Host populations are under continual selection by parasites due to reduced fitness of infected individuals relative to uninfected individuals. This should select for host resistance against ...parasites, and ample evidence from the laboratory and natural populations demonstrates that hosts can respond rapidly to parasitism by evolving resistance. Why then do parasites still exist? In part, this is due to ongoing arms races as parasites evolve counteradaptations to overcome resistance and to the presence of spatial structure and refuges. However, host-parasite coexistence can also be explained through loss of resistance over time due either to selection against costly resistance mechanisms or constant loss of resistance via reversion mutations.
Abstract
Bacteria–phage coevolution, the reciprocal evolution between bacterial hosts and the phages that infect them, is an important driver of ecological and evolutionary processes in microbial ...communities. There is growing evidence from both laboratory and natural populations that coevolution can maintain phenotypic and genetic diversity, increase the rate of bacterial and phage evolution and divergence, affect community structure, and shape the evolution of ecologically relevant bacterial traits. Although the study of bacteria–phage coevolution is still in its infancy, with open questions regarding the specificity of the interaction, the gene networks of coevolving partners, and the relative importance of the coevolving interaction in complex communities and environments, there have recently been major advancements in the field. In this review, we sum up our current understanding of bacteria–phage coevolution both in the laboratory and in nature, discuss recent findings on both the coevolutionary process itself and the impact of coevolution on bacterial phenotype, diversity and interactions with other species (particularly their eukaryotic hosts), and outline future directions for the field.
Empirical evidence for bacteria-phage coevolution from both laboratory and natural populations suggests that coevolution is a key driver of ecological and evolutionary processes in microbial communities.
The evolution of resistance to parasites is fundamentally important to disease ecology, yet we remain unable to predict when and how resistance will evolve. This is largely due to the ...context-dependent nature of host-parasite interactions, as the benefit of resistance will depend on the abiotic and biotic environment. Through experimental evolution of the plant pathogenic bacterium Pseudomonas syringae and two lytic bacteriophages across two different environments (high-nutrient media and the tomato leaf apoplast), we demonstrate that de novo evolution of resistance is negligible in planta despite high levels of resistance evolution in vitro. We find no evidence supporting the evolution of phage-selected resistance in planta despite multiple passaging experiments, multiple assays for resistance, and high multiplicities of infection. Additionally, we find that phage-resistant mutants (evolved in vitro) did not realize a fitness benefit over phage-sensitive cells when grown in planta in the presence of phage, despite reduced growth of sensitive cells, evidence of phage replication in planta, and a large fitness benefit in the presence of phage observed in vitro. Thus, this context-dependent benefit of phage resistance led to different evolutionary outcomes across environments. These results underscore the importance of studying the evolution of parasite resistance in ecologically relevant environments.
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.
Bacteriophages as obligate parasites are characterized by a host range which is subjected to multifaceted drivers that influence phage ecology and their application in biotechnology.
Studying the coevolutionary dynamics between bacteria and the bacteriophage viruses that infect them is critical to understanding both microbial diversity and ecosystem functioning. Phages can play a ...key role in shaping bacterial population dynamics and can significantly alter both intra- and inter-specific competition among bacterial hosts. Predicting how phages might influence community stability and apparent competition, however, requires an understanding of how bacteria-phage interaction networks evolve as a function of host diversity and community dynamics. Here, we first review the progress that has been made in understanding phage specificity, including the use of experimental evolution, we then introduce a new dataset on natural bacteriophages collected from the phyllosphere of horse chestnut trees, and finally we highlight that bacterial sensitivity to phage is rarely a binary trait and that this variation should be taken into account and reported. We emphasize that there is currently insufficient evidence to make broad generalizations about phage host range in natural populations, the limits of phage adaptation to novel hosts, or the implications of phage specificity in shaping microbial communities. However, the combination of experimental and genomic approaches with the study of natural communities will allow new insight to the evolution and impact of phage specificity within complex bacterial communities.
Priority effects in microbiome assembly Debray, Reena; Herbert, Robin A; Jaffe, Alexander L ...
