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Abstract As parasites of bacteria, phages can regulate microbiome diversity and composition and may therefore affect susceptibility to pathogens and disease. Many infectious diseases are associated with altered bacteriophage communities, but observational studies alone do not allow us to determine when altered phage community composition is a contributor to disease risk, a response to infection, or simply an indicator of dysbiosis. To address this question directly, we used size-selective filtration to deplete plant-associated microbial communities of phages, then challenged plants with the bacterial pathogen Pseudomonas syringae. Plants with phage-depleted microbiomes were more susceptible to infection, an effect that could not be explained by direct effects of the phage communities on either P. syringae or the plant host. Moreover, the presence of phages was most impactful when the phage communities were isolated from neighboring field locations rather than from the same host plant as the bacteria, possibly suggesting that moderate rates of lysis maintain a community structure that is most resistant to pathogen invasion. Overall, our results support the idea that phage communities contribute to plant defenses by modulating the microbiome. 

ABSTRACT ThePseudomonas syringaespecies complex is a heterogeneous group of plant pathogenic bacteria associated with a wide distribution of plant species. Advances in genomics are revealing the complex evolutionary history of this species complex and the wide array of genetic adaptations underpinning their diverse lifestyles. Here, we genomically characterize twoP. syringaeisolates collected from diseased Callery pears (Pyrus calleryana) in Berkeley, California in 2019 and 2022. We also isolated a lytic bacteriophage, which we characterized and evaluated for biocontrol efficiency. Using a multilocus sequence analysis and core genome alignment, we classified theP. syringaeisolates as members of phylogroup 2, related to other strains previously isolated fromPyrusandPrunus. An analysis of effector proteins demonstrated an evolutionary conservation of effectoromes across isolates classified in PG2 and yet uncovered unique effector profiles for each, including the two newly identified isolates. Whole-genome sequencing of the associated phage uncovered a novel phage genus related toPseudomonas syringaepv.actinidiaephage PHB09 and theFlaumdravirusgenus. Finally, usingin plantainfection assays, we demonstrate that the phage was equally useful in symptom mitigation of immature pear fruit regardless of the Pss strain tested. Overall, this study demonstrates the diversity ofP. syringaeand their viruses associated with ornamental pear trees, posing spill-over risks to commercial pear trees and the possibility of using phages as biocontrol agents to reduce the impact of disease.IMPORTANCEGlobal change exacerbates the spread and impact of pathogens, especially in agricultural settings. There is a clear need to better monitor the spread and diversity of plant pathogens, including in potential spillover hosts, and for the development of novel and sustainable control strategies. In this study, we characterize the first described strains ofPseudomonas syringaepv.syringaeisolated from Callery pear in Berkeley, California from diseased tissues in an urban environment. We show that these strains have divergent virulence profiles from previously described strains and that they can cause disease in commercial pears. Additionally, we describe a novel bacteriophage that is associated with these strains and explore its potential to act as a biocontrol agent. Together, the data presented here demonstrate that ornamental pear trees harbor novelP. syringaepv.syringaeisolates that potentially pose a risk to local fruit production, or vice versa—but also provide us with novel associated phages, effective in disease mitigation. 

Abstract Bacteriophages are obligate parasites of bacteria characterized by the breadth of hosts that they can infect. This “host range” depends on the genotypes and morphologies of the phage and the bacterial host, but also on the environment in which they are interacting. Understanding phage host range is critical to predicting the impacts of these parasites in their natural host communities and their utility as therapeutic agents, but is also key to predicting how phages evolve and in doing so drive evolutionary change in their host populations, including through movement of genes among unrelated bacterial genomes. Here, we explore the drivers of phage infection and host range from the molecular underpinnings of the phage–host interaction to the ecological context in which they occur. We further evaluate the importance of intrinsic, transient, and environmental drivers shaping phage infection and replication, and discuss how each influences host range over evolutionary time. The host range of phages has great consequences in phage-based application strategies, as well as natural community dynamics, and we therefore highlight both recent developments and key open questions in the field as phage-based therapeutics come back into focus. 

Viruses of bacteriophages (phages) have broad effects on bacterial ecology and evolution in nature that mediate microbial interactions, shape bacterial diversity, and influence nutrient cycling and ecosystem function. The unrelenting impact of phages within the microbial realm is the result, in large part, of their ability to rapidly evolve in response to bacterial host dynamics. The knowledge gained from laboratory systems, typically using pairwise interactions between single-host and single-phage systems, has made clear that phages coevolve with their bacterial hosts rapidly, somewhat predictably, and primarily by counteradapting to host resistance. Recent advancement in metagenomics approaches, as well as a shifting focus toward natural microbial communities and host-associated microbiomes, is beginning to uncover the full picture of phage evolution and ecology within more complex settings. As these data reach their full potential, it will be critical to ask when and how insights gained from studies of phage evolution in vitro can be meaningfully applied to understanding bacteria-phage interactions in nature. In this review, we explore the myriad ways that phages shape and are themselves shaped by bacterial host populations and communities, with a particular focus on observed and predicted differences between the laboratory and complex microbial communities. Expected final online publication date for the Annual Review of Virology, Volume 9 is September 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates. 

Abstract Bacteria and lytic viruses (phages) engage in highly dynamic coevolutionary interactions over time, yet we have little idea of how transient selection by phages might shape the future evolutionary trajectories of their host populations. To explore this question, we generated genetically diverse phage-resistant mutants of the bacterium Pseudomonas syringae. We subjected the panel of mutants to prolonged experimental evolution in the absence of phages. Some populations re-evolved phage sensitivity, whereas others acquired compensatory mutations that reduced the costs of resistance without altering resistance levels. To ask whether these outcomes were driven by the initial genetic mechanisms of resistance, we next evolved independent replicates of each individual mutant in the absence of phages. We found a strong signature of historical contingency: some mutations were highly reversible across replicate populations, whereas others were highly entrenched. Through whole-genome sequencing of bacteria over time, we also found that populations with the same resistance gene acquired more parallel sets of mutations than populations with different resistance genes, suggesting that compensatory adaptation is also contingent on how resistance initially evolved. Our study identifies an evolutionary ratchet in bacteria–phage coevolution and may explain previous observations that resistance persists over time in some bacterial populations but is lost in others. We add to a growing body of work describing the key role of phages in the ecological and evolutionary dynamics of their host communities. Beyond this specific trait, our study provides a new insight into the genetic architecture of historical contingency, a crucial component of interpreting and predicting evolution.