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Viruses
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Diversity and Evolution of Phage Genomes
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Diversity and Evolution of Phage Genomes

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Bacterial Viruses".

Deadline for manuscript submissions: closed (30 April 2019) | Viewed by 102254

Special Issue Editors

Dr. Alejandro Reyes Muñoz

E-Mail Website
Guest Editor
Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia
Interests: computational biology; microbial ecology; viral ecology associated with different environments; viral genomic characterization
Dr. Martha J. Vives

E-Mail Website
Guest Editor
Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia
Interests: microbial bioprospection; phage therapy; environmental microbiology; technology transfer

Special Issue Information

Dear Colleagues,

The increasing problem of multidrug-resistant bacteria has renewed interest in phages as biological control agents. Despite its enormous potential, phage therapy is far from being widely accepted. Medical doctors’ and veterinarians’ principal concerns about the use of phages are due to its viral nature and potential for dissemination of toxins and virulence determinants. Furthermore, bacterial resistance mechanisms may render phage therapy useless soon if not properly applied.

In parallel, the last decade has seen the rise of the field of viral ecology, in which viruses and, in particular, phages are identified and recognized as important components of microbial ecosystems. While the microbiome is now dominating the headlines, it is clear that in every microbial environment, we will find at least an equivalent number of viral particles; however, our current understanding of viral diversity and its coding potential is still in its earliest development.

As can be seen, both research areas converge on the need to characterize phage genomes and their insights into phage diversity and evolution. We aim to generate a collection of articles with recent advances in phage diversity and evolution through genomic sequencing that are paving the way for both basic and applied research in phage biology.

Dr. Alejandro Reyes Muñoz
Dr. Martha J. Vives
Guest Editors

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Viruses is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • phage biology
  • genomics
  • biodiversity
  • evolution
  • phage therapy

Published Papers (18 papers)

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Editorial

Jump to: Research, Review

6 pages, 196 KiB  
Editorial
Paving the Way to Unveil the Diversity and Evolution of Phage Genomes
by Alejandro Reyes and Martha J. Vives
Viruses 2020, 12(9), 905; https://0-doi-org.brum.beds.ac.uk/10.3390/v12090905 - 19 Aug 2020
Cited by 1 | Viewed by 2490
Abstract
Phage biology has been developing for the last hundred years, and the potential of phages as tools and treatments has been known since their early discovery. However, the lack of knowledge of the molecular mechanisms coded in phage genomes hindered the development of [...] Read more.
Phage biology has been developing for the last hundred years, and the potential of phages as tools and treatments has been known since their early discovery. However, the lack of knowledge of the molecular mechanisms coded in phage genomes hindered the development of the field. With current molecular methods, the last decade has been a resurgence of the field. The Special Issue on “Diversity and Evolution of Phage Genomes” is a great example with its 17 manuscripts published. It covers some of the latest methods to sample and characterize environmental and host associated viromes, considering experimental biases and computational developments. Furthermore, the use of molecular tools coupled with traditional methods has allowed to isolate and characterize viruses from different hosts and environments with such diversity that even a new viral class is being proposed. The viruses described cover all different phage families and lifestyles. However, is not only about diversity; the molecular evolution is studied in a set of manuscripts looking at phage-host interactions and their capacity to uncover the frequency and type of mutations behind the bacterial resistance mechanisms and viral pathogenesis, and such methods are opening new ways into identifying potential receptors and characterizing the bacterial host range. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)

