Genomic diversity, life strategies and ecology of marine HTVC010P-type pelagiphages

Abstract

SAR11 bacteria dominate ocean surface bacterioplankton communities, and play an important role in marine carbon and nutrient cycling. The biology and ecology of SAR11 are impacted by SAR11 phages (pelagiphages) that are highly diverse and abundant in the ocean. Among the currently known pelagiphages, HTVC010P represents an extremely abundant but under-studied phage group in the ocean. In this study, we have isolated seven new HTVC010P-type pelagiphages, and recovered 77 nearly full-length HTVC010P-type metagenomic viral genomes from marine metagenomes. Comparative genomic and phylogenomic analyses showed that HTVC010P-type pelagiphages display genome synteny and can be clustered into two major subgroups, with subgroup I consisting of strictly lytic phages and subgroup II mostly consisting of phages with potential lysogenic life cycles. All but one member of the subgroup II contain an integrase gene. Site-specific integration of subgroup II HTVC010P-type pelagiphage was either verified experimentally or identified by in silico genomic sequence analyses, which revealed that various SAR11 tRNA genes can serve as the integration sites of HTVC010P-type pelagiphages. Moreover, HTVC010P-type pelagiphage integration was confirmed by the detection of several Global Ocean Survey (GOS) fragments that contain hybrid phage–host integration sites. Metagenomic recruitment analysis revealed that these HTVC010P-type phages were globally distributed and most lytic subgroup I members exhibited higher relative abundance. Altogether, this study significantly expands our knowledge about the genetic diversity, life strategies and ecology of HTVC010P-type pelagiphages.

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

“…Recently, the presence of temperate phage in oligotrophic Pelagibacter species has been validated (28,29), consistent with our observations of phage satellites in the genomes of this ubiquitous bacterioplankton group. Similarly, cyanophages of Prochlorococcus often encode integrases, which allows them to integrate into host genomes (30).…”

“…Specifically, the most prevalent cellular hosts of surface water marine VEIMEs were Pelagibacter and the cyanobacterium Prochlorococcus , among the most abundant bacterial groups present in open ocean surface waters (26, 27). Recently, the presence of temperate phage in oligotrophic Pelagibacter species has been validated (28, 29), consistent with our observations of phage satellites in the genomes of this ubiquitous bacterioplankton group. Similarly, cyanophages of Prochlorococcus often encode integrases, which allows them to integrate into host genomes (30).…”

Auxiliary Metabolic Gene Functions in Pelagic and Benthic Viruses of the Baltic Sea

“…The enzyme is involved in the synthesis of sulfite from phosphoadenosine 5’-phosphosulfate (PAPS) and thus part of the sulfate reduction pathway ( Bick et al, 2000 ). The cysH gene has been identified in phages infecting members of the SAR11 clade, which lack the phosphoadenosine 5’-phosphosulfate reductase and other genes required in assimilatory sulfate reduction but has recently also been found to be generally widespread in marine phages ( Du et al, 2021 ; Kieft et al, 2021 ).…”

Pelagibacter phage Skadi - An abundant polar specialist that exemplifies ecotypic niche specificity among the most abundant viruses on Earth

“…Whole-genome alignment showed that the Skadi genome is arranged into early and late genomic regions similar to other HTVC010P-type genomes [27]. A TonB-dependent receptor protein located between the two tail tube proteins A and B and the major capsid protein suggests TonB as a putative receptor for adsorption and initiating infection [39,40] (Figure 1).…”

“…Located within the direct terminal repeat region is a conserved TerL gene for packaging. For cell lysis, Skadi encodes a peptidase M15, similar to other HTVC010P-type pelagiphages [27]. Alignment of HTVC010P-type genomes showed that regions related to DNA replication and metabolism, as well as the terminase and phage head related proteins are conserved, using recommended amino acid identity (AAI) thresholds of >30% [38] (Supplementary Figure 1).…”