The effect of phage genetic diversity on bacterial resistance evolution

Broniewski, Jenny M.; Meaden, Sean; Paterson, Steve; Buckling, Angus; Westra, Edze R.

doi:10.1038/s41396-019-0577-7

Cited by 55 publications

(55 citation statements)

References 40 publications

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“…Although host cell killing tends to be the key determination for phage therapy, host range is often determined by success or failure of adsorption. Under laboratory conditions, bacteria evolve high levels of CRISPR-based immunity against clonal populations of phages (Common et al, 2019;Broniewski et al, 2020). However, when infected with genetically diverse phage populations, the majority of the bacterial host population evolves a surface modification preventing phage adsorption and providing generalized defense against a broader range of phage genotypes (Broniewski et al, 2020).…”

Section: Escherichia Coli Strains Isolated From Cheese Are Not Lysedmentioning

confidence: 99%

Diversity and Local Coadaptation of Escherichia coli and Coliphages From Small Ruminants

et al. 2020

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Bacteriophages are highly specific predators that drive bacterial diversity through coevolution while striking tradeoffs among preserving host populations for long-term exploitation and increasing their virulence, structural stability, or host range. Escherichia coli and other coliform bacteria present in the microbiota of milk and during early ripening of raw milk cheeses have been linked to the production of gas, manifested by the appearance of eyes, and the development of off-flavors; thus, they might cause early blowing and cheese spoilage. Here, we report the characterization of coliphages isolated from manure from small ruminant farms and E. coli strains isolated from goat and sheep raw milk cheese. Additionally, the virulence and host range of locally isolated and laboratory collection phages were determined by comparing the susceptibility of E. coli strains from different sources. In agreement with the high genetic diversity found within the species E. coli, clustering analysis of whole-cell protein revealed a total of 13 distinct profiles but none of the raw milk cheese isolates showed inhibition of growth by reference or water-isolated coliphages. Conversely, 10 newly isolated phages had a broad host range (i.e., able to lyse ≥50% of bacterial hosts tested), thus exhibiting utility for biocontrol and only one cheese-isolated E. coli strain was resistant to all the phages. Whereas there was a high positive correlation between bacterial susceptibility range and lysis intensity, the phages virulence decreased as range increased until reaching a plateau. These results suggest local gene-for-gene coevolution between hosts and phages with selective tradeoffs for both resistance and competitive ability of the bacteria and host-range extension and virulence of the phage populations. Hence, different phage cocktail formulations might be required when devising long-term and short-term biocontrol strategies.

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Section: Escherichia Coli Strains Isolated From Cheese Are Not Lysedmentioning

confidence: 99%

Diversity and Local Coadaptation of Escherichia coli and Coliphages From Small Ruminants

et al. 2020

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“…Finally, our understanding of the ecological and evolutionary consequences of CRISPR-Cas immune responses is limited to in vitro experiments that lack much of the biotic and abiotic complexity of natural environments. Could it be that the biotic and abiotic complexity of the real world, where communities of microbes include multiple species and strains as well as diversity in phage and plasmids, are spatially structured, and exist in fluctuating environments, is critical to the evolution and maintenance of CRISPR (50,85,(139)(140)(141)? Filling these gaps in our current understanding of CRISPR ecology and evolution requires interdisciplinary approaches that combine observational studies and mathematical and computer simulation models, as well as population and evolutionary dynamics experiments.…”

Section: Discussionmentioning

confidence: 99%

It is unclear how important CRISPR-Cas systems are for protecting natural populations of bacteria against infections by mobile genetic elements

