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1. The LuxO-OpaR quorum-sensing cascade differentially controls Vibriophage VP882 lysis-lysogeny decision making in liquid and on surfaces

   https://doi.org/10.1371/journal.pgen.1011243  

   Santoriello, Francis J; Bassler, Bonnie L (July 2024, PLOS Genetics)

   Dalia, Ankur B (Ed.)

   Quorum sensing (QS) is a process of cell-to-cell communication that bacteria use to synchronize collective behaviors. QS relies on the production, release, and group-wide detection of extracellular signaling molecules called autoinducers.Vibrios use two QS systems: the LuxO-OpaR circuit and the VqmA-VqmR circuit. Both QS circuits control group behaviors including biofilm formation and surface motility. TheVibrio parahaemolyticustemperate phage φVP882 encodes a VqmA homolog (called VqmAφ). When VqmAφ is produced by φVP882 lysogens, it binds to the host-produced autoinducer called DPO and launches the φVP882 lytic cascade. This activity times induction of lysis with high host cell density and presumably promotes maximal phage transmission to new cells. Here, we explore whether, in addition to induction from lysogeny, QS controls the initial establishment of lysogeny by φVP882 in naïve host cells. Using mutagenesis, phage infection assays, and phenotypic analyses, we show that φVP882 connects its initial lysis-lysogeny decision to both host cell density and whether the host resides in liquid or on a surface. Host cells in the low-cell-density QS state primarily undergo lysogenic conversion. The QS regulator LuxO~P promotes φVP882 lysogenic conversion of low-cell-density planktonic host cells. By contrast, the ScrABC surface-sensing system regulates lysogenic conversion of low-cell-density surface-associated host cells. ScrABC controls the abundance of the second messenger molecule cyclic diguanylate, which in turn, modulates motility. ThescrABCoperon is only expressed when its QS repressor, OpaR, is absent. Thus, at low cell density, QS-dependent derepression ofscrABCdrives lysogenic conversion in surface-associated host cells. These results demonstrate that φVP882 integrates cues from multiple sensory pathways into its lifestyle decision making upon infection of a new host cell. 

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2. Host population diversity as a driver of viral infection cycle in wild populations of green sulfur bacteria with long standing virus-host interactions

   https://doi.org/10.1038/s41396-020-00870-1  

   Berg, Maureen; Goudeau, Danielle; Olmsted, Charles; McMahon, Katherine D.; Yitbarek, Senay; Thweatt, Jennifer L.; Bryant, Donald A.; Eloe-Fadrosh, Emiley A.; Malmstrom, Rex R.; Roux, Simon (June 2021, The ISME Journal)

   Abstract Temperate phages are viruses of bacteria that can establish two types of infection: a lysogenic infection in which the virus replicates with the host cell without producing virions, and a lytic infection where the host cell is eventually destroyed, and new virions are released. While both lytic and lysogenic infections are routinely observed in the environment, the ecological and evolutionary processes regulating these viral dynamics are still not well understood, especially for uncultivated virus-host pairs. Here, we characterized the long-term dynamics of uncultivated viruses infecting green sulfur bacteria (GSB) in a model freshwater lake (Trout Bog Lake, TBL). As no GSB virus has been formally described yet, we first used two complementary approaches to identify new GSB viruses from TBL; one in vitro based on flow cytometry cell sorting, the other in silico based on CRISPR spacer sequences. We then took advantage of existing TBL metagenomes covering the 2005–2018 period to examine the interactions between GSB and their viruses across years and seasons. From our data, GSB populations in TBL were constantly associated with at least 2-8 viruses each, including both lytic and temperate phages. The dominant GSB population in particular was consistently associated with two prophages with a nearly 100% infection rate for >10 years. We illustrate with a theoretical model that such an interaction can be stable given a low, but persistent, level of prophage induction in low-diversity host populations. Overall, our data suggest that lytic and lysogenic viruses can readily co-infect the same host population, and that host strain-level diversity might be an important factor controlling virus-host dynamics including lytic/lysogeny switch. 

