Marine viral particles reveal an expansive repertoire of phage-parasitizing mobile elements

Abstract

Phage satellites are mobile genetic elements that propagate by parasitizing bacteriophage replication. We report here the discovery of abundant and diverse phage satellites that were packaged as concatemeric repeats within naturally occurring bacteriophage particles in seawater. These same phage-parasitizing mobile elements were found integrated in the genomes of dominant co-occurring bacterioplankton species. Like known phage satellites, many of the marine phage satellites encoded genes for integration, DNA replication, phage interference, and capsid assembly. Many also contained distinctive gene suites indicative of unique virus hijacking, phage interference and mobilization mechanisms. Marine phage satellite sequences were widespread in local and global oceanic virioplankton populations, reflecting their ubiquity, abundance, and temporal persistence in marine planktonic communities worldwide. Their gene content and putative life cycles suggest they may impact host-cell phage immunity and defense, lateral gene transfer, and bacteriophage-induced cell mortality and host and virus productivity. These previously unrecognized marine phage satellites therefore, have potential to impact the ecology and evolution of bacteria and their bacteriophages in the ocean, and similar phage parasites likely thrive in many other microbial habitats as well.

Identification and characterization of thousands of bacteriophage satellites across bacteria

“…Such elements may use novel exciting mechanisms for replication, sensing, or phage hijacking. Many elements in marine bacteria have recently been proposed to be phage satellites (17), and other some “incomplete” PLEs were recently described in Vibrionacea other than V. cholerae (42). Considering that half of the bacteria have at least one prophage (48) and that we identified satellites in a much smaller number of bacterial genomes, it is very likely that this is the beginning of the characterization of a vast diversity of phage satellites.…”

“…These studies have helped recognize phage satellites as characteristic mobile elements that have specialized in being mobilized by fully functional phages. Moreover, there have been recent reports of genomic islands transduced by phages that are different from known phage satellites, which suggests that different types of satellites remain to be discovered (17, 18).…”

“…We used the region from the integrase to the last identified core component to delimit the PICI (the element lacking the integrase was discarded). The resulting 1435 PICI have a median size of 9.5Kb (15 proteins), and only a few elements(17) have between 20 and 28Kb (Fig 2F, Fig 2G). PICI are much more diverse, as measured by the wGRR, than P4-like satellites (p=0, twosample Kolmogorov-Smirnov test).…”