Stumbling across the Same Phage: Comparative Genomics of Widespread Temperate Phages Infecting the Fish Pathogen Vibrio anguillarum

Abstract

Nineteen Vibrio anguillarum-specific temperate bacteriophages isolated across Europe and Chile from aquaculture and environmental sites were genome sequenced and analyzed for host range, morphology and life cycle characteristics. The phages were classified as Siphoviridae with genome sizes between 46,006 and 54,201 bp. All 19 phages showed high genetic similarity, and 13 phages were genetically identical. Apart from sporadically distributed single nucleotide polymorphisms (SNPs), genetic diversifications were located in three variable regions (VR1, VR2 and VR3) in six of the phage genomes. Identification of specific genes, such as N6-adenine methyltransferase and lambda like repressor, as well as the presence of a tRNAArg, suggested a both mutualistic and parasitic interaction between phages and hosts. During short term phage exposure experiments, 28% of a V. anguillarum host population was lysogenized by the temperate phages and a genomic analysis of a collection of 31 virulent V. anguillarum showed that the isolated phages were present as prophages in >50% of the strains covering large geographical distances. Further, phage sequences were widely distributed among CRISPR-Cas arrays of publicly available sequenced Vibrios. The observed distribution of these specific temperate Vibriophages across large geographical scales may be explained by efficient dispersal of phages and bacteria in the marine environment combined with a mutualistic interaction between temperate phages and their hosts which selects for co-existence rather than arms race dynamics.

Prevalence of genetically similarFlavobacterium columnarephages across aquaculture environments reveals a strong potential for pathogen control

“…In addition, the isolated phage genomes were highly similar to the previously described phages in our dataset, as also reported earlier with phages infecting the genetic group C bacteria (Laanto et al, 2017). Comparable findings have been reported also in other phage-bacterium systems, for example with aquaculture pathogens F. psychrophilum and Vibrio anquillarum (Castillo and Middelboe, 2016;Kalatzis et al, 2017), where genetically similar phages were widely distributed across large temporal and spatial scales. Phages infecting flavobacterial species are known to regulate the genetic and phenotypic diversity of their bacterial hosts.…”

Marine Viruses: Key Players in Marine Ecosystems

“…Later, a worldwide distribution of a virus infecting the picophytoplankton Micromonas pusilla was reported by Cottrell and Suttle [ 34 ], suggesting that viruses are efficiently spread in the marine environment. This is supported by the study by Kalatzis et al [ 28 ], which demonstrates that H20-like vibriophages infecting the fish pathogen Vibrio anguillarum are globally distributed either as free phages or as prophages inside bacterial genomes. The authors argue that selection for co-existence, rather than arms race dynamics, might explain the global distribution of near-identical H20-like bacteriophages and their prevalence as prophages in Vibrio genomes.…”

“…The large number of unknown viral populations in the marine metagenome emphasizes the need for further isolation, characterization and sequencing of specific marine viruses. This special issue presents several new marine viruses of eukaryotes ( Prymnesium parvum , [ 26 ]) and bacteria ( Shewanella , [ 27 ], Vibrio anguillarum [ 28 ] and Dinoroseobacter shibae [ 29 ]), adding to the rapidly growing database of genome-sequenced and characterized marine viruses. Several auxiliary metabolic genes and other functional genes were identified in the phage genomes, suggesting a mutual benefit for both phage and host that could potentially be disseminated to other hosts by horizontal gene transfer ( Figure 1 ).…”

Bacteriophage Interactions with Marine Pathogenic Vibrios: Implications for Phage Therapy

“…In a recent study, several temperate V. anguillarum -specific bacteriophages, designated as H20-like phages, were shown to contain a lambda-like cI repressor gene in their genomes. It was suggested that this mechanism possibly confers repressor-mediated immunity to other H20-like phages in their V. anguillarum host [ 141 ]. A Sie system-encoding prophage has recently been reported to confer phage resistance in the V. cholerae strain 919TP [ 142 ].…”