Research

Jump to: Editorial, Review

12 pages, 643 KiB  
Communication
Rates of Molecular Evolution in a Marine Synechococcus Phage Lineage
by Anne Kupczok and Tal Dagan
Viruses 2019, 11(8), 720; https://0-doi-org.brum.beds.ac.uk/10.3390/v11080720 - 06 Aug 2019
Cited by 10 | Viewed by 3426
Abstract
Cyanophages are characterized by vast genomic diversity and the formation of stable ecotypes over time. The evolution of phage diversity includes vertical processes, such as mutation, and horizontal processes, such as recombination and gene transfer. Here, we study the contribution of vertical and [...] Read more.
Cyanophages are characterized by vast genomic diversity and the formation of stable ecotypes over time. The evolution of phage diversity includes vertical processes, such as mutation, and horizontal processes, such as recombination and gene transfer. Here, we study the contribution of vertical and horizontal processes to short-term evolution of marine cyanophages. Analyzing time series data of Synechococcus-infecting Myoviridae ecotypes spanning up to 17 years, we found a high contribution of recombination relative to mutation (r/m) in all ecotypes. Additionally, we found a molecular clock of substitution and recombination in one ecotype, RIM8. The estimated RIM8 evolutionary rates are 2.2 genome-wide substitutions per year (1.275 × 10−5 substitutions/site/year) and 29 genome-wide nucleotide alterations due to recombination per year. We found 26 variable protein families, of which only two families have a predicted functional annotation, suggesting that they are auxiliary metabolic genes with bacterial homologs. A comparison of our rate estimates to other phage evolutionary rate estimates in the literature reveals a negative correlation of phage substitution rates with their genome size. A comparison to evolutionary rates in bacterial organisms further shows that phages have high rates of mutation and recombination compared to their bacterial hosts. We conclude that the increased recombination rate in phages likely contributes to their vast genomic diversity. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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10 pages, 1506 KiB  
Article
A Protocol for Extraction of Infective Viromes Suitable for Metagenomics Sequencing from Low Volume Fecal Samples
by Ling Deng, Ronalds Silins, Josué L. Castro-Mejía, Witold Kot, Leon Jessen, Jonathan Thorsen, Shiraz Shah, Jakob Stokholm, Hans Bisgaard, Sylvain Moineau and Dennis Sandris Nielsen
Viruses 2019, 11(7), 667; https://0-doi-org.brum.beds.ac.uk/10.3390/v11070667 - 20 Jul 2019
Cited by 26 | Viewed by 8064
Abstract
The human gut microbiome (GM) plays an important role in human health and diseases. However, while substantial progress has been made in understanding the role of bacterial inhabitants of the gut, much less is known regarding the viral component of the GM. Bacteriophages [...] Read more.
The human gut microbiome (GM) plays an important role in human health and diseases. However, while substantial progress has been made in understanding the role of bacterial inhabitants of the gut, much less is known regarding the viral component of the GM. Bacteriophages (phages) are viruses attacking specific host bacteria and likely play important roles in shaping the GM. Although metagenomic approaches have led to the discoveries of many new viruses, they remain largely uncultured as their hosts have not been identified, which hampers our understanding of their biological roles. Existing protocols for isolation of viromes generally require relatively high input volumes and are generally more focused on extracting nucleic acids of good quality and purity for down-stream analysis, and less on purifying viruses with infective capacity. In this study, we report the development of an efficient protocol requiring low sample input yielding purified viromes containing phages that are still infective, which also are of sufficient purity for genome sequencing. We validated the method through spiking known phages followed by plaque assays, qPCR, and metagenomic sequencing. The protocol should facilitate the process of culturing novel viruses from the gut as well as large scale studies on gut viromes. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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15 pages, 38225 KiB  
Article
Bacillus Phage vB_BtS_B83 Previously Designated as a Plasmid May Represent a New Siphoviridae Genus
by Emma G. Piligrimova, Olesya A. Kazantseva, Nikita A. Nikulin and Andrey M. Shadrin
Viruses 2019, 11(7), 624; https://0-doi-org.brum.beds.ac.uk/10.3390/v11070624 - 07 Jul 2019
Cited by 14 | Viewed by 6288
Abstract
The Bacillus cereus group of bacteria includes, inter alia, the species known to be associated with human diseases and food poisoning. Here, we describe the Bacillus phage vB_BtS_B83 (abbreviated as B83) infecting the species of this group. Transmission electron microscopy (TEM) micrographs indicate [...] Read more.
