Bacteriophages that infect marine roseobacters: genomics and ecology

Abstract

Summary Viruses are the most abundant biological entities in seawater. They influence microbial population dynamics, genetic heterogeneity and biogeochemical cycles in marine ecosystems. The isolation and characterization of viruses that infect specific hosts have greatly advanced our knowledge of the biological and ecological interactions between viruses and their hosts. Marine Roseobacter are abundant, ubiquitous and diverse in the ocean and play active roles in global biogeochemical cycling, especially the sulfur cycle. Currently, 32 bacteriophages that infect multiple lineages of roseobacters have been isolated and sequenced. These roseophages exhibit diverse morphologies, nucleic acid types and genomic features. Here, we provide the most up‐to‐date overview of roseophages. Most roseophages are host specific and have a wide range of genome sizes and open reading frames. Based on a genome‐wide comparison, at least eight distinctly different types of roseophages were identified, indicating their diversity. Lysogenic‐related and gene transfer agent‐related genes are commonly found in roseophage genomes, implying the importance of genetic transfer within roseobacters. This feature could provide the versatility for roseobacters to quickly adapt to the changing environments. A wide distribution range of roseophages in the global ocean, especially in coastal environments, has been observed, reflecting the cosmopolitan nature of the Roseobacter lineage.

A newly isolated roseophage represents a distinct member of Siphoviridae family

“…Among all the 19 strains tested, phage R4C can only infect D. shibae DFL12 (Additional file 1: Table S1), but other yet-to-be discovered hosts cannot be ruled out here. This result is consistent with the previous finding that roseophages seem to have narrow host ranges [12]. The suspensions of R4C treated with three different concentrations of chloroform showed obvious lytic plaques, indicating the absence of lipids outside the capsid, which is commonly observed in phages of the order Caudovirales [18].…”

“…ORF 16 is the largest gene in the RcGTA operon and known to be involved in host specificity. These four hallmark GTA-like genes have also been found in other roseophages within the family Siphoviridae [12]. In the phylogenetic analysis based on these four GTA-like sequences, the roseophages formed distinct clades from their hosts, indicating the independent evolution of the phage-encoded and host GTA-like genes (Fig.…”

“…Until now, over 96% of the phages reported in the scientific literature belong to the order Caudovirales , and the siphoviruses comprise approximately 61% of the tailed phages [24]. However, only 33% of the known roseophages belong to Siphoviridae , and the rest to the families Podoviridae and Microviridae [12].…”

“…However, only a handful of roseophages have been isolated and characterized. Recently, Zhan et al provided an up-to-date overview of the roseophages isolated from different lineages of Roseobacter , demonstrating the phylogenetic diversity of the roseophages and their multiple mutual effects on Roseobacter [12]. Therefore, the roseophage– Roseobacter could offer an ideal system to gain new insights into the diversity and evolution of phages and the relationships between phages and their bacterial hosts.…”

Diverse, Abundant, and Novel Viruses Infecting the Marine Roseobacter RCA Lineage

“…Currently, more than 30 phages that infect representatives of several major Roseobacter clusters have been reported (27). All of these roseophages were isolated from the Roseobacter strains that can grow in rich culture media and have high growth rates, such as Roseobacter SIO67, Ruegeria pomeroyi DSS-3, Roseobacter denitrificans OCh114, Sulfitobacter spp., and Dinoroseobacter shibae DFL 12 (27–32). Metagenomic analyses suggested that homologs of some roseophages were widespread in the ocean, while most of the isolated roseophages were not reported to make up a significant portion of viromic sequences in the ocean.…”