A New Freshwater Cyanosiphovirus Harboring Integrase

Abstract

Pelagic cyanobacteria are key players in the functioning of aquatic ecosystems, and their viruses (cyanophages) potentially affect the abundance and composition of cyanobacterial communities. Yet, there are few well-described freshwater cyanophages relative to their marine counterparts, and in general, few cyanosiphoviruses (family Siphoviridae) have been characterized, limiting our understanding of the biology and the ecology of this prominent group of viruses. Here, we characterize S-LBS1, a freshwater siphovirus lytic to a phycoerythrin-rich Synechococcus isolate (Strain TCC793). S-LBS1 has a narrow host range, a burst size of ∼400 and a relatively long infecting step before cell lysis occurs. It has a dsDNA 34,641 bp genome with putative genes for structure, DNA packing, lysis, replication, host interactions, DNA repair and metabolism. S-LBS1 is similar in genome size, genome architecture, and gene content, to previously described marine siphoviruses also infecting PE-rich Synechococcus, e.g., S-CBS1 and S-CBS3. However, unlike other Synechococcus phages, S-LBS1 encodes an integrase, suggesting its ability to establish lysogenic relationships with its host. Sequence recruitment from viral metagenomic data showed that S-LBS1-like viruses are diversely present in a wide range of aquatic environments, emphasizing their potential importance in controlling and structuring Synechococcus populations. A comparative analysis with 16 available sequenced cyanosiphoviruses reveals the absence of core genes within the genomes, suggesting high degree of genetic variability in siphoviruses infecting cyanobacteria. It is likely that cyanosiphoviruses have evolved as distinct evolutionary lineages and that adaptive co-evolution occurred between these viruses and their hosts (i.e., Synechococcus, Prochlorococcus, Nodularia, and Acaryochloris), constituting an important driving force for such phage diversification.

Genomic Analysis of Mic1 Reveals a Novel Freshwater Long-Tailed Cyanophage

“…Phylogenetic analysis based on the large terminase subunit TerL showed that Mic1 falls into the "P22-like headful" cluster ( Figure 4A), which has a terminally redundant and circularly permuted genome (Casjens and Gilcrease, 2009). Mic1 is closely related to siphovirus Lactobacillus thermophilus prophage Lj964 (Desiere et al, 2000) and Staphylococcus aureus phage phiETA (Yamaguchi et al, 2000) based on the pac-site DNA packaging and long tail morphogenesis modules, but distinct from the λ-like freshwater cyanosiphophage S-LBS1 (Zhong et al, 2018).…”

“…Before Mic1, only 14 cyanosiphophages have been genomesequenced, including 11 marine and 3 freshwater cyanophages. To determine the degree of genomic variability between the cyanosiphophages, the heatmap was clustered based on Bray-Curtis similarity (Zhong et al, 2018) and compared the gene similarities between two phages ( Figure 5A). The cyanophages A-HIS1 and A-HIS2 of the unicellular cyanobacterium Acaryochloris marina (Chan et al, 2011), CrV-01T of the filamentous Cylindrospermopsis (Raphidiopsis) raciborskii (Martin et al, 2019), vB_NpeS-2AV2 of the filamentous nitrogen fixing cyanobacterium Nodularia sp.…”

“…Afterward, four contractile-tailed phages, MaMV-DC (Ou et al, 2015a), S-CRM01 (Dreher et al, 2011), A-1 and N-1 (Chenard et al, 2016), five short-tailed phages, PP (Zhou et al, 2013), Pf-WMP3 (Liu et al, 2008), Pf-WMP4 (Liu et al, 2007), A-4L (Ou et al, 2015b) and S-EIV1 (Chenard et al, 2015) and one so-called tailless phage PaV-LD (Gao et al, 2012) were sequentially isolated from different sources of freshwater. Nevertheless, only three complete genomes of freshwater siphophages, S-2L (Marliere, 2006), S-LBS1 (Zhong et al, 2018), and CrV-01T (Martin et al, 2019) have been reported to date.…”

Genome-resolved viral and cellular metagenomes revealed potential key virus-host interactions in a deep freshwater lake

“…Some major achievements in marine viromics include the identification of viruses infecting the dominant bacterioplankton lineages (53)(54)(55)(56), which have eluded cultivation-based efforts (57)(58)(59)(60). In freshwater systems, in addition to viruses that infect cyanobacteria (61)(62)(63)(64), which are relatively amenable to cultivation, several viruses that infect ubiquitous freshwater bacterioplankton lineages have been identified in the last few years, including isolated viruses that infect LD28 (Ca. Methylopumilus) (44) and Comamonadaceae (65), and metagenomically-recovered viruses of Actinobacteria (66) and Polynucleobacter (67).…”

Viruses of freshwater bloom‐forming cyanobacteria: genomic features, infection strategies and coexistence with the host

“…Again, these Group IV and V viruses also showed no sequence similarities with known viruses in the current databases (Figs 3 and 7). It is worth to note that two freshwater Synechococcus viruses (S-LBS1 and S-CRM01) were shown to cluster together with marine cyanoviruses and not with other freshwater cyanoviruses (Dreher et al, 2011;Zhong et al, 2018). In addition, freshwater Synechococcus virus S-CBWM1 and S-EIV1 also shared more homologues with marine counterparts S-TIM5 and S-CBS2, whereas they only showed partial sequence similarities of a few genes with Microcystis virus Mic1 and Cylindrospermopsis virus CrV-01T respectively (Figs 4 and 5).…”