Bacteria-Phage Antagonistic Coevolution in Soil

Gómez, Pedro Sánchez; Buckling, Angus

doi:10.1126/science.1198767

Cited by 412 publications

(412 citation statements)

References 26 publications

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“…Some of the prime experimental models are bacteria and their lytic phages, which exhibit rapid evolution and are amenable to time-shift tests. Recent study indicates that coevolving populations may exhibit either ARD or FSD (12,(21)(22)(23)(24), and there is some evidence for the genetic mechanism involved [e.g., mutations at tail fiber genes (12,25)] and for the expansion of the phage host range as coevolution proceeds (6). Most studies of bacteria-phage coevolution involve the model system Pseudomonas fluorescens SBW25 and its lytic phage ϕ2 (15).…”

mentioning

confidence: 99%

Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

Betts

Kaltz

Hochberg

2014

Proc. Natl. Acad. Sci. U.S.A.

100

101

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Significance Scientists have long debated the dynamic form of perpetual reciprocal adaptations, or coevolution, between hosts and their parasites. The two main types of antagonistic coevolution described to date are arms race dynamics, in which interaction traits escalate through time, and fluctuating selection dynamics, in which traits cycle through time. We used experimental evolution between Pseudomonas aeruginosa and a panel of its lytic phages and found the full known range of coevolutionary dynamics. We argue that the coevolutionary pattern is determined by whether phages typically adsorb directly to receptors on the bacterial outer membrane or instead use retractable type IV pili as a primary or alternative site. Our results have applications in the use of phages as therapeutics or disinfectants to control bacterial pathogens.

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mentioning

confidence: 99%

Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

Betts

Kaltz

Hochberg

2014

Proc. Natl. Acad. Sci. U.S.A.

100

101

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“…While there is considerable evidence for coevolutionary arms races taking place among bacteria and phages (Bohannan and Lenski 2000;Buckling and Rainey 2002a;Mizoguchi et al 2003;Brockhurst et al 2006;Forde et al 2008;Scanlan et al 2011) and various other host-parasite systems (Little et al 2006;Schulte et al 2010), there is limited evidence of fluctuations in range except for some plantfungus interactions (e.g., Thrall and Burdon 2003). Recent work with Pseudomonas fluorescens and lytic phages has shown that fluctuating selection between genotypes with similar ranges is possible, either following or in the absence of a coevolutionary arms race (Gomez and Buckling 2011). In addition, the frequent occurrence of local adaptation indicates that there may be multiple routes to generalism (Buckling and Rainey 2002b;Morgan et al 2005;Vos et al 2009;Koskella et al 2011).…”

Section: Resultsmentioning

confidence: 99%

Spatial Structure Mitigates Fitness Costs in Host-Parasite Coevolution

Ashby

Gupta

Buckling

2014

The American Naturalist

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JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. Online enhancements: appendixes, code files. abstract:The extent of population mixing is known to influence the coevolutionary outcomes of many host and parasite traits, including the evolution of generalism (the ability to resist or infect a broad range of genotypes). While the segregation of populations into interconnected demes has been shown to influence the evolution of generalism, the role of local interactions between individuals is unclear. Here, we combine an individual-based model of microbial communities with a well-established framework of genetic specificity that matches empirical observations of bacterium-phage interactions. We find the evolution of generalism in well-mixed populations to be highly sensitive to the severity of associated fitness costs, but the constraining effect of costs on the evolution of generalism is lessened in spatially structured populations. The contrasting outcomes between the two environments can be explained by different scales of competition (i.e., global vs. local). These findings suggest that local interactions may have important effects on the evolution of generalism in host-parasite interactions, particularly in the presence of high fitness costs.

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“…Continuous supply and migration of resistant bacteria from biofilms would have then likely increased the proportion of resistant bacteria also in planktonic populations leading to nonobservable coevolutionary dynamics. It has also been shown that spatially structured soil environments could favour fluctuating coevolutionary dynamics and local phage–bacteria adaptation in time (Gomez & Buckling, 2011), while spatial structure could decrease bacteria–phage encounter rates leading to slower rate of coevolution (Brockhurst et al., 2006). In future, it would be interesting to test directly how the absence and presence of spatial refugees affect the host–parasite coevolutionary dynamics.…”

Section: Discussionmentioning

confidence: 99%

Rapid evolution of generalized resistance mechanisms can constrain the efficacy of phage–antibiotic treatments

Moulton‐Brown

Friman

2018

Evolutionary Applications

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Antimicrobial resistance has been estimated to be responsible for over 700,000 deaths per year; therefore, new antimicrobial therapies are urgently needed. One way to increase the efficiency of antibiotics is to use them in combination with bacteria‐specific parasitic viruses, phages, which have been shown to exert additive or synergistic effects in controlling bacteria. However, it is still unclear to what extent these combinatory effects are limited by rapid evolution of resistance, especially when the pathogen grows as biofilm on surfaces typical for many persistent and chronic infections. To study this, we used a microcosm system, where genetically isogenic populations of Pseudomonas aeruginosa PAO1 bacterial pathogen were exposed to a phage 14/1, gentamycin or a combination of them both in a spatially structured environment. We found that even though antibiotic and phage–antibiotic treatments were equally effective at controlling bacteria in the beginning of the experiment, combination treatment rapidly lost its efficacy in both planktonic and biofilm populations. In a mechanistic manner, this was due to rapid resistance evolution: While both antibiotic and phage selected for increased resistance on their own, phage selection correlated positively with increase in antibiotic resistance, while biofilm growth, which provided generalized resistance mechanism, was favoured most in the combination treatment. Only relatively small cost of resistance and weak evidence for coevolutionary dynamics were observed. Together, these results suggest that spatial heterogeneity can promote rapid evolution of generalized resistance mechanisms without corresponding increase in phage infectivity, which could potentially limit the effectiveness of phage–antibiotic treatments in the evolutionary timescale.

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Bacteria-Phage Antagonistic Coevolution in Soil

Cited by 412 publications

References 26 publications

Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

Spatial Structure Mitigates Fitness Costs in Host-Parasite Coevolution

Rapid evolution of generalized resistance mechanisms can constrain the efficacy of phage–antibiotic treatments

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