Introducing a Novel, Broad Host Range Temperate Phage Family Infecting Rhizobium leguminosarum and Beyond

Abstract

Temperate phages play important roles in bacterial communities but have been largely overlooked, particularly in non-pathogenic bacteria. In rhizobia the presence of temperate phages has the potential to have significant ecological impacts but few examples have been described. Here we characterize a novel group of 5 Rhizobium leguminosarum prophages, capable of sustaining infections across a broad host range within their host genus. Genome comparisons identified further putative prophages infecting multiple Rhizobium species isolated globally, revealing a wider family of 10 temperate phages including one previously described lytic phage, RHEph01, which appears to have lost the ability to form lysogens. Phylogenetic discordance between prophage and host phylogenies suggests a history of active mobilization between Rhizobium lineages. Genome comparisons revealed conservation of gene content and order, with the notable exception of an approximately 5 kb region of hypervariability, containing almost exclusively hypothetical genes. Additionally, several horizontally acquired genes are present across the group, including a putative antirepressor present only in the RHEph01 genome, which may explain its apparent inability to form lysogens. In summary, both phenotypic and genomic comparisons between members of this group of phages reveals a clade of viruses with a long history of mobilization within and between Rhizobium species.

Viruses of nitrogen-fixing Mesorhizobium bacteria in globally distributed chickpea root nodules

“…After clustering the > 10 kbp viral contigs at 95% average nucleotide identity, we retained 106 viral operational taxonomic units (vOTUs). The number of recovered vOTUs is low compared to recent soil viral assemblage studies that have recovered thousands of vOTUs [27], probably because we focused only on viruses likely to infect Mesorhizobium. Moreover, we focused on root nodules, which are an intrinsically low diversity environment [11] and thus likely to have fewer vOTUs than more diverse environments such as soil.…”

Lysogeny destabilizes computationally simulated microbiomes

“…Therefore, when temperate were generalists, their infections of many bacterial hosts were lytic, and thus their effects were more similar to those of virulent phages. In nature, some phages are capable of lysogenizing more than one bacterial host species [43, 44]. New theory is needed to understand how such generalist lysogeny affects bacterial community dynamics.…”

“…Both the probability that a phage enters the lysogenic cycle and the rate at which prophages are induced can depend on environmental factors including the densities of bacteria and phages [34,[37][38][39]. It has been suggested that lysogeny may alter the effect of phages on microbial ecosystems [32,34,35,[40][41][42][43], but little is known about how this mode of infection affects the diversity and dynamics of microbiomes [17,30,35,44].…”

Discovery of a novel filamentous prophage in the genome of the Mimosa pudica microsymbiont Cupriavidus taiwanensis STM 6018

“…Bacteriophages are ubiquitous in bacterial populations, and although they can kill or impose metabolic burdens on their hosts, phages that are integrated into the chromosome can supply benefits to the host bacterium as agents of horizontal gene transfer (HGT), sources of genetic variation, in bacterial competition, and by supplying phage-encoded virulence genes; they may also affect bacterial motility, biofilm production and relationships with hosts (Figueroa-Bossi et al, 2001;Wagner and Waldor, 2002;Allison, 2007;Harrison and Brockhurst, 2017;Secor et al, 2020). Although the recent expansion of both phage-derived and bacterial sequence databases has uncovered a high abundance of prophages within Proteobacterial genomes in particular (López-Leal et al, 2022), their role in rhizobial lifestyles is currently not well understood (Ford et al, 2021).…”