Infection strategy and biogeography distinguish cosmopolitan groups of marine jumbo bacteriophages

Abstract

Recent research has underscored the immense diversity and key biogeochemical roles of large DNA viruses in the ocean. Although they are important constituents of marine ecosystems, it is sometimes difficult to detect these viruses due to their large size and complex genomes. This is true for “jumbo” bacteriophages, which have genome sizes >200 kbp and large capsids reaching up to 0.45 µm in diameter. In this study, we sought to assess the genomic diversity and distribution of these bacteriophages in the ocean by generating and analyzing jumbo phage genomes from metagenomes. We recover 85 marine jumbo phages that ranged in size from 201 to 498 kilobases, and we examine their genetic similarities and biogeography together with a reference database of marine jumbo phage genomes. By analyzing Tara Oceans metagenomic data, we show that although most jumbo phages can be detected in a range of different size fractions, 17 of our bins tend to be found in those greater than 0.22 µm, potentially due to their large size. Our network-based analysis of gene-sharing patterns reveals that jumbo bacteriophages belong to five genome clusters that are typified by diverse replication strategies, genomic repertoires, and potential host ranges. Our analysis of jumbo phage distributions in the ocean reveals that depth is a major factor shaping their biogeography, with some phage genome clusters occurring preferentially in either surface or mesopelagic waters, respectively. Taken together, our findings indicate that jumbo phages are widespread community members in the ocean with complex genomic repertoires and ecological impacts that warrant further targeted investigation.

Plankton-infecting relatives of herpesviruses clarify the evolutionary trajectory of giant viruses

“…The Caudoviricetes and Nucleocytoviricota viruses are prevalent in the sunlit ocean where they play a critical role in regulating the community composition and blooming activity of plankton 7–9 . Metagenomic assemblies and genome-resolved metagenomics were used to target these viruses within plankton, complementing culture-dependent virus isolation efforts and leading to our improved appreciation of their genomic diversity 7,8,10–12 . These environmental surveys emphasized the prevalence and functional complexity of DNA viruses in the sunlit ocean and supported the evolutionary demarcation between the virion and informational modules of Varidnaviria and Duplodnaviria realms.…”

Diversity and Ecology of Caudoviricetes Phages with Genome Terminal Repeats in Fecal Metagenomes from Four Dutch Cohorts

“…Furthermore, different regions of the same phage genome may employ different genetic codes [ 38 , 89 ]. Finally, the sensitivity and selectivity of virus detection is strongly influenced by the selection of the breadth of coverage threshold [ 50 , 90 ]. In this study, we considered a vOTU detected if the breadth of representative sequence coverage by reads reached 75%.…”

Viral Complexity

“…Although still a minority compared to smaller phages, over 300 jumbo phages have been cultivated and had their genomes sequenced [ 23 ]. Moreover, cultivation-independent approaches have reconstructed genomes of many more of these phages, some with genome sizes >700 kbp, and suggested that they are ubiquitous in the biosphere [ 24 , 25 , 26 , 27 ].…”

“…Relatively less is known about the functional repertoires of jumbo phages owing to the lack of detectable homologs in many genomes and the relatively recent discovery of many new groups [ 24 , 25 , 27 , 81 ]. Moreover, given the small number of jumbo phage genomes currently available, it is at present unclear if these viruses have any distinct functional capabilities that distinguish them from their smaller relatives.…”

“…Because the 200 kbp cutoff that is usually used to define jumbo bacteriophages is somewhat arbitrary, it is reasonable to assume that clades of jumbo phages will form groups with smaller viruses within the Caudoviricetes . Gene clustering analyses have generally borne out this expectation, though the higher-order evolutionary relationships between clades of jumbo phages remain unclear [ 25 , 160 ]. Large DNA viruses in the order Herpesvirales have a shared evolutionary history with tailed bacteriophages owing to their use of a homologous HK97-fold capsid, and both of these orders are currently classified in the kingdom Heunggongvirae [ 155 ].…”