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

Abstract

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.The cyanobacterium Microcystis aeruginosa is a toxic, bloomforming bacteria found in eutrophic freshwaters throughout the world (12). The bacterium produces potent hepatotoxins, cyclic peptides called "microcystins," which inhibit eukaryotic protein phosphatase types 1 and 2A and can cause hepatocellular carcinoma (42,53,82). Blooms of M. aeruginosa can lead to the deaths of livestock and humans and pose serious problems for water management (12, 13).The mechanisms controlling bloom initiation and termination remain unclear; however, there have been many studies concerning the effects of environmental factors on M. aeruginosa growth (57). Recently, viral mortality of algae was recognized as one of the factors involved in the termination of algal blooms, including M. aeruginosa blooms (10,52,71,74,75). We previously reported culturing the lytic cyanophage Ma-LMM01 infecting the toxic M. aeruginosa strain NIES298 (81). Currently, M. aeruginosa NIES298 and Ma-LMM01 are the sole culture host/virus system to study interactions between a toxic cyanobacterium and its phage.Ma-LMM01 is a member of the Myoviridae family with a contractile tail (81), the distinctive morphological feature of this viral family. Myoviridae has at least six subgroups: T4-, P1-, P2-, Mu-, SPO1-, and H-like phages (23). These subgroups sh...

Polar freshwater cyanophage S-EIV1 represents a new widespread evolutionary lineage of phages

“…Of the five sequenced cyanophages that infect Microcystis aeruginosa (Yoshida et al, 2008), Phormidium foveolarum (Liu et al, 2007(Liu et al, , 2008, Planktothrix agardhii (Gao et al, 2012) and Synechococcus spp. (Dreher et al, 2011), only the myovirus S-CRM01 that infects the latter is related to myoviruses infecting marine Synechococcus spp.…”

Horizontal gene transfer of an entire metabolic pathway between a eukaryotic alga and its DNA virus

“…Viruses are known to carry a variety of host genes. Recent genomics studies are increasingly revealing interesting cases of HGT between prokaryotic phytoplankton (cyanobacteria) and their viruses (cyanophages) (Lindell et al 2004(Lindell et al , 2005Sullivan et al 2006;Yoshida et al 2008). From the observation of ''host-like'' genes in bacteriophage genomes, Hendrix and other authors proposed a modular theory of phage evolution, in which phages evolve through the stepwise acquisition of genes from diverse sources (Hendrix et al 2000;Brussow and Hendrix 2002).…”

The Distribution of a Phage-Related Insertion Sequence Element in the Cyanobacterium, Microcystis aeruginosa

“…The genome of Ma-LMM01 has 162,109 bp and contains 184 predicted protein-coding genes. The majority of the predicted genes have no detectable homologues in the present databases and the genome showed no co-linearity with previously sequenced genomes of other Myoviridae including cyanomyoviruses; and thus Ma-LMM01 was assigned as a member of a new lineage of the Myoviridae family (45). Unlike most of the marine cyanophages, Ma-LMM01 has no homologues of the photosynthesis genes.…”

“…Unlike most of the marine cyanophages, Ma-LMM01 has no homologues of the photosynthesis genes. Instead, the genome harbors several 'hostlike' genes including nblA involved in the maintenance of the photosynthetic reaction center (45). Of the 'host-like' genes in Ma-LMM01, a region of ca.…”

“…1,800 bp including ORF135 and ORF136 shows high nucleotide sequence similarity (82% identity) with a partial sequence of the Cyanothece sp. CCY0110 genome (GenBank: NZ_AAXW01000043) suggesting this region has experienced HGT between Ma-LMM01-related phages and cyanobacteria (45).…”