Genomic diversification of marine cyanophages into stable ecotypes

Abstract

SummaryUnderstanding the structure and origin of natural bacteriophage genomic diversity is important in elucidating how bacteriophages influence the mortality rates and composition of their host communities. Here, we examine the genetic structure and genomic diversification of naturally occurring bacteriophages by analyzing the full genomic sequences of over 100 isolates of Synechococcus-infecting cyanophages collected over 15 years from coastal waters of Southern New England, USA. Our analysis revealed wellsupported cyanophage genomic clusters (genomewide average nucleotide identity (ANI) >93%) and subclusters (genome-wide ANI >98%) that remained consistent for a decade or longer. Furthermore, by combining the genomic data with genetic analysis of an additional 800 isolates and environmental amplicon sequence data both genomic clusters and subclusters were found to exhibit clear temporal and/ or spatial patterns of abundance, suggesting that these units represent distinct viral ecotypes. The processes responsible for diversification of cyanophages into genomic clusters and subclusters were similar across genetic scales and included allelic exchange as well as gene gain and loss. Isolates belonging to different subclusters were found to differ in genes that encoded auxiliary metabolic functions, restriction modification enzymes, and virion structural proteins, although the specific traits and selection pressures responsible for the maintenance of distinct ecotypes remain unknown.

Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept

“…In cyanophages, population genetic analyses support the validity of this cut-off in delineating populations under different selective pressures and where barriers to cross-population gene flow exist (Gregory et al, 2016). Others have shown the existence of stable cyanophage ecotypes that persist for decades and that exhibit distinct temporal and spatial patterns of abundance—though in this study the clusters were defined at >93 and >98% ANI for their defined “clusters” and “subclusters,” respectively (Marston and Martiny, 2016). Yet, the appropriateness of the genome-similarity-based threshold remains unexplored in non-cyanophage systems and has not yet included consideration of fitness-determining infection traits.…”

“…Determination of fitness-conferring infection traits for the large collections of closely related phages (e.g., Pope et al, 2015; Gregory et al, 2016; Marston and Martiny, 2016) is a valuable metric that—while labor intensive to collect—would further test this OTU-defining model and enable the application of theory to advance viral community ecology.…”

“…For phages, this concept has been in development for some time and has been supported by the stable spatial and temporal distribution of T4-like cyanomyophage isolates based on gene marker (Marston and Amrich, 2009) and full-genome analyses (Marston and Martiny, 2016), as well as genome-wide analyses of viral-tagged metagenomic contigs from wild virus populations (Deng et al, 2014). Most recently, a phylogenomic analysis of 142 marine T4-like cyanophages isolated on a single host ( Synechococcus WH7803) observed that when this >95% threshold was applied, (i) recombination rates were greater within genotypic phage populations than between them, indicative of intra-population barriers to gene flow and (ii) different genes were under selection in the different populations, while the selection profile was conserved within populations (Gregory et al, 2016).…”

Variation in the Genetic Repertoire of Viruses Infecting Micromonas pusilla Reflects Horizontal Gene Transfer and Links to Their Environmental Distribution

“…The relationship between virus gene content in prasinoviruses and their environmental distribution is unexplored, but marine virus communities show biogeographic patterns [32,33,34], including viruses infecting Ostreococcus tauri , which form distinct communities in contrasting environments [35]. Furthermore, the diversity and composition of prasinovirus communities is influenced by environmental factors, particularly the availability of phosphate [36].…”

“…Furthermore, the diversity and composition of prasinovirus communities is influenced by environmental factors, particularly the availability of phosphate [36]. A recent study on cyanophage isolates, which prominently host a range of AMGs, linked their genome similarity with environmental distribution, thus formulating a diversification of viruses into ecotypes [34]. This suggests that the gene content of prasinoviruses may reflect their environmental distribution.…”