrin than the related NIES-3708 strain does. Here, we determined the complete genome sequence of the NIES-3709 strain. Our genome data suggest that the different copy number of rod linker genes for phycoerythrin leads to the different phycoerythrin contents between the two strains.

GENOME ANNOUNCEMENT

Certain cyanobacteria species modulate the composition of light-harvesting antenna proteins, phycoerythrin and phycocyanin, within the phycobilisome. This phenomenon is called complementary chromatic acclimation (CCA) (1, 2) and is conventionally classified as two types (3): type II species that modulate phycoerythrin content only, and type III species that modulate both phycoerythrin and phycocyanin content. Recent studies showed that type II species utilize the CcaS-CcaR photosensory system for CCA (4, 5), whereas type III species utilize the RcaE-RcaF-RcaC system (69). In the type II CCA, the CcaS-CcaR system directly regulates the expression of the rod linker gene of phycoerythrin and, in several species, the hydrophobic rod-core linker of phycocyanin (10).
The cyanobacterium Geminocystis sp. strain NIES-3709 accumulates a larger amount of phycoerythrin than the related NIES-3708 strain does, although the two strains are isolated from the same freshwater stream. We already reported the complete genome sequence of the NIES-3708 strain. To explore the molecular basis of the different cellular phycoerythrin contents in the two strains, we performed whole-genome sequencing of the NIES-3709 strain using the MiSeq (Illumina) system. An 800-bp paired-end library and an 8-kbp mate-pair library were prepared using the TruSeq DNA PCR-free sample preparation kit (Illumina) and Nextera mate-pair sample preparation kit (Illumina), respectively. The libraries were sequenced on the MiSeq instrument with the MiSeq reagent kit version 3 (600 cycles; Illumina). The reads were filtered using ShortReadManager, based on a 17-mer frequency (11). A total of eight million paired-end reads (209 Mbp) and 10 million mate-pair reads (150 Mbp) were assembled using Newbler version 2.8 (Roche), yielding 11 scaffolds and 156 large contigs (>1 kbp). The sequence gaps between the contigs were determined in silico using GenoFinisher and AceFileViewer (11). We succeeded in determining the complete genome sequence of Geminocystis sp. NIES-3709, which comprises one chromosome and 12 plasmids (total, 4,426,059 bp). The G+C content of the genome was calculated to be 33%. A total of 3,937 protein-coding genes, 6 rRNA genes, and 44 tRNA genes were predicted using the Rapid Annotations using Subsystems Technology (RAST) (12).
The CCA genes of the NIES-3709 strain consist of a CcaS-CcaR photosensory system and a putative light-regulated cpeE-cpeR operon, which is the same structure of the CCA genes of the NIES-3708 strain. The NIES-3709 strain harbors single copies of genes of the rod-core linker of phycocyanin (cpcG), core of phycocyanin (cpcB and cpcA), and core of phycoerythrin (cpeB and cpeA), whose copy numbers are also the same as those of the NIES-3708 strain. However, we found that the total copy number of rod linker genes of phycoerythrin (cpeC and cpeE) of the NIES-3709 strain is four, whereas that of the NIES-3708 strain is three. This difference may reflect the different rod structure of phycobilisome in the two strains that leads the different cellular phycoerythrin contents. Further biochemical analysis is required to explore this hypothesis.

Nucleotide sequence accession numbers.

The complete genome sequence of Geminocystis sp. NIES-3709 has been deposited in the DNA Data Bank of Japan under accession numbers AP014821 through AP014832.

ACKNOWLEDGMENTS

We thank Yoshiyuki Sakaki for encouraging this work.
This work was supported by a grant-in-aid for young scientists (B) (no. 25830130) from the Japan Society for the Promotion of Science (to Y.H.) and by research funds for young researchers from EIIRIS and the Toyohashi University of Technology.