The Bacillus cereus group of bacteria includes, inter alia, the species known to be associated with human diseases and food poisoning. Here, we describe the Bacillus phage vB_BtS_B83 (abbreviated as B83) infecting the species of this group. Transmission electron microscopy (TEM) micrographs indicate that B83 belongs to the Siphoviridae family. B83 is a temperate phage using an arbitrium system for the regulation of the lysis–lysogeny switch, and is probably capable of forming a circular plasmid prophage. Comparative analysis shows that it has been previously sequenced, but was mistaken for a plasmid. B83 shares common genome organization and >46% of proteins with other the Bacillus phage, BMBtp14. Phylograms constructed using large terminase subunits and a pan-genome presence–absence matrix show that these phages form a clade distinct from the closest viruses. Based on the above, we propose the creation of a new genus named Bembunaquatrovirus that includes B83 and BMBtp14. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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19 pages, 4598 KiB  
Article
Nine Novel Phages from a Plateau Lake in Southwest China: Insights into Aeromonas Phage Diversity
by Meng Bai, Ya-Hui Cheng, Xue-Qin Sun, Zi-Yi Wang, Yong-Xia Wang, Xiao-Long Cui and Wei Xiao
Viruses 2019, 11(7), 615; https://0-doi-org.brum.beds.ac.uk/10.3390/v11070615 - 05 Jul 2019
Cited by 17 | Viewed by 3780
Abstract
Aeromonas species are common pathogens of fish and some of them can opportunistically cause infectious diseases in humans. The overuse of antibiotics has led to the emergence of bacterial drug-resistance. To date, only 51 complete genome sequences of Aeromonas phages are available in [...] Read more.
Aeromonas species are common pathogens of fish and some of them can opportunistically cause infectious diseases in humans. The overuse of antibiotics has led to the emergence of bacterial drug-resistance. To date, only 51 complete genome sequences of Aeromonas phages are available in GenBank. Here, we report the isolation of nine Aeromonas phages from a plateau lake in China. The protein cluster, dot plot and ANI analyses were performed on all 60 currently sequenced Aeromonas phage genomes and classified into nine clusters and thirteen singletons. Among the nine isolated phages, the DNA-packaging strategy of cluster 2L372D (including 2L372D, 2L372X, 4L372D, 4L372XY) is unknown, while the other five phages use the headful (P22/Sf6) DNA-packaging strategy. Notably, the isolated phages with larger genomes conservatively encode auxiliary metabolism genes, DNA replication and metabolism genes, while in smaller phage genomes, recombination-related genes were conserved. Finally, we propose a new classification scheme for Aeromonas phages. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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21 pages, 3231 KiB  
Article
Two Phages of the Genera Felixunavirus Subjected to 12 Hour Challenge on Salmonella Infantis Showed Distinct Genotypic and Phenotypic Changes
by Dácil Rivera, Lauren K. Hudson, Thomas G. Denes, Christopher Hamilton-West, David Pezoa and Andrea I. Moreno-Switt
Viruses 2019, 11(7), 586; https://0-doi-org.brum.beds.ac.uk/10.3390/v11070586 - 27 Jun 2019
Cited by 11 | Viewed by 5001
Abstract
Salmonella Infantis is considered in recent years an emerging Salmonella serovar, as it has been associated with several outbreaks and multidrug resistance phenotypes. Phages appear as a possible alternative strategy to control Salmonella Infantis (SI). The aims of this work were [...] Read more.
Salmonella Infantis is considered in recent years an emerging Salmonella serovar, as it has been associated with several outbreaks and multidrug resistance phenotypes. Phages appear as a possible alternative strategy to control Salmonella Infantis (SI). The aims of this work were to characterize two phages of the Felixounavirus genus, isolated using the same strain of SI, and to expose them to interact in challenge assays to identify genetic and phenotypic changes generated from these interactions. These two phages have a shared nucleotide identity of 97% and are differentiated by their host range: one phage has a wide host range (lysing 14 serovars), and the other has a narrow host range (lysing 6 serovars). During the 12 h challenge we compared: (1) optical density of SI, (2) proportion of SI survivors from phage-infected cultures, and (3) phage titer. Isolates obtained through the assays were evaluated by efficiency of plating (EOP) and by host-range characterization. Genomic modifications were characterized by evaluation of single nucleotide polymorphisms (SNPs). The optical density (600 nm) of phage-infected SI decreased, as compared to the uninfected control, by an average of 0.7 for SI infected with the wide-host-range (WHR) phage and by 0.3 for SI infected with the narrow-host-range (NHR) phage. WHR phage reached higher phage titer (7 × 1011 PFU/mL), and a lower proportion of SI survivor was obtained from the challenge assay. In SI that interacted with phages, we identified SNPs in two genes (rfaK and rfaB), which are both involved in lipopolysaccharide (LPS) polymerization. Therefore, mutations that could impact potential phage receptors on the host surface were selected by lytic phage exposure. This work demonstrates that the interaction of Salmonella phages (WHR and NHR) with SI for 12 h in vitro leads to emergence of new phenotypic and genotypic traits in both phage and host. This information is crucial for the rational design of phage-based control strategies. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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Graphical abstract

