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Ma-LMM01 Infecting Toxic Microcystis aeruginosa Illuminates Diverse Cyanophage Genome Strategies

Takashi Yoshida,^1*, Keizo Nagasaki,^2, Yukari Takashima,^1, Yoko Shirai,² Yuji Tomaru,² Yoshitake Takao,² Shigetaka Sakamoto,³ Shingo Hiroishi,¹ and Hiroyuki Ogata^4*,

Department of Marine Bioscience, Fukui Prefectural University, 1-1 Gakuencho, Obama, Fukui 917-0003, Japan,¹ Harmful Algal Bloom Division, National Research Institute of Inland Sea, Fisheries Research Agency, 2-17-5 Maruishi, Hatsukaichi, Hiroshima 739-0452, Japan,² Holonics, 4F Ohkubo-Daini-Building, 85 Soeji, Numazu, Shizuoka 410-0803, Japan,³ Information Génomique et Structurale, CNRS-UPR2589, IBSM, Parc Scientifique de Luminy, 163 Avenue de Luminy, Case 934, 13288 Marseille Cedex 9, France⁴

Received 24 September 2007/ Accepted 29 November 2007

Cyanobacteria and their phages are significant microbial components of the freshwater and marine environments. We identified a lytic phage, Ma-LMM01, infecting Microcystis aeruginosa, a cyanobacterium that forms toxic blooms on the surfaces of freshwater lakes. Here, we describe the first sequenced freshwater cyanomyovirus genome of Ma-LMM01. The linear, circularly permuted, and terminally redundant genome has 162,109 bp and contains 184 predicted protein-coding genes and two tRNA genes. The genome exhibits no colinearity with previously sequenced genomes of cyanomyoviruses or other Myoviridae. The majority of the predicted genes have no detectable homologues in the databases. These findings indicate that Ma-LMM01 is a member of a new lineage of the Myoviridae family. The genome lacks homologues for the photosynthetic genes that are prevalent in marine cyanophages. However, it has a homologue of nblA, which is essential for the degradation of the major cyanobacteria light-harvesting complex, the phycobilisomes. The genome codes for a site-specific recombinase and two prophage antirepressors, suggesting that it has the capacity to integrate into the host genome. Ma-LMM01 possesses six genes, including three coding for transposases, that are highly similar to homologues found in cyanobacteria, suggesting that recent gene transfers have occurred between Ma-LMM01 and its host. We propose that the Ma-LMM01 NblA homologue possibly reduces the absorption of excess light energy and confers benefits to the phage living in surface waters. This phage genome study suggests that light is central in the phage-cyanobacterium relationships where the viruses use diverse genetic strategies to control their host's photosynthesis.

Published ahead of print on 7 December 2007.

T. Yoshida, K. Nagasaki, Y. Takashima, and H. Ogata contributed equally to this study.

This article has been cited by other articles:

• Yoshida, M., Yoshida, T., Kashima, A., Takashima, Y., Hosoda, N., Nagasaki, K., Hiroishi, S. (2008). Ecological Dynamics of the Toxic Bloom-Forming Cyanobacterium Microcystis aeruginosa and Its Cyanophages in Freshwater. Appl. Environ. Microbiol. 74: 3269-3273 [Abstract] [Full Text]