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3. Lysogeny in the oceans: Lessons from cultivated model systems and a reanalysis of its prevalence

   https://doi.org/10.1111/1462-2920.15233  

   Tuttle, Matthew J.; Buchan, Alison (September 2020, Environmental Microbiology)

   Summary In the oceans, viruses that infect bacteria (phages) influence a variety of microbially mediated processes that drive global biogeochemical cycles. The nature of their influence is dependent upon infection mode, be it lytic or lysogenic. Temperate phages are predicted to be prevalent in marine systems where they are expected to execute both types of infection modes. Understanding the range and outcomes of temperate phage–host interactions is fundamental for evaluating their ecological impact. Here, we (i) review phage‐mediated rewiring of host metabolism, with a focus on marine systems, (ii) consider the range and nature of temperate phage–host interactions, and (iii) draw on studies of cultivated model systems to examine the consequences of lysogeny among several dominant marine bacterial lineages. We also readdress the prevalence of lysogeny among marine bacteria by probing a collection of 1239 publicly available bacterial genomes, representing cultured and uncultivated strains, for evidence of complete prophages. Our conservative analysis, anticipated to underestimate true prevalence, predicts 18% of the genomes examined contain at least one prophage, the majority (97%) were found within genomes of cultured isolates. These results highlight the need for cultivation of additional model systems to better capture the diversity of temperate phage–host interactions in the oceans. 

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4. The value of information gathering in phage–bacteria warfare

   https://doi.org/10.1093/pnasnexus/pgad431  

   Dahan, Yuval; Wingreen, Ned S.; Meir, Yigal; Bahar, ed., Ivet (January 2024, PNAS Nexus)

   Abstract Phages—viruses that infect bacteria—have evolved over billions of years to overcome bacterial defenses. Temperate phage, upon infection, can “choose” between two pathways: lysis—in which the phage create multiple new phage particles, which are then liberated by cell lysis, and lysogeny—where the phage’s genetic material is added to the bacterial DNA and transmitted to the bacterial progeny. It was recently discovered that some phages can read information from the environment related to the density of bacteria or the number of nearby infection attempts. Such information may help phage make the right choice between the two pathways. Here, we develop a theoretical model that allows an infecting phage to change its strategy (i.e. the ratio of lysis to lysogeny) depending on an outside signal, and we find the optimal strategy that maximizes phage proliferation. While phages that exploit extra information naturally win in competition against phages with a fixed strategy, there may be costs to information, e.g. as the necessary extra genes may affect the growth rate of a lysogen or the burst size of new phage for the lysis pathway. Surprisingly, even when phages pay a large price for information, they can still maintain an advantage over phages that lack this information, indicating the high benefit of intelligence gathering in phage–bacteria warfare. 

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5. A Transducing Bacteriophage Infecting Staphylococcus epidermidis Contributes to the Expansion of a Novel Siphovirus Genus and Implies the Genus Is Inappropriate for Phage Therapy

   https://doi.org/10.1128/msphere.00524-22  

   Andrews, Taylor; Hoyer, J. Steen; Ficken, Karolyn; Fey, Paul D.; Duffy, Siobain; Boyd, Jeffrey M. (April 2023, mSphere)

   Imperiale, Michael J. (Ed.)

   ABSTRACT The effort to discover novel phages infecting Staphylococcus epidermidis contributes to both the development of phage therapy and the expansion of genome-based phage phylogeny. Here, we report the genome of an S. epidermidis -infecting phage, Lacachita, and compare its genome with those of five other phages with high sequence identity. These phages represent a novel siphovirus genus, which was recently reported in the literature. The published member of this group was favorably evaluated as a phage therapeutic agent, but Lacachita is capable of transducing antibiotic resistance and conferring phage resistance to transduced cells. Members of this genus may be maintained within their host as extrachromosomal plasmid prophages, through stable lysogeny or pseudolysogeny. Therefore, we conclude that Lacachita may be temperate and members of this novel genus are not suitable for phage therapy. IMPORTANCE This project describes the discovery of a culturable bacteriophage infecting Staphylococcus epidermidis that is a member of a rapidly growing novel siphovirus genus. A member of this genus was recently characterized and proposed for phage therapy, as there are few phages currently available to treat S. epidermidis infections. Our data contradict this, as we show Lacachita is capable of moving DNA from one bacterium to another, and it may be capable of maintaining itself in a plasmid-like state in infected cells. These phages’ putative plasmid-like extrachromosomal state appears to be due to a simplified maintenance mechanism found in true plasmids of Staphylococcus and related hosts. We suggest Lacachita and other identified members of this novel genus are not suitable for phage therapy. 

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