A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans

Abstract

Viruses infecting bacteria (phages) are thought to greatly impact microbial population dynamics as well as the genome diversity and evolution of their hosts. Here we report on the discovery of a novel lineage of tailed dsDNA phages belonging to the family Myoviridae and describe its first representative, S-TIM5, that infects the ubiquitous marine cyanobacterium, Synechococcus. The genome of this phage encodes an entirely unique set of structural proteins not found in any currently known phage, indicating that it uses lineage-specific genes for virion morphogenesis and represents a previously unknown lineage of myoviruses. Furthermore, among its distinctive collection of replication and DNA metabolism genes, it carries a mitochondrial-like DNA polymerase gene, providing strong evidence for the bacteriophage origin of the mitochondrial DNA polymerase. S-TIM5 also encodes an array of bacterial-like metabolism genes commonly found in phages infecting cyanobacteria including photosynthesis, carbon metabolism and phosphorus acquisition genes. This suggests a common gene pool and gene swapping of cyanophage-specific genes among different phage lineages despite distinct sets of structural and replication genes. All cytosines following purine nucleotides are methylated in the S-TIM5 genome, constituting a unique methylation pattern that likely protects the genome from nuclease degradation. This phage is abundant in the Red Sea and S-TIM5 gene homologs are widespread in the oceans. This unusual phage type is thus likely to be an important player in the oceans, impacting the population dynamics and evolution of their primary producing cyanobacterial hosts.

Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent

“…Our analysis does not include the highly divergent non-T4-like cyanomyovirus described recently by Sabehi et al (2012) as it was not available when we began the work. We compared the frequencies of genes in cyanomyovirus genomes in three marine environments to identify genes that the environments have in common and genes that distinguish them.…”

Species concepts and speciation factors in cyanobacteria, with connection to the problems of diversity and classification

“…In terms of cyanobacteria, it has been further suggested that most HGT are mediated by phages (cyanophages) (e.g. Sullivan et al 2010;Sabehi et al 2012). These phages often contain genes important in photosynthesis (Zheng et al 2014).…”

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

“…Similarly, most cyanophages have been isolated using a few strains of Synechococcus spp. ; however, a previously unknown lineage of myoviruses (S-TIM5) was isolated from the Red Sea using a different Synechococcus strain (Sabehi et al, 2012). Clearly, there is enormous potential to isolate representatives of previously unknown groups of viruses by screening untested taxa of host organisms.…”

“…Host-range studies have revealed that some cyanophages have broad host ranges and are able to infect strains that are distantly related (Suttle and Chan, 1993;Waterbury and Valois, 1993) or that even belong to different genera (Sullivan et al, 2003). Nonetheless, the mosaic architecture of phage genomes, including structural genes that result in similar morphology but that appear to have a different evolutionary origin (Sabehi et al, 2012), increasingly call into question the use of a Linnaeanbased hierarchical classification, including morphology, as a basis for classifying phage (Lawrence et al, 2002;Nelson, 2004).…”

“…( Chen and Lu, 2002;Mann et al, 2005;Millard et al, 2009;Sullivan et al, 2010;Huang et al, 2012;Sabehi et al, 2012) and Prochlorococcus spp. (Sullivan et al, 2005(Sullivan et al, , 2009Sullivan et al, 2010;Labrie et al, 2013), as well as one from a myovirus that infects both genera (Weigele et al, 2007).…”