Virulent coliphages in 1-year-old children fecal samples are fewer, but more infectious than temperate coliphages

Mathieu, Aurélie; Dion, Moïra B.; Deng, Ling; Tremblay, Denise M.; Moncaut, Elisabeth; Shah, Samir A.; Stokholm, Jakob; Krogfelt, Karen A.; Schjørring, Susanne; Bisgaard, Hans; Nielsen, Dennis Sandris; Moineau, Sylvain; Petit, Marie-Agnès

doi:10.1038/s41467-019-14042-z

Cited by 71 publications

(85 citation statements)

References 72 publications

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“…There is some published evidence on differences in host ranges between temperate and virulent phages. For example, virulent coliphages isolated from the faeces of toddlers infect a broader range of gut strains than temperate ones (49). The implications of our findings are that groups of temperate phages that might be sexually isolated (because they infect phylogenetically distant hosts) can exchange genes indirectly through recombination with broader host range virulent phages.…”

Section: Discussionmentioning

confidence: 99%

Causes and consequences of bacteriophage diversification via genetic exchanges across lifestyles and bacterial taxa

Sousa

Pfeifer

Touchon

et al. 2020

Preprint

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11 12Bacteriophages (henceforth phages) evolve by mutation and recombination. Temperate 13 phages are known to evolve rapidly by genetic exchanges. In contrast, recombination events 14 between virulent and between temperate and virulent phages have rarely been reported. A 15 gene flow barrier between these two large distinct groups of phages could affect the ability of 16 phages to acquire novel functions. Here, we show that genomes of temperate and virulent 17 phages are very distinct but often have a few almost identical genes. These cases are due to 18 recent genetic exchanges of both phage-like and bacterial-like genes. These exchanges were 19 probably mediated by phage recombinases with low homology requirements and mechanisms 20 of non-homologous end joining, since both were over-represented in recombinant phages and 21 their hosts. When assessing the impact of gene flow across the two populations of phages we 22 realized that temperate phages have narrower host ranges than virulent phages. This 23 suggests, and we find some evidence, that gene flow between temperate phages infecting 24 distant bacterial hosts might be mediated by recombination with the broader host virulent 25 phages. Hence, gene flow across phages with distinct lifestyles could drastically increase the 26 gene repertoire available for phage evolution, including the transfer of functional innovations 27 across taxa. These results also have implications for bacterial evolution because of the impact 28 of phage predation in bacterial population dynamics and the contribution of temperate phages 29 to the evolution of bacterial gene repertoires. 31 SIGNIFICANCE STATEMENT 33Many microbial communities are intensely predated by temperate and virulent 34 bacteriophages. The former also contribute to bacterial gene repertoires. Gene transfers 35 between bacteriophages favor their rapid adaptation, but are thought to occur rarely between 36 virulent and temperate bacteriophages because their genomes are very different in terms of 37 gene repertoires and genetic organization. We found that genetic exchanges occur frequently 38 3 between these types of bacteriophages, involve different phage and bacterial functions, and 39 are likely due to multiple DNA repair processes. Since we show that virulent bacteriophages 40 have broader host ranges, they can shuttle genes between temperate bacteriophages present 41 in taxa that are beyond the typical range of the latter. This enhances phages diversification 42 and has multiple impacts on bacterial evolution. 43 65 accretion in virulent phages, even if some families of virulent phages have remarkable 66 diversity in their genomes' size, suggesting the existence of mechanisms of gene exchange 67 (12). The genomic plasticity of temperate lambdoid phages has been much more extensively 68 studied (9, 13, 14). Their analyses reveal that pairs of phages tend to have patches of regions 69 of very similar sequences within genomes that are often very dissimilar. This genome 70 mosaicism is facilitated by the modular or...

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Section: Discussionmentioning

confidence: 99%

Causes and consequences of bacteriophage diversification via genetic exchanges across lifestyles and bacterial taxa

Sousa

Pfeifer

Touchon

et al. 2020

Preprint

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“…As described later, for comparative purposes, we also performed high-throughput genetic assays in the E. coli BL21 strain background. Despite E. coli being a well-studied model organism [78,79], there are significant knowledge gaps regarding gene function [80] and phage interaction mechanisms [26,27,46,81,82]. Different serotypes of E. coli are also important pathogens with significant global threat and are crucial players in specific human-relevant ecologies [83][84][85], leading to the question of whether strain variation is also important in predicting the response to phage-mediated selection or whether the mechanisms are likely to be conserved.…”

