Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina
Edited by Elisabeth Gantt, University of Maryland, College Park, MD, and approved December 18, 2007
Abstract
Acaryochloris marina is a unique cyanobacterium that is able to produce chlorophyll d as its primary photosynthetic pigment and thus efficiently use far-red light for photosynthesis. Acaryochloris species have been isolated from marine environments in association with other oxygenic phototrophs, which may have driven the niche-filling introduction of chlorophyll d. To investigate these unique adaptations, we have sequenced the complete genome of A. marina. The DNA content of A. marina is composed of 8.3 million base pairs, which is among the largest bacterial genomes sequenced thus far. This large array of genomic data is distributed into nine single-copy plasmids that code for >25% of the putative ORFs. Heavy duplication of genes related to DNA repair and recombination (primarily recA) and transposable elements could account for genetic mobility and genome expansion. We discuss points of interest for the biosynthesis of the unusual pigments chlorophyll d and α-carotene and genes responsible for previously studied phycobilin aggregates. Our analysis also reveals that A. marina carries a unique complement of genes for these phycobiliproteins in relation to those coding for antenna proteins related to those in Prochlorococcus species. The global replacement of major photosynthetic pigments appears to have incurred only minimal specializations in reaction center proteins to accommodate these alternate pigments. These features clearly show that the genus Acaryochloris is a fitting candidate for understanding genome expansion, gene acquisition, ecological adaptation, and photosystem modification in the cyanobacteria.
Data Availability
Data deposition: The sequences reported in this paper have been deposited in the DNA Data Bank of Japan/European Molecular Biology Laboratory/GenBank databases [accession nos. CP000828 (the main chromosome of A. marina) and CP000838, CP000839, CP000840, CP000841, CP000842, CP000843, CP000844, CP000845, and CP000846 (the nine plasmids, pREB1–pREB9)].
ACKNOWLEDGMENTS.
We thank Paul Stothard for assistance with the generation of the circular genome and plasmid maps, Brendon Hill at 454 Life Sciences for coordination of 454 sequencing, and Jonathan Eisen for helpful discussions. This work was supported by the U.S. National Science Foundation Phototrophic Prokaryotes Sequencing Project Grant 0412824 and by a Grant-in-Aid for Creative Scientific Research (no. 17GS0314) from the Japanese Society for Promotion of Science. W.D.S. is funded by the Japanese Society for Promotion of Science Postdoctoral Fellowship for Foreign Researchers (no. P07141). M.C. is funded by an Australian Research Council Discovery Project (DP0665169). Partial support for the participation of P.C.C. and L.E.K. in this research was provided by a grant to Washington University from the Howard Hughes Medical Institute through the Undergraduate Biological Sciences Education Program.
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© 2008 by The National Academy of Sciences of the USA.
Data Availability
Data deposition: The sequences reported in this paper have been deposited in the DNA Data Bank of Japan/European Molecular Biology Laboratory/GenBank databases [accession nos. CP000828 (the main chromosome of A. marina) and CP000838, CP000839, CP000840, CP000841, CP000842, CP000843, CP000844, CP000845, and CP000846 (the nine plasmids, pREB1–pREB9)].
Submission history
Received: October 19, 2007
Published online: February 12, 2008
Published in issue: February 12, 2008
Change history
December 14, 2023: The SI Appendix has been updated.
Keywords
Acknowledgments
We thank Paul Stothard for assistance with the generation of the circular genome and plasmid maps, Brendon Hill at 454 Life Sciences for coordination of 454 sequencing, and Jonathan Eisen for helpful discussions. This work was supported by the U.S. National Science Foundation Phototrophic Prokaryotes Sequencing Project Grant 0412824 and by a Grant-in-Aid for Creative Scientific Research (no. 17GS0314) from the Japanese Society for Promotion of Science. W.D.S. is funded by the Japanese Society for Promotion of Science Postdoctoral Fellowship for Foreign Researchers (no. P07141). M.C. is funded by an Australian Research Council Discovery Project (DP0665169). Partial support for the participation of P.C.C. and L.E.K. in this research was provided by a grant to Washington University from the Howard Hughes Medical Institute through the Undergraduate Biological Sciences Education Program.
Notes
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0709772105/DC1.
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The authors declare no conflict of interest.
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