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1. The impact of phage and phage resistance on microbial community dynamics

   https://doi.org/10.1371/journal.pbio.3002346  

   Alseth, Ellinor O; Custodio, Rafael; Sundius, Sarah A; Kuske, Rachel A; Brown, Sam P; Westra, Edze R (April 2024, PLOS Biology)

   Barr, Jeremy J (Ed.)

   Where there are bacteria, there will be bacteriophages. These viruses are known to be important players in shaping the wider microbial community in which they are embedded, with potential implications for human health. On the other hand, bacteria possess a range of distinct immune mechanisms that provide protection against bacteriophages, including the mutation or complete loss of the phage receptor, and CRISPR-Cas adaptive immunity. While our previous work showed how a microbial community may impact phage resistance evolution, little is known about the inverse, namely how interactions between phages and these different phage resistance mechanisms affect the wider microbial community in which they are embedded. Here, we conducted a 10-day, fully factorial evolution experiment to examine how phage impact the structure and dynamics of an artificial four-species bacterial community that includes eitherPseudomonas aeruginosawild-type or an isogenic mutant unable to evolve phage resistance through CRISPR-Cas. Additionally, we used mathematical modelling to explore the ecological interactions underlying full community behaviour, as well as to identify general principles governing the impacts of phage on community dynamics. Our results show that the microbial community structure is drastically altered by the addition of phage, withAcinetobacter baumanniibecoming the dominant species andP.aeruginosabeing driven nearly extinct, whereasP.aeruginosaoutcompetes the other species in the absence of phage. Moreover, we find that aP.aeruginosastrain with the ability to evolve CRISPR-based resistance generally does better when in the presence ofA.baumannii, but that this benefit is largely lost over time as phage is driven extinct. Finally, we show that pairwise data alone is insufficient when modelling our microbial community, both with and without phage, highlighting the importance of higher order interactions in governing multispecies dynamics in complex communities. Combined, our data clearly illustrate how phage targeting a dominant species allows for the competitive release of the strongest competitor while also contributing to community diversity maintenance and potentially preventing the reinvasion of the target species, and underline the importance of mapping community composition before therapeutically applying phage. 

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2. Biofilm Structure Promotes Coexistence of Phage-Resistant and Phage-Susceptible Bacteria

   https://doi.org/10.1128/mSystems.00877-19  

   Simmons, Emilia L.; Bond, Matthew C.; Koskella, Britt; Drescher, Knut; Bucci, Vanni; Nadell, Carey D. (June 2020, mSystems)

   Bordenstein, Seth (Ed.)

   ABSTRACT Encounters among bacteria and their viral predators (bacteriophages) are among the most common ecological interactions on Earth. These encounters are likely to occur with regularity inside surface-bound communities that microbes most often occupy in natural environments. Such communities, termed biofilms, are spatially constrained: interactions become limited to near neighbors, diffusion of solutes and particulates can be reduced, and there is pronounced heterogeneity in nutrient access and physiological state. It is appreciated from prior theoretical work that phage-bacteria interactions are fundamentally different in spatially structured contexts, as opposed to well-mixed liquid culture. Spatially structured communities are predicted to promote the protection of susceptible host cells from phage exposure, and thus weaken selection for phage resistance. The details and generality of this prediction in realistic biofilm environments, however, are not known. Here, we explore phage-host interactions using experiments and simulations that are tuned to represent the essential elements of biofilm communities. Our simulations show that in biofilms, phage-resistant cells—as their relative abundance increases—can protect clusters of susceptible cells from phage exposure, promoting the coexistence of susceptible and phage-resistant bacteria under a large array of conditions. We characterize the population dynamics underlying this coexistence, and we show that coexistence is recapitulated in an experimental model of biofilm growth measured with confocal microscopy. Our results provide a clear view into the dynamics of phage resistance in biofilms with single-cell resolution of the underlying cell-virion interactions, linking the predictions of canonical theory to realistic models and in vitro experiments of biofilm growth. IMPORTANCE In the natural environment, bacteria most often live in communities bound to one another by secreted adhesives. These communities, or biofilms, play a central role in biogeochemical cycling, microbiome functioning, wastewater treatment, and disease. Wherever there are bacteria, there are also viruses that attack them, called phages. Interactions between bacteria and phages are likely to occur ubiquitously in biofilms. We show here, using simulations and experiments, that biofilms will in most conditions allow phage-susceptible bacteria to be protected from phage exposure, if they are growing alongside other cells that are phage resistant. This result has implications for the fundamental ecology of phage-bacteria interactions, as well as the development of phage-based antimicrobial therapeutics. 

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3. A cytoskeletal vortex drives phage nucleus rotation during jumbo phage replication in E. coli

   https://doi.org/10.1016/j.celrep.2022.111179  

   Birkholz, Erica A.; Laughlin, Thomas G.; Armbruster, Emily; Suslov, Sergey; Lee, Jina; Wittmann, Johannes; Corbett, Kevin D.; Villa, Elizabeth; Pogliano, Joe (August 2022, Cell Reports)
4. Renaissance for Phage-Based Bacterial Control

   https://doi.org/10.1021/acs.est.1c06232  

   Schwarz, Cory; Mathieu, Jacques; Laverde Gomez, Jenny A.; Yu, Pingfeng; Alvarez, Pedro J. (November 2021, Environmental Science & Technology)
5. Pattern formation by bacteria-phage interactions

   https://doi.org/10.1101/2023.09.19.558479  

   Martínez-Calvo, Alejandro; Wingreen, Ned S; Datta, Sujit S (September 2023, bioRxiv)

   The interactions between bacteria and phages—viruses that infect bacteria—play critical roles in agriculture, ecology, and medicine; however, how these interactions influence the spatial organization of both bacteria and phages remain largely unexplored. Here, we address this gap in knowledge by developing a theoretical model of motile, proliferating bacteria that aggregate via motility-induced phase separation (MIPS) and encounter phage that infect and lyse the cells. We find that the non-reciprocal predator-prey interactions between phage and bacteria strongly alter spatial organization, in some cases giving rise to a rich array of finite-scale stationary and dynamic patterns in which bacteria and phage coexist. We establish principles describing the onset and characteristics of these diverse behaviors, thereby helping to provide a biophysical basis for understanding pattern formation in bacteria-phage systems, as well as in a broader range of active and living systems with similar predator-prey or other non-reciprocal interactions. 

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