Westra

Levin

2020

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

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Articles on CRISPR commonly open with some variant of the phrase “these short palindromic repeats and their associated endonucleases (Cas) are an adaptive immune system that exists to protect bacteria and archaea from viruses and infections with other mobile genetic elements.” There is an abundance of genomic data consistent with the hypothesis that CRISPR plays this role in natural populations of bacteria and archaea, and experimental demonstrations with a few species of bacteria and their phage and plasmids show that CRISPR-Cas systems can play this role in vitro. Not at all clear are the ubiquity, magnitude, and nature of the contribution of CRISPR-Cas systems to the ecology and evolution of natural populations of microbes and the strength of selection mediated by different types of phage and plasmids to the evolution and maintenance of CRISPR-Cas systems. In this perspective, with the aid of heuristic mathematical–computer simulation models, we explore the a priori conditions under which exposure to lytic and temperate phage and conjugative plasmids will select for and maintain CRISPR-Cas systems in populations of bacteria and archaea. We review the existing literature addressing these ecological and evolutionary questions and highlight the experimental and other evidence needed to fully understand the conditions responsible for the evolution and maintenance of CRISPR-Cas systems and the contribution of these systems to the ecology and evolution of bacteria, archaea, and the mobile genetic elements that infect them.

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“…Finally, our understanding of the ecological and evolutionary consequences of CRISPR-Cas immune responses are limited to in vitro experiments that lack much of the biotic and abiotic complexity of natural environments. Could it be that the biotic and abiotic complexity of the real world, where communities of microbes include multiple species and strains as well as diversity in phage and plasmids, are spatially structured and exist in fluctuating environments are critical to the evolution and maintenance of CRISPR (50,85,139,140)? Filling these gaps in our current understanding of CRISPR ecology and evolution requires interdisciplinary approaches that combine observational studies, mathematical and computer simulation models, as well as population and evolutionary dynamics experiments.…”

Section: Discussionmentioning

confidence: 99%

How important is CRISPR-Cas for protecting natural populations of bacteria against infections by mobile genetic elements?

Westra

Levin

2020

Preprint

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Articles on CRISPR commonly open with some variant of the phrase 'these short-palindromic repeats and their associated endonucleases (Cas) are an adaptive immune system that exists to protect bacteria and archaea from viruses and infections with other deleterious ("badass") DNAs'.There is an abundance of genomic data consistent with the hypothesis that CRISPR plays this role in natural populations of bacteria and archaea, and experimental demonstrations with a few species of bacteria and their phage and plasmids show that CRISPR-Cas systems can play this role in vitro.Not at all clear are the ubiquity, magnitude and nature of the contribution of CRISPR-Cas systems to the ecology and evolution of natural populations of microbes, and the strength of selection mediated by different types of phage and plasmids to the evolution and maintenance of CRISPR-Cas systems. In this perspective, with the aid of heuristic mathematical-computer simulation models, we explore the a priori conditions under which exposure to lytic and temperate phage and conjugative plasmids will select for and maintain CRISPR-Cas systems in populations of bacteria and archaea. We review the existing literature addressing these ecological and evolutionary questions and highlight the experimental and other evidence needed to fully understand the conditions responsible for the evolution and maintenance of CRISPR-Cas systems and the contribution of these systems to the ecology and evolution of bacteria, archaea and the mobile genetic elements that infect them. SignificanceThere is no question about the importance and utility of CRISPR-Cas for editing and modifying genomes. On the other hand, the mechanisms responsible for the evolution and maintenance of these systems and the magnitude of their importance to the ecology and evolution of bacteria, archaea and their infectious DNAs, are not at all clear. With the aid of heuristic mathematical/simulation models and reviews of the existing literature, we raise questions that have to be answered to elucidate the contribution of selection -mediated by phage and plasmids -to the evolution and maintenance of this adaptive immune system and its consequences for the ecology and evolution of prokaryotes and their viruses and plasmids.

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The effect of phage genetic diversity on bacterial resistance evolution

Cited by 55 publications

References 40 publications

Diversity and Local Coadaptation of Escherichia coli and Coliphages From Small Ruminants

Diversity and Local Coadaptation of Escherichia coli and Coliphages From Small Ruminants

It is unclear how important CRISPR-Cas systems are for protecting natural populations of bacteria against infections by mobile genetic elements

How important is CRISPR-Cas for protecting natural populations of bacteria against infections by mobile genetic elements?

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