PhageWeb – Web Interface for Rapid Identification and Characterization of Prophages in Bacterial Genomes

Sousa, Ailton Lopes de; Maués, Dener; Lobato, Amália Raiana Fonseca; Franco, Edian F.; Pinheiro, Kenny C.; Araújo, Fabrício Almeida; Pantoja, Yan; Silva, Artur da Costa da Luiz; Morais, Jefferson; Ramos, Rommel Thiago Jucá

doi:10.3389/fgene.2018.00644

Cited by 32 publications

(19 citation statements)

References 33 publications

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“…For the VANA approach, a low efficiency of detection was observed for viruses or families with low titer and/or less stable particles, although Closteroviridae, which are known to have quite labile particles, have been detected here and elsewhere (33,47). It should be mentioned that the excess of reads annotated as having a bacterial origin detected in two sites by VANA may in fact represent the detection of phages, since many integrated phages, which can make up to 10% to 20% of bacterial genomes (48,49), have been sequenced and annotated as part of bacterial genomes. Overall, the results obtained would, however, point to a limited presence of phage in the analyzed plant-associated viromes.…”

Section: Discussionmentioning

confidence: 99%

Phytovirome Analysis of Wild Plant Populations: Comparison of Double-Stranded RNA and Virion-Associated Nucleic Acid Metagenomic Approaches

Marais

Lefebvre

et al. 2019

J Virol

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Metagenomic studies have indicated that the diversity of plant viruses was until recently far underestimated. As important components of ecosystems, there is a need to explore the diversity and richness of the viruses associated with plant populations and to understand the drivers shaping their diversity in space and time. Two viral sequence enrichment approaches, double-stranded RNA (dsRNA) and virion-associated nucleic acids (VANA), have been used and compared here for the description of the virome of complex plant pools representative of the most prevalent plant species in unmanaged and cultivated ecosystems. A novel bioinformatics strategy was used to assess viral richness not only at the family level but also by determining operational taxonomic units (OTU) following the clustering of conserved viral domains. A large viral diversity dominated by novel dsRNA viruses was detected in all sites, while a large between-site variability limited the ability to draw a clear conclusion on the impact of cultivation. A trend for a higher diversity of dsRNA viruses was nevertheless detected in unmanaged sites (118 versus 77 unique OTUs). The dsRNA-based approach consistently revealed a broader and more comprehensive diversity for RNA viruses than the VANA approach, whatever the assessment criterion. In addition, dissimilarity analyses indicated both approaches to be largely reproducible but not necessarily convergent. These findings illustrate features of phytoviromes in various ecosystems and a novel strategy for precise virus richness estimation. These results allow us to reason methodological choices in phytovirome studies and likely in other virome studies where RNA viruses are the focal taxa. IMPORTANCE There are today significant knowledge gaps on phytovirus populations and on the drivers impacting them but also on the comparative performance-methodological approaches for their study. We used and compared two viral sequence enrichment approaches, double-stranded RNAs (dsRNA) and virion-associated nucleic acids (VANA), for phytovirome description in complex pools representative of the most prevalent plant species in unmanaged and cultivated ecosystems. Viral richness was assessed by determining operational taxonomic units (OTU) following the clustering of conserved viral domains. There is some limited evidence of an impact of cultivation on viral populations. These results provide data allowing us to reason the methodological choices in virome studies. For researchers primarily interested in RNA viruses, the dsRNA approach is recommended because it consistently provided a more comprehensive description of the analyzed phytoviromes, but it understandably underrepresented DNA viruses and bacteriophages.

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Section: Discussionmentioning

confidence: 99%

Phytovirome Analysis of Wild Plant Populations: Comparison of Double-Stranded RNA and Virion-Associated Nucleic Acid Metagenomic Approaches

Marais

Lefebvre

et al. 2019

J Virol

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“…[2016]; accessed in January 2019). The PHASTER program was chosen due to its solid performance in benchmarking studies (de Sousa et al. 2018) and its useful scoring system that ranks predictions based on a prophage region completeness (Song et al.…”

Section: Methodsmentioning

confidence: 99%

Machine-Learning Classification Suggests That Many Alphaproteobacterial Prophages May Instead Be Gene Transfer Agents

