Abstract

The oceanic cyanobacteria Prochlorococcus are globally important, ecologically diverse primary producers. It is thought that their viruses (phages) mediate population sizes and affect the evolutionary trajectories of their hosts. Here we present an analysis of genomes from three Prochlorococcus phages: a podovirus and two myoviruses. The morphology, overall genome features, and gene content of these phages suggest that they are quite similar to T7-like (P-SSP7) and T4-like (P-SSM2 and P-SSM4) phages. Using the existing phage taxonomic framework as a guideline, we examined genome sequences to establish “core” genes for each phage group. We found the podovirus contained 15 of 26 core T7-like genes and the two myoviruses contained 43 and 42 of 75 core T4-like genes. In addition to these core genes, each genome contains a significant number of “cyanobacterial” genes, i.e., genes with significant best BLAST hits to genes found in cyanobacteria. Some of these, we speculate, represent “signature” cyanophage genes. For example, all three phage genomes contain photosynthetic genes (psbA, hliP) that are thought to help maintain host photosynthetic activity during infection, as well as an aldolase family gene (talC) that could facilitate alternative routes of carbon metabolism during infection. The podovirus genome also contains an integrase gene (int) and other features that suggest it is capable of integrating into its host. If indeed it is, this would be unprecedented among cultured T7-like phages or marine cyanophages and would have significant evolutionary and ecological implications for phage and host. Further, both myoviruses contain phosphate-inducible genes (phoH and pstS) that are likely to be important for phage and host responses to phosphate stress, a commonly limiting nutrient in marine systems. Thus, these marine cyanophages appear to be variations of two well-known phages—T7 and T4—but contain genes that, if functional, reflect adaptations for infection of photosynthetic hosts in low-nutrient oceanic environments.

Highlights

  • Prochlorococcus is the numerically dominant primary producer in the temperate and tropical surface oceans [1]. These cyanobacteria are the smallest known photosynthetic organisms, yet are significant contributors to global photosynthesis [2,3] because they occur in high abundance throughout much of the world’s oceans

  • Cyanophages likely play a role in maintaining the extensive microdiversity within marine cyanobacteria [9,10] through keeping ‘‘competitive dominants’’ in check, as well as by carrying photosynthetic ‘‘host’’ genes [14,15,16] and mediating horizontal transfer of genetic material between cyanobacterial hosts [14]

  • What are the functions of the absent gene set? It includes genes that in T7 are involved in ligation of DNA fragments (1.3), inhibition of host RNA polymerase (RNAP) (2), interactions that are specific to the host cell envelope during virion formation (6.7, 13, 14), lysis events (3.5, 17.5), smallsubunit terminase activity (18), and unknown functions (5.7, 6.5, 18.5) [23]

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Summary

Introduction

Prochlorococcus is the numerically dominant primary producer in the temperate and tropical surface oceans [1]. It includes genes that in T7 are involved in ligation of DNA fragments (1.3), inhibition of host RNAP (2), interactions that are specific to the host cell envelope during virion formation (6.7, 13, 14), lysis events (3.5, 17.5), smallsubunit terminase activity (18), and unknown functions (5.7, 6.5, 18.5) [23] These same genes are absent in the marine podovirus genomes in the T7 supergroup (cyanophage P60, vibriophage VpV262, and roseophage SIO1; Table 3). P-SSM2 contains ORFs with high sequence similarity to host-encoded homologs of five genes involved in pyrimidine (pyrE) and purine (purH, purL, purM, and purN) biosynthesis (Table 5) These non-T4like genes might compensate for T4-like nucleotide metabolism and/or chaperone genes that are absent.

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