REFERENCES

1.
Gutu A, Kehoe DM. 2012. Emerging perspectives on the mechanisms, regulation, and distribution of light color acclimation in cyanobacteria. Mol Plant 5:1–13.
2.
Kehoe DM, Gutu A. 2006. Responding to color: the regulation of complementary chromatic adaptation. Annu Rev Plant Biol 57:127–150.
3.
Tandeau de Marsac N. 1977. Occurrence and nature of chromatic adaptation in cyanobacteria. J Bacteriol 130:82–91.
4.
Hirose Y, Shimada T, Narikawa R, Katayama M, Ikeuchi M. 2008. Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein. Proc Natl Acad Sci USA 105:9528–9533.
5.
Hirose Y, Narikawa R, Katayama M, Ikeuchi M. 2010. Cyanobacteriochrome CcaS regulates phycoerythrin accumulation in Nostoc punctiforme, a group II chromatic adapter. Proc Natl Acad Sci USA 107:8854–8859.
6.
Hirose Y, Rockwell NC, Nishiyama K, Narikawa R, Ukaji Y, Inomata K, Lagarias JC, Ikeuchi M. 2013. Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle. Proc Natl Acad Sci USA 110:4974–4979.
7.
Kehoe DM, Grossman AR. 1996. Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273:1409–1412.
8.
Kehoe DM, Grossman AR. 1997. New classes of mutants in complementary chromatic adaptation provide evidence for a novel four-step phosphorelay system. J Bacteriol 179:3914–3921.
9.
Chiang GG, Schaefer MR, Grossman AR. 1992. Complementation of a red-light-indifferent cyanobacterial mutant. Proc Natl Acad Sci USA 89:9415–9419.
10.
Watanabe M, Semchonok DA, Webber-Birungi MT, Ehira S, Kondo K, Narikawa R, Ohmori M, Boekema EJ, Ikeuchi M. 2014. Attachment of phycobilisomes in an antenna-photosystem I supercomplex of cyanobacteria. Proc Natl Acad Sci USA 111:2512–2517.
11.
Ohtsubo Y, Maruyama F, Mitsui H, Nagata Y, Tsuda M. 2012. Complete genome sequence of Acidovorax sp. strain KKS102, a polychlorinated-biphenyl degrader. J Bacteriol 194:6970–6971.
12.
Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R. 2014. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 42:D206–D214.

Information & Contributors

Information

Published In

cover image Genome Announcements
Genome Announcements
Volume 3Number 230 April 2015
eLocator: 10.1128/genomea.00385-15

History

Received: 16 March 2015
Accepted: 20 March 2015
Published online: 30 April 2015

Contributors

Authors

Yuu Hirose
Department of Environmental and Life Sciences, Toyohashi University of Technology, Tempaku, Toyohashi, Aichi, Japan
Electronics-Inspired Interdisciplinary Research Institute (EIIRIS), Toyohashi University of Technology, Tempaku, Toyohashi, Aichi, Japan
Mitsunori Katayama
College of Industrial Technology, Nihon University, Narashino, Chiba, Japan
Yoshiyuki Ohtsubo
Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi, Japan
Naomi Misawa
Electronics-Inspired Interdisciplinary Research Institute (EIIRIS), Toyohashi University of Technology, Tempaku, Toyohashi, Aichi, Japan
Erica Iioka
Center for Omics and Bioinformatics, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba, Japan
Wataru Suda
Center for Omics and Bioinformatics, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba, Japan
Department of Microbiology and Immunology, Keio University School of Medicine, Shinjuku-ku, Tokyo, Japan
Kenshiro Oshima
Center for Omics and Bioinformatics, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba, Japan
Mitsumasa Hanaoka
Division of Applied Biological Chemistry, Graduate School of Horticulture, Chiba University, Matsudo, Chiba, Japan
Kan Tanaka
Chemical Resources Laboratory, Tokyo Institute of Technology, Midori-ku, Yokohama, Kanagawa, Japan
Toshihiko Eki
Department of Environmental and Life Sciences, Toyohashi University of Technology, Tempaku, Toyohashi, Aichi, Japan
Masahiko Ikeuchi
Department of Life Sciences (Biology), The University of Tokyo, Meguro, Tokyo, Japan
Yo Kikuchi
Graduate School of Advanced Science and Engineering, Waseda University, Shinjuku-ku, Tokyo, Japan
Makoto Ishida
Electronics-Inspired Interdisciplinary Research Institute (EIIRIS), Toyohashi University of Technology, Tempaku, Toyohashi, Aichi, Japan
Masahira Hattori
Center for Omics and Bioinformatics, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba, Japan

Notes

Address correspondence to Yuu Hirose, [email protected].

Metrics & Citations

Metrics

Note:

  • For recently published articles, the TOTAL download count will appear as zero until a new month starts.
  • There is a 3- to 4-day delay in article usage, so article usage will not appear immediately after publication.
  • Citation counts come from the Crossref Cited by service.

Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. For an editable text file, please select Medlars format which will download as a .txt file. Simply select your manager software from the list below and click Download.

View Options

Figures

Tables

Media

Share

Share

Share the article link

Share with email

Email a colleague

Share on social media

American Society for Microbiology ("ASM") is committed to maintaining your confidence and trust with respect to the information we collect from you on websites owned and operated by ASM ("ASM Web Sites") and other sources. This Privacy Policy sets forth the information we collect about you, how we use this information and the choices you have about how we use such information.
FIND OUT MORE about the privacy policy