Kogay

Neely

Birnbaum

et al. 2019

Genome Biology and Evolution

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Many of the sequenced bacterial and archaeal genomes encode regions of viral provenance. Yet, not all of these regions encode bona fide viruses. Gene transfer agents (GTAs) are thought to be former viruses that are now maintained in genomes of some bacteria and archaea and are hypothesized to enable exchange of DNA within bacterial populations. In Alphaproteobacteria, genes homologous to the “head–tail” gene cluster that encodes structural components of the Rhodobacter capsulatus GTA (RcGTA) are found in many taxa, even if they are only distantly related to Rhodobacter capsulatus. Yet, in most genomes available in GenBank RcGTA-like genes have annotations of typical viral proteins, and therefore are not easily distinguished from their viral homologs without additional analyses. Here, we report a “support vector machine” classifier that quickly and accurately distinguishes RcGTA-like genes from their viral homologs by capturing the differences in the amino acid composition of the encoded proteins. Our open-source classifier is implemented in Python and can be used to scan homologs of the RcGTA genes in newly sequenced genomes. The classifier can also be trained to identify other types of GTAs, or even to detect other elements of viral ancestry. Using the classifier trained on a manually curated set of homologous viruses and GTAs, we detected RcGTA-like “head–tail” gene clusters in 57.5% of the 1,423 examined alphaproteobacterial genomes. We also demonstrated that more than half of the in silico prophage predictions are instead likely to be GTAs, suggesting that in many alphaproteobacterial genomes the RcGTA-like elements remain unrecognized.

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“…NRC-l genome, and code for transposases associated with phage genomes and other mobile genetic elements (Bonneau et al, 2004). A recent web based tool called PhageWeb, for the identification and characterization of prophages within bacterial genomes, may expand the exploration of prophages in a variety of species (Sousa et al, 2018). The prevalence of prophages in bacterial genomes is intriguing, firstly, because of the imminent danger of lytic cycle induction and, secondly, the metabolic burden of replicating and expressing the prophage genetic elements.…”

Section: Prevalence Of Prophages In Bacterial Genomesmentioning

confidence: 99%

Bacterial ‘Grounded’ Prophages: Hotspots for Genetic Renovation and Innovation

2019

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Bacterial genomes are highly plastic allowing the generation of variants through mutations and acquisition of genetic information. The fittest variants are then selected by the econiche thereby allowing the bacterial adaptation and colonization of the habitat. Larger genomes, however, may impose metabolic burden and hence bacterial genomes are optimized by the loss of frivolous genetic information. The activity of temperate bacteriophages has acute consequences on the bacterial population as well as the bacterial genome through lytic and lysogenic cycles. Lysogeny is a selective advantage as the prophage provides immunity to the lysogen against secondary phage attack. Since the non-lysogens are eliminated by the lytic phages, lysogens multiply and colonize the habitat. Nevertheless, all lysogens have an imminent risk of lytic cycle activation and cell lysis. However, a mutation in the attachment sites or in the genes that encode the specific recombinase responsible for prophage excision could result in ‘grounding’ of the prophage. Since the lysogens with grounded prophage are immune to respective phage infection as well as dodge the induction of lytic cycle, we hypothesize that the selection of these mutant lysogens is favored relative to their normal lysogenic counterparts. These grounded prophages offer several advantages to the bacterial genome evolution through propensity for genetic variations including inversions, deletions, and insertions via horizontal gene transfer. We propose that the grounded prophages expedite bacterial genome evolution by acting as ‘genetic buffer zones’ thereby increasing the frequency as well as the diversity of variations on which natural selection favors the beneficial variants. The grounded prophages are also hotspots for horizontal gene transfer wherein several ecologically significant genes such as those involved in stress tolerance, antimicrobial resistance, and novel metabolic pathways, are integrated. Moreover, the high frequency of genetic changes within prophages also allows proportionate probability for the de novo genesis of genetic information. Through sequence analyses of well-characterized E. coli prophages we exemplify various roles of grounded prophages in E. coli ecology and evolution. Therefore, the temperate prophages are one of the most significant drivers of bacterial genome evolution and sites of biogenesis of genetic information.

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PhageWeb – Web Interface for Rapid Identification and Characterization of Prophages in Bacterial Genomes

Cited by 32 publications

References 33 publications

Phytovirome Analysis of Wild Plant Populations: Comparison of Double-Stranded RNA and Virion-Associated Nucleic Acid Metagenomic Approaches

Phytovirome Analysis of Wild Plant Populations: Comparison of Double-Stranded RNA and Virion-Associated Nucleic Acid Metagenomic Approaches

Machine-Learning Classification Suggests That Many Alphaproteobacterial Prophages May Instead Be Gene Transfer Agents

Bacterial ‘Grounded’ Prophages: Hotspots for Genetic Renovation and Innovation

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