Nature reviews. Microbiology,
02/2022, Volume:
20, Issue:
2
Journal Article
Peer reviewed
Advances in next-generation sequencing have enabled the widespread measurement of microbiome composition across systems and over the course of microbiome assembly. Despite substantial progress in ...understanding the deterministic drivers of community composition, the role of historical contingency remains poorly understood. The establishment of new species in a community can depend on the order and/or timing of their arrival, a phenomenon known as a priority effect. Here, we review the mechanisms of priority effects and evidence for their importance in microbial communities inhabiting a range of environments, including the mammalian gut, the plant phyllosphere and rhizosphere, soil, freshwaters and oceans. We describe approaches for the direct testing and prediction of priority effects in complex microbial communities and illustrate these with re-analysis of publicly available plant and animal microbiome datasets. Finally, we discuss the shared principles that emerge across study systems, focusing on eco-evolutionary dynamics and the importance of scale. Overall, we argue that predicting when and how current community state impacts the success of newly arriving microbial taxa is crucial for the management of microbiomes to sustain ecological function and host health. We conclude by discussing outstanding conceptual and practical challenges that are faced when measuring priority effects in microbiomes.
Coevolution, the process of reciprocal adaptation and counter-adaptation between ecologically interacting species, affects most organisms and is considered a key force structuring biological ...diversity. Our understanding of the pattern and process of coevolution, particularly of antagonistic species interactions, has been hugely advanced in recent years by an upsurge in experimental studies that directly observe coevolution in the laboratory. These experiments pose new questions by revealing novel facets of the coevolutionary process not captured by current theory, while also providing the first empirical tests of longstanding coevolutionary ideas, including the influential Red Queen hypothesis. In this article, we highlight emerging directions for this field, including experimental coevolution of mutualistic interactions and understanding how pairwise coevolutionary processes scale up within species-rich communities.
There is longstanding interest in studying microbial communities below ground, while little attention has historically been paid to the above ground portions of plants (the phyllosphere). The ...phyllosphere has been estimated to make up around 60% of the biomass across all taxa on Earth, making it a key habitat for microbial organisms. The more we study these complex and dynamic communities, the more we come to realize their importance to the health of plant hosts. Overall, the phyllosphere is proving to be both an important microbial habitat and a tractable model system for asking questions in microbial ecology and evolution.
Britt Koskella introduces the phyllosphere, the microbial communities that colonize the above-ground parts of plants.
Interactions between bacteria and bacteriophage viruses (phages) are known to influence pathogen growth and virulence, microbial diversity and even biogeochemical cycling. Lytic phages in particular ...infect and lyse their host cells, and can therefore have significant effects on cell densities as well as competitive dynamics within microbial communities. Despite the known impacts of lytic phages on the ecology and evolution of bacteria in free‐living communities, little is known about the role of lytic phages in host‐associated microbiomes. We set out to characterize the impact of phages in the tomato phyllosphere, that is the bacteria associated with above‐ground plant tissues, by transferring microbial communities from field‐grown tomato plants to juvenile plants grown under mostly sterile conditions in either the presence or absence of their associated phage community. In three separate experiments, we found that the presence of phages affects overall bacterial abundance during colonization of new host plants. Furthermore, bacterial community analysis using 16S rRNA amplicon sequencing shows that phages significantly alter the relative abundance of dominant community members and can influence both within‐ and among‐host diversity. These results underscore the importance of lytic phages in host‐associated microbiomes and are relevant to microbiome transplantation approaches, as they suggest transferring nonbacterial components of the microbiome among hosts is likely to have a strong impact on growth of both the resident and colonizing microbiota.
Predicting the emergence, spread and evolution of parasites within and among host populations requires insight to both the spatial and temporal scales of adaptation, including an understanding of ...within‐host up through community‐level dynamics. Although there are very few pathosystems for which such extensive data exist, there has been a recent push to integrate studies performed over multiple scales or to simultaneously test for dynamics occurring across scales. Drawing on examples from the literature, with primary emphasis on three diverse host–parasite case studies, we first examine current understanding of the spatial structure of host and parasite populations, including patterns of local adaptation and spatial variation in host resistance and parasite infectivity. We then explore the ways to measure temporal variation and dynamics in host–parasite interactions and discuss the need to examine change over both ecological and evolutionary timescales. Finally, we highlight new approaches and syntheses that allow for simultaneous analysis of dynamics across scales. We argue that there is great value in examining interplay among scales in studies of host–parasite interactions.
PDF
