Coevolution between bacteriophages (phages) and their bacterial hosts occurs through changes in resistance and counter-resistance mechanisms. To assess phage-host evolution in wild populations, we isolated 195 Vibrio crassostreae strains and 243 vibriophages during a five month time-series from an oyster farm and combined these isolates with existing V. crassostreae and phage isolates. Cross-infection studies of 81,926 host-phage pairs delineated a modular network where phages are best at infecting cooccurring hosts, indicating local adaptation. Successful propagation of phage is restricted by the ability to adsorb to closely related bacteria and further constrained by strain-specific defence systems. These defences are highly diverse and predominantly located on mobile genetic elements, and multiple defences are active within a single genome. We further show that epigenetic and genomic modifications enable phage to adapt to bacterial defences and alter host range. Our findings reveal that the evolution of bacterial defences and phage counter-defences are underpinned by frequent genetic exchanges with, and between, mobile genetic elements.
24 ORIGINALITY-SIGNIFICANCE STATEMENT 25A recent study highlighted the role of a herpes virus as primary etiological agent of Pacific oyster 26 mortality syndrome (POMS), which affects juveniles of the oyster Crassostrea gigas. We show 27 here that the selection of virulent bacteria in oyster farms is also an important piece of the POMS 28 puzzle. This bacteria taxonomically assigned to Vibrio crassostreae species, carries a plasmid 29 that encodes a Type 6 Secretion System (T6SS), which increases its ability to kill the major 30 cellular players of oyster immunity, the hemocytes. This T6SS was identified in two additional 31 species that infect mollusks, suggesting a parallel evolution of these pathogens. Finally, our 32 results indicate that broad range of pathogens kill their hosts via hemocyte cytotoxicity. 33 34 ABSTRACT 35Pacific oyster mortality syndrome affects juveniles of Crassostrea gigas oysters and threatens the 36 sustainability of commercial and natural stocks of this species. Vibrio crassostreae has been 37 repeatedly isolated from diseased animals and the majority of the strains have been demonstrated 38 to be virulent for oysters. In this study we showed that oyster farms exhibited a high prevalence 39 of a virulence plasmid carried by V. crassostreae while oysters, at an adult stage, were reservoirs 40 of this virulent population. The pathogenicity of V. crassostreae depends on a novel 41 transcriptional regulator, which activates the bidirectional promoter of a Type 6 Secretion System 42 (T6SS) genes cluster. Both the T6SS and a second chromosomal virulence factor, r5.7, are 43 necessary for virulence but act independently to cause to hemocyte (oyster immune cell) 44 cytotoxicity. A phylogenetically closely related T6SS was identified in V. aestuarianus and V. 45 tapetis, which infect adult oysters and clams, respectively. We propose that hemocyte 46 cytotoxicity, is a lethality trait shared by a broad range of mollusk pathogens and we speculate 47 107 108 RESULTS 110The virulence plasmid is widespread in V. crassostreae population occurring in oyster farms 111We previously hypothesized that the introgression of the virulence plasmid pGV into 112 V. crassostreae might have been favored by elevated host density in farming areas (Bruto et al., 113 2017). However, wild oyster beds can also reach high densities, as exemplified by the recent 114 invasion of C. gigas oysters into the Wadden sea (North Sea) (Reise et al., 2017). To date, no 115Vibrio-associated mass mortalities have been observed in this area, in contrast to observations in 116 heavily farmed areas. We thus investigated the presence and frequency of the pGV plasmid in 117 V. crassostreae strains sampled from Sylt. For this, 910 Vibrio strains were isolated from 118 seawater fractions and oysters from Sylt, genotyped by partial hsp60 gene sequencing and 119 assigned to Vibrio populations as described previously ( Figure S1). Multi Locus Sequencing 120Typing (MLST) further confirmed the taxonomic assignment of 47 V. crassostreae str...
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