Although it is generally accepted that phages drive bacterial evolution, how these dynamics play out in the wild remains poorly understood. We found that susceptibility to viral killing in marine Vibrio is mediated by large and highly diverse mobile genetic elements. These phage defense elements display exceedingly fast evolutionary turnover, resulting in differential phage susceptibility among clonal bacterial strains while phage receptors remain invariant. Protection is cumulative, and a single bacterial genome can harbor 6 to 12 defense elements, accounting for more than 90% of the flexible genome among close relatives. The rapid turnover of these elements decouples phage resistance from other genomic features. Thus, resistance to phages in the wild follows evolutionary trajectories alternative to those predicted from laboratory-based evolutionary experiments.

Rapid evolutionary turnover of mobile genetic elements drives bacterial resistance to phages

Coevolution between bacteriophages (phages) and their bacterial hosts occurs through changes in resistance and counter-resistance mechanisms. To assess phage-host evolution in wild populations, we isolated 195 Vibrio crassostreae strains and 243 vibriophages during a 5-month time series from an oyster farm and combined these isolates with existing V. crassostreae and phage isolates. Cross-infection studies of 81,926 host-phage pairs delineated a modular network where phages are best at infecting co-occurring hosts, indicating local adaptation. Successful propagation of phage is restricted by the ability to adsorb to closely related bacteria and further constrained by strain-specific defence systems. These defences are highly diverse and predominantly located on mobile genetic elements, and multiple defences are active within a single genome. We further show that epigenetic and genomic modifications enable phage to adapt to bacterial defences and alter host range. Our findings reveal that the evolution of bacterial defences and phage counter-defences is underpinned by frequent genetic exchanges with, and between, mobile genetic elements. 

https://hal.univ-brest.fr/hal-04084906/document

Phage–host coevolution in natural populations

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.

https://www.annualreviews.org/doi/pdf/10.1146/annurev-virology-091919-075914

Understanding the Impacts of Bacteriophage Viruses: From Laboratory Evolution to Natural Ecosystems.

https://doi.org/10.1016/j.celrep.2023.112048

Genetic determinants of host tropism in Klebsiella phages

Abstract Soil viruses remain understudied when compared to virus found in aquatic ecosystems. Here, we investigate the ecological patterns of soil viral communities across various land use types encompassing forest, agricultural, and urban soil in Xiamen, China. We recovered 59,626 viral operational taxonomic units (vOTUs) via size-fractioned viromic approach with additional mitomycin C treatment to induce virus release from bacterial fraction. Our results show that viral communities are significantly different amongst the land use types considered. A microdiversity analysis indicates that selection act on soil vOTUs, resulting in disparities between land use associated viral communities. Soil pH is one of the major determinants of viral community structure, associated with changes of in-silico predicted host compositions of soil vOTUs. Habitat disturbance and variation of soil moisture potentially contribute to the dynamics of putative lysogenic vOTUs. These findings provide mechanistic understandings of the ecology and evolution of soil viral communities in changing environments. 

/pdf/response-of-soil-viral-communities-to-land-use-changes-1hxespmm.pdf

Response of soil viral communities to land use changes

We commonly acknowledge that bacterial viruses (phages) shape the composition and evolution of bacterial communities in nature and therefore have important roles in ecosystem functioning. This view stems from studies in the 1990s to the first decade of the twenty-first century that revealed high viral abundance, high viral diversity and virus-induced microbial death in aquatic ecosystems as well as an association between collapses in bacterial density and peaks in phage abundance. The recent surge in metagenomic analyses has provided deeper insight into the abundance, genomic diversity and spatio-temporal dynamics of phages in a wide variety of ecosystems, ranging from deep oceans to soil and the mammalian digestive tract. However, the causes and consequences of variations in phage community compositions remain poorly understood. In this Review, we explore current knowledge of the composition and evolution of phage communities, as well as their roles in controlling the population and evolutionary dynamics of bacterial communities. We discuss the need for greater ecological realism in laboratory studies to capture the complexity of microbial communities that thrive in natural environments.

Benoît J Pons

Papers

Interactions between bacterial and phage communities in natural environments.