14 pages, 3188 KiB  
Article
Isolation and Characterization T4- and T7-Like Phages that Infect the Bacterial Plant Pathogen Agrobacterium tumefaciens
by Hedieh Attai and Pamela J.B. Brown
Viruses 2019, 11(6), 528; https://0-doi-org.brum.beds.ac.uk/10.3390/v11060528 - 07 Jun 2019
Cited by 11 | Viewed by 5492
Abstract
In the rhizosphere, bacteria–phage interactions are likely to have important impacts on the ecology of microbial communities and microbe–plant interactions. To better understand the dynamics of Agrobacteria–phage interactions, we have isolated diverse bacteriophages which infect the bacterial plant pathogen, Agrobacterium tumefaciens. Here, [...] Read more.
In the rhizosphere, bacteria–phage interactions are likely to have important impacts on the ecology of microbial communities and microbe–plant interactions. To better understand the dynamics of Agrobacteria–phage interactions, we have isolated diverse bacteriophages which infect the bacterial plant pathogen, Agrobacterium tumefaciens. Here, we complete the genomic characterization of Agrobacterium tumefaciens phages Atu_ph04 and Atu_ph08. Atu_ph04—a T4-like phage belonging to the Myoviridae family—was isolated from waste water and has a 143,349 bp genome that encodes 223 predicted open reading frames (ORFs). Based on phylogenetic analysis and whole-genome alignments, Atu_ph04 is a member of a newly described T4 superfamily that contains other Rhizobiales-infecting phages. Atu_ph08, a member of the Podoviridae T7-like family, was isolated from waste water, has a 59,034 bp genome, and encodes 75 ORFs. Based on phylogenetic analysis and whole-genome alignments, Atu_ph08 may form a new T7 superfamily which includes Sinorhizobium phage PCB5 and Ochrobactrum phage POI1126. Atu_ph08 is predicted to have lysogenic activity, as we found evidence of an integrase and several transcriptional repressors with similarity to proteins in transducing phage P22. Together, this data suggests that Agrobacterium phages are diverse in morphology, genomic content, and lifestyle. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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18 pages, 2253 KiB  
Article
Characterization of Flagellotropic, Chi-Like Salmonella Phages Isolated from Thai Poultry Farms
by Preeda Phothaworn, Matthew Dunne, Rattaya Supokaivanich, Catherine Ong, Jiali Lim, Rutjawate Taharnklaew, Mongkol Vesaratchavest, Rabuesak Khumthong, Onanong Pringsulaka, Pravech Ajawatanawong, Jochen Klumpp, Nathan Brown, Mohammed Imam, Martha R. J. Clokie, Edouard E. Galyov and Sunee Korbsrisate
Viruses 2019, 11(6), 520; https://0-doi-org.brum.beds.ac.uk/10.3390/v11060520 - 05 Jun 2019
Cited by 26 | Viewed by 5982
Abstract
Despite a wealth of knowledge on Salmonella phages worldwide, little is known about poultry-associated Salmonella phages from Thailand. Here, we isolated 108 phages from Thai poultry farms that infect Salmonella enterica serovar Typhimurium. Phages STm101 and STm118 were identified as temperate Siphoviridae phages. [...] Read more.
Despite a wealth of knowledge on Salmonella phages worldwide, little is known about poultry-associated Salmonella phages from Thailand. Here, we isolated 108 phages from Thai poultry farms that infect Salmonella enterica serovar Typhimurium. Phages STm101 and STm118 were identified as temperate Siphoviridae phages. Genome sequencing and analyses revealed these phages share approximately 96% nucleotide sequence similarity to phage SPN19, a member of the Chi-like virus genus. PCR amplification of the gene encoding capsid protein E of the Chi-like phage was positive for 50% of phage isolates, suggesting a predominance of this phage type among the sampled poultry farms. In addition to the flagella, two phages required the lipopolysaccharide to infect and lyse Salmonella. Furthermore, phylogenomic analysis demonstrated that phages STm101 and STm118 formed a monophyletic clade with phages isolated from Western countries, but not from closer isolated phages from Korea. However, further investigation and more phage isolates are required to investigate possible causes for this geographic distribution. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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29 pages, 25661 KiB  
Article
Still Something to Discover: Novel Insights into Escherichia coli Phage Diversity and Taxonomy
by Imke H. E. Korf, Jan P. Meier-Kolthoff, Evelien M. Adriaenssens, Andrew M. Kropinski, Manfred Nimtz, Manfred Rohde, Mark J. van Raaij and Johannes Wittmann
Viruses 2019, 11(5), 454; https://0-doi-org.brum.beds.ac.uk/10.3390/v11050454 - 17 May 2019
Cited by 56 | Viewed by 9185
Abstract
The aim of this study was to gain further insight into the diversity of Escherichia coli phages followed by enhanced work on taxonomic issues in that field. Therefore, we present the genomic characterization and taxonomic classification of 50 bacteriophages against E. coli isolated [...] Read more.
