BACPHLIP: Predicting bacteriophage lifestyle from conserved protein domains

Hockenberry, Adam J.; Wilke, Claus O.

doi:10.1101/2020.05.13.094805

Cited by 6 publications

(6 citation statements)

References 44 publications

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“…2012 ) to predict their lifestyle, having identified 1,161 virulent and 1,336 temperate phages. To control for the difficulties in phage lifestyle assessment, we repeated all the key analyses of this study while restricting the phage data set to the high confidence predictions of PHACTS, and also by using the alternative tool BACPHLIP ( Hockenberry and Wilke 2020 ), which uses an extensive manual curation of the data from Mavrich and Hatfull (2017) . We systematically found similar qualitative results for these controls.…”

Section: Resultsmentioning

confidence: 99%

“…Using these criteria, we classified as confident 54% of the phages into 571 virulent and 780 temperate phages. Alternatively, we used BACPHLIP version 0.9.3 ( Hockenberry and Wilke 2020 ) (default parameters) to predict the lifestyle of each phage, for almost all (>99%) of the genomes. Data for the HGCF and LGCF phages were taken from ( Mavrich and Hatfull 2017 ) by matching the NCBI identifiers.…”

Section: Methodsmentioning

confidence: 99%

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Causes and Consequences of Bacteriophage Diversification via Genetic Exchanges across Lifestyles and Bacterial Taxa

Sousa

Pfeifer

Touchon

et al. 2021

Molecular Biology and Evolution

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Bacteriophages (phages) evolve rapidly by acquiring genes from other phages leading to mosaic genomes. Here, we identify numerous genetic transfers between distantly related phages and aim at understanding their frequency, consequences and the conditions favoring them. Gene flow tends to occur between phages that are enriched for recombinases, transposases and non-homologous end joining, suggesting that both homologous and illegitimate recombination contribute to gene flow. Phage family and host phyla are strong barriers to gene exchange, but phage lifestyle is not. Even if we observe four times more recent transfers between temperate phages than between other pairs, there is extensive gene flow between temperate and virulent phages, and between the latter. These predominantly involve virulent phages with large genomes previously classed as low gene flux, and lead to the preferential transfer of genes encoding functions involved in cell energetics, nucleotide metabolism, DNA packaging and injection, and virion assembly. Such exchanges may contribute to the observed twice larger genomes of virulent phages. We used genetic transfers, which occur upon co-infection of a host, to compare phage host range. We found that virulent phages have broader host ranges and can mediate genetic exchanges between narrow host range temperate phages infecting distant bacterial hosts, thus contributing to gene flow between virulent phages, as well as between temperate phages. This gene flow drastically expands the gene repertoires available for phage and bacterial evolution, including the transfer of functional innovations across taxa.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Causes and Consequences of Bacteriophage Diversification via Genetic Exchanges across Lifestyles and Bacterial Taxa

Sousa

Pfeifer

Touchon

et al. 2021

Molecular Biology and Evolution

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“…We analysed a dataset of 2487 complete phage genome sequences and used PHACTS (McNair et al 2012) to predict their lifestyle, having identified 1161 virulent and 1336 temperate phages. To control for the difficulties in phage lifestyle assessment, we repeated all the key analyses of this study while restricting the phage dataset to the high confidence predictions of PHACTS, and using the alternative tool BACPHLIP (Hockenberry and Wilke 2020), which uses an extensive manual curation of the data from (Mavrich and Hatfull 2017)).…”

Section: Resultsmentioning

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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“…However, this approach may obscure important differences in how natural selection operates on the translation-initiation regions of different phages. We thus predicted the lifestyle of each phage genome in the dataset using BACPHLIP [58] and noticed a striking difference between phages that are confidently predicted (≥ 0.95% probability) to be either temperate or virulent (n=143, of which 39 are temperate and 104 are virulent, Fig. 2B).…”

Section: Sequence Features In Translation-initiation Regions Differ Between Virulent and Temperate Phagesmentioning

confidence: 99%

“…We used the BACPHLIP software [58] to categorize all phage genomes in our dataset into temperate and virulent lifestyles. BACPHLIP uses genome-sequence input, determines the presence/absence of several hundred lysogeny-associated protein domains, and uses a random forest classifier return a probability of the given phage being either temperate or virulent.…”

Section: Phage Lifestyle Predictionmentioning

confidence: 99%

Virulent but not temperate bacteriophages display hallmarks of rapid translation initiation

Hockenberry

Weaver

Wilke

2021

Preprint

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Bacteriophages rely almost exclusively on host-cell machinery to produce their proteins, and their mRNAs must therefore compete with host mRNAs for valuable translational resources. In many bacterial species, highly translated mRNAs are characterized by the presence of a Shine-Dalgarno sequence motif upstream of the start codon and weak secondary structure within the start codon region. However, the general constraints and principles underlying the translation of phage mRNAs are largely unknown. Here, we show that phage mRNAs are highly enriched in strong Shine-Dalgarno sequences and have comparatively weaker secondary structures in the start codon region than host-cell mRNAs. Phage mRNAs appear statistically similar to the most highly expressed host genes in E. coli according to both features, strongly suggesting that they initiate translation at particularly high rates. Interestingly, we find that these observations are driven largely by virulent phages and that temperate phages encode mRNAs with similar start codon features to their host genes. These findings apply broadly across a wide-diversity of host-species and phage genomes. Further study of phage translational regulation — with a particular emphasis on virulent phages — may provide new strategies for engineering phage genomes and recombinant expression systems more generally.

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BACPHLIP: Predicting bacteriophage lifestyle from conserved protein domains

Cited by 6 publications

References 44 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

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

Virulent but not temperate bacteriophages display hallmarks of rapid translation initiation

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