Ecology, diversity and comparative genomics of oceanic cyanobacterial viruses

Abstract

The marine cyanobacteria Prochlorococcus and Synechococcus are numerically dominant primary producers in the oceans. Each genera consists of multiple physiologically and genetically distinct groups (termed "ecotypes" in Prochlorococcus). Cyanobacterial viruses (cyanophages) that infect Synechococcus are abundant (to 104-106 phage ml-1) in the oceans and calculations suggest that they play a small but significant role in host mortality. Cyanophages are also thought to shape their host populations through regulation of sub-populations and through transfer of genes. Here we describe the isolation of Prochlorococcus cyanophages and the assembly of a culture collection established using a broadly diverse suite of Prochlorococcus and Synechococcus hosts. The collection contains three morphological families, Myoviridae, Podoviridae and Siphoviridae, known to infect marine bacteria and cyanobacteria. Host strains of similar ecotypes often yielded cyanophages of the same family. Host-range analyses of these isolates demonstrated varying levels of specificity among the different morphological types, ranging from infection of a single strain to infection across ecotypes and even across both cyanobacterial genera. Strain-specific cyanophage titers were low in open ocean waters where total cyanobacterial abundances were high, suggesting low phage titers might be a feature of open oceans. Investigations of the underlying cause(s) of this trend require culture-independent assays for quantifying phage that infect particular hosts.

(cont.) We used the phage g20 gene, which encodes the portal protein, to examine the diversity of Myoviridae isolates and found that g20 sequences from our isolates had high similarity to those from other cultured isolates, but not to six phylogenetic clusters of environmental g20 sequences that lacked cultured representatives. Three Prochlorococcus cyanophage genomes were sequenced and analysis of these genomes show striking similarity to the well-studied T7- and T4-like phages, but additionally suggest that these Prochlorococcus cyanophages are modified for infection of photosynthetic hosts, that live in nutrient-limited environments. All three cyanophage genomes contain, among other novel genes of interest, photosynthetic genes that are full-length, conserved, and clustered in the genome suggesting they are functional during infection. Phylogenetic inference suggests that some of these genes were horizontally transferred between host and phage influencing the evolution and ecology of both host and phage.