Section: Mapping Genetic Determinants Of Phage Resistance Using High-mentioning

confidence: 99%

“…Despite nearly a century of pioneering molecular work, the mechanistic insights into phage specificity for a given host, infection pathways, and the breadth of bacterial responses to different phages have largely focused on a handful of individual bacterium-phage systems [9][10][11][12][13]. Bacterial sensitivity/resistance to phages is typically characterized using phenotypic methods such as cross-infection patterns against a panel of phages [14][15][16][17][18][19][20][21][22][23][24][25][26][27] or by whole-genome sequencing of phage-resistant mutants [28][29][30][31][32]. As such, our understanding of bacterial resistance mechanisms against phages remains limited, and the field is therefore in need of improved methods to characterize phage-host interactions, determine the generality and diversity of phage resistance mechanisms in nature, and identify the degree of specificity for each bacterial resistance mechanism across diverse phage types [13,25,26,[33][34][35][36][37][38][39][40][41][42][43][44][45][46][47].…”

Section: Introductionmentioning

confidence: 99%

High-throughput mapping of the phage resistance landscape inE. coli

Mutalik¹,

Adler²,

Rishi³

et al. 2020

Preprint

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Bacteriophages (phages) are critical players in the dynamics and function of microbial communities and drive processes as diverse as global biogeochemical cycles and human health. Phages tend to be predators finely tuned to attack specific hosts, even down to the strain level, which in turn defend themselves using an array of mechanisms. However, to date, efforts to rapidly and comprehensively identify bacterial host factors important in phage infection and resistance have yet to be fully realized. Here, we globally map the host genetic determinants involved in resistance to 14 phylogenetically diverse double-stranded DNA phages using two model Escherichia coli strains (K-12 and BL21) with known sequence divergence to demonstrate strain-specific differences. Using genome-wide loss-of-function and gain-of-function genetic technologies, we are able to confirm previously described phage receptors as well as uncover a number of previously unknown host factors that confer resistance to one or more of these phages. We uncover differences in resistance factors that strongly align with the susceptibility of K-12 and BL21 to specific phage. We also identify both phage specific mechanisms, such as the unexpected role of cyclic-di-GMP in host sensitivity to phage N4, and more generic defenses, such as the overproduction of colanic acid capsular polysaccharide that defends against a wide array of phages. Our results indicate that host responses to phages can occur via diverse cellular mechanisms. Our systematic and highthroughput genetic workflow to characterize phage-host interaction determinants can be extended to diverse bacteria to generate datasets that allow predictive models of how phagemediated selection will shape bacterial phenotype and evolution. The results of this study and future efforts to map the phage resistance landscape will lead to new insights into the coevolution of hosts and their phage, which can ultimately be used to design better phage therapeutic treatments and tools for precision microbiome engineering.3 Introduction:

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“…These results are especially pertinent for K.pneumoniae in clinical settings because many antibiotics stimulate prophage induction(Allen et al 2011, Otsuji et al 1959, Wagner and Waldor 2002 and facilitate phage infection(Comeau et al 2007, Kim et al 2018. Also, phages in the mammalian gut, the most frequent habitat of K. pneumoniae, tend to be temperate and result from in situ prophage induction(De Paepe et al 2016, Mathieu et al 2020.…”

mentioning

confidence: 99%

Modular prophage interactions driven by capsule serotype select for capsule loss under phage predation

Sousa

Nucci

Haudiquet

et al. 2019

Preprint

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Klebsiella species are able to colonize a wide range of environments and include worrisome nosocomial pathogens. Here, we sought to determine the abundance and infectivity of prophages of Klebsiella to understand how the interactions between induced prophages and bacteria affect population dynamics and evolution. We identified many prophages in the species, placing these taxa among the top 5% of the most polylysogenic bacteria. We selected 35 representative strains of the Klebsiella pneumoniae species complex to establish a network of induced phage-bacteria interactions. This revealed that many prophages are able to enter the lytic cycle, and subsequently kill or lysogenize closely-related Klebsiella strains. Although 60% of the tested strains could produce phages that infect at least one other strain, the interaction network of all pairwise cross-infections is very sparse and mostly organized in modules corresponding to the strains capsule serotypes. Accordingly, capsule mutants remain uninfected showing that the capsule is a key factor for successful infections. Surprisingly, experiments in which bacteria are predated by their own prophages result in accelerated loss of the capsule. Our results show that phage infectiousness defines interaction modules between small subsets of phages and bacteria in function of capsule serotype. This limits the role of prophages as competitive weapons because they can infect very few strains of the species complex. This should also restrict phage-driven gene flow across the species. Finally, the accelerated loss of the capsule in bacteria being predated by their own phages, suggests that phages drive serotype switch in nature.

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Virulent coliphages in 1-year-old children fecal samples are fewer, but more infectious than temperate coliphages

Cited by 71 publications

References 72 publications

Causes and consequences of bacteriophage diversification via genetic exchanges across lifestyles and bacterial taxa

Causes and consequences of bacteriophage diversification via genetic exchanges across lifestyles and bacterial taxa

High-throughput mapping of the phage resistance landscape inE. coli

Modular prophage interactions driven by capsule serotype select for capsule loss under phage predation

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