Rates of Mutation and Recombination in Siphoviridae Phage Genome Evolution over Three Decades

Kupczok, Anne; Neve, Horst; Huang, Kun; Hoeppner, Marc P.; Heller, Knut J.; Franz, Charles M. A. P.

doi:10.1093/molbev/msy027

Cited by 68 publications

(70 citation statements)

References 99 publications

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“…Interestingly, even in bacteria and archaea, which have traditionally been regarded as essentially non-recombining, the majority of species displays values of r/µ that are significantly larger than one [73][74][75]. Similarly, a recent study of the evolution of Siphoviridae phages revealed a ratio of recombination events to mutational substitutions of about 24 [76]. In eukaryotes this ratio is expected to be considerably higher [40].…”

Section: Discussionmentioning

confidence: 99%

Recombination and mutational robustness in neutral fitness landscapes

2019

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Mutational robustness quantifies the effect of random mutations on fitness. When mutational robustness is high, most mutations do not change fitness or have only a minor effect on it. From the point of view of fitness landscapes, robust genotypes form neutral networks of almost equal fitness. Using deterministic population models it has been shown that selection favors genotypes inside such networks, which results in increased mutational robustness. Here we demonstrate that this effect is massively enhanced by recombination. Our results are based on a detailed analysis of mesa-shaped fitness landscapes, where we derive precise expressions for the dependence of the robustness on the landscape parameters for recombining and non-recombining populations. In addition, we carry out numerical simulations on different types of random holey landscapes as well as on an empirical fitness landscape. We show that the mutational robustness of a genotype generally correlates with its recombination weight, a new measure that quantifies the likelihood for the genotype to arise from recombination. We argue that the favorable effect of recombination on mutational robustness is a highly universal feature that may have played an important role in the emergence and maintenance of mechanisms of genetic exchange.

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Section: Discussionmentioning

confidence: 99%

Recombination and mutational robustness in neutral fitness landscapes

2019

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“…Nevertheless, some cases have been studied in detail. Evolution of virulent phages of Lactococcus lactis from a dairy production line showed that recombination brings more polymorphism than point mutations to their genomes (25), and studies on T4 and T7 phages revealed events of recombination and gene accretion (26, 27). Much less is known regarding genetic exchanges between temperate and virulent phages, even if they are assumed to be rare.…”

Section: Introductionmentioning

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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“…The analysis was performed using the multi-gene alignment described previously, and a fixed mean substitution rate, since these crAssphage strains are mostly contemporaneous. Because a substitution rate for crAssphage or other Podoviridae bacteriophages has not been estimated as of yet, we used a rate of 1.9 x 10 -4 substitutions per site per year as estimated for bacteriophages in the family Siphoviridae [48], the members of which also infect bacteria and archaea. Our Bayesian Skyline plot (BSP) (S3 Fig) shows that crAssphage strains underwent an expansion event likely within the past 200 years.…”

Section: Resultsmentioning

confidence: 99%

“…To estimate the timing of a potential population expansion among crAssphage sequences, the multi-gene alignment was used as input for BEAST v1.8.4 [47]. Since substitution rates for crAssphage or crAss-like phages remain undetermined, we used a substitution rate of 1.9 x 10 -4 substitutions per site per year as estimated for bacteriophages belonging to the Siphoviridae family [48]. We used a GTR+G+I model of nucleotide substitution, an uncorrelated lognormal clock model with uniform rate across branches, and a Bayesian Coalescent Skyline plot tree prior.…”

Section: Methodsmentioning

confidence: 99%

Biogeographic study of human gut-associated crAssphage suggests impacts from industrialization and recent expansion

Honap

Sankaranarayanan

Schnorr

et al. 2018

Preprint

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31CrAssphage (cross-assembly phage) is a bacteriophage that was first discovered in 32 human gut metagenomic data. CrAssphage belongs to a diverse family of crAss-like 33 bacteriophages thought to infect gut commensal bacteria belonging to Bacteroides species. 34However, not much is known about the biogeography of crAssphage and whether certain strains 35 are associated with specific human populations. In this study, we screened publicly available 36 human gut metagenomic data from 3,341 samples for the presence of crAssphage sensu stricto 37 (NC_024711.1). We found that crAssphage prevalence is low in traditional, hunter-gatherer 38 populations, such as the Hadza from Tanzania and Matses from Peru, as compared to 39 industrialized, urban populations. Statistical comparisons showed no association of crAssphage 40 prevalence with variables such as age, sex, body mass index, and health status of individuals. 41Phylogenetic analyses show that crAssphage strains reconstructed from the same individual over 42 multiple time-points, cluster together. CrAssphage strains from individuals from the same study 43 population do not always cluster together. Some evidence of clustering is seen at the level of 44 broadly defined geographic regions, however, the relative positions of these clusters within the 45 crAssphage phylogeny are not well-supported. We hypothesize that this lack of strong 46 biogeographic structuring is suggestive of a recent expansion event within crAssphage. Using a 47Bayesian dating approach, we estimate this expansion has occurred within the past 200 years. 48Overall, we determine that crAssphage presence is associated with an industrialized lifestyle. 49The absence of strong biogeographic structuring within global crAssphage strains is likely due to 50 a recent population expansion within this bacteriophage. 51 52

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Rates of Mutation and Recombination in Siphoviridae Phage Genome Evolution over Three Decades

Cited by 68 publications

References 99 publications

Recombination and mutational robustness in neutral fitness landscapes

Recombination and mutational robustness in neutral fitness landscapes

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

Biogeographic study of human gut-associated crAssphage suggests impacts from industrialization and recent expansion

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