The aim of this study was to gain further insight into the diversity of Escherichia coli phages followed by enhanced work on taxonomic issues in that field. Therefore, we present the genomic characterization and taxonomic classification of 50 bacteriophages against E. coli isolated from various sources, such as manure or sewage. All phages were examined for their host range on a set of different E. coli strains, originating, e.g., from human diagnostic laboratories or poultry farms. Transmission electron microscopy revealed a diversity of morphotypes (70% Myo-, 22% Sipho-, and 8% Podoviruses), and genome sequencing resulted in genomes sizes from ~44 to ~370 kb. Annotation and comparison with databases showed similarities in particular to T4- and T5-like phages, but also to less-known groups. Though various phages against E. coli are already described in literature and databases, we still isolated phages that showed no or only few similarities to other phages, namely phages Goslar, PTXU04, and KWBSE43-6. Genome-based phylogeny and classification of the newly isolated phages using VICTOR resulted in the proposal of new genera and led to an enhanced taxonomic classification of E. coli phages. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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15 pages, 2421 KiB  
Article
Mouse Vendor Influence on the Bacterial and Viral Gut Composition Exceeds the Effect of Diet
by Torben Sølbeck Rasmussen, Liv de Vries, Witold Kot, Lars Hestbjerg Hansen, Josué L. Castro-Mejía, Finn Kvist Vogensen, Axel Kornerup Hansen and Dennis Sandris Nielsen
Viruses 2019, 11(5), 435; https://0-doi-org.brum.beds.ac.uk/10.3390/v11050435 - 13 May 2019
Cited by 45 | Viewed by 6029
Abstract
Often physiological studies using mice from one vendor show different outcome when being reproduced using mice from another vendor. These divergent phenotypes between similar mouse strains from different vendors have been assigned to differences in the gut microbiome. During recent years, evidence has [...] Read more.
Often physiological studies using mice from one vendor show different outcome when being reproduced using mice from another vendor. These divergent phenotypes between similar mouse strains from different vendors have been assigned to differences in the gut microbiome. During recent years, evidence has mounted that the gut viral community plays a key role in shaping the gut microbiome and may thus also influence mouse phenotype. However, to date inter-vendor variation in the murine gut virome has not been studied. Using a metavirome approach, combined with 16S rRNA gene sequencing, we here compare the composition of the viral and bacterial gut community of C57BL/6N mice from three different vendors exposed to either a chow-based low-fat diet or high-fat diet. Interestingly, both the bacterial and the viral component of the gut community differed significantly between vendors. The different diets also strongly influenced both the viral and bacterial gut community, but surprisingly the effect of vendor exceeded the effect of diet. In conclusion, the vendor effect is substantial not only on the gut bacterial community but also strongly influences viral community composition. Given the effect of GM on mice phenotype, this is essential to consider for increasing reproducibility of mouse studies. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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15 pages, 3742 KiB  
Article
Prevalence and Diversity Analysis of Candidate Prophages to Provide An Understanding on Their Roles in Bacillus Thuringiensis
by Yajuan Fu, Yan Wu, Yihui Yuan and Meiying Gao
Viruses 2019, 11(4), 388; https://0-doi-org.brum.beds.ac.uk/10.3390/v11040388 - 25 Apr 2019
Cited by 15 | Viewed by 3821
Abstract
Bacillus thuringiensis (Bt) is widely used in producing biological insecticides. Phage contaminations during Bt fermentation can cause severe losses of yields. Lots of strategies have been engaged to control extrinsic phage contamination during Bt fermentation, but their effectiveness is low. In this study, [...] Read more.
Bacillus thuringiensis (Bt) is widely used in producing biological insecticides. Phage contaminations during Bt fermentation can cause severe losses of yields. Lots of strategies have been engaged to control extrinsic phage contamination during Bt fermentation, but their effectiveness is low. In this study, the candidate endogenous prophages (prophages) in 61 Bt chromosomes that had been deposited in GenBank database were analyzed. The results revealed that all chromosomes contained prophage regions, and 398 candidate prophage regions were predicted, including 135 putative complete prophages and 263 incomplete prophage regions. These putative complete prophages showed highly diverse genetic backgrounds. The inducibility of the prophages of ten Bt strains (4AJ1, 4BD1, HD-1, HD-29, HD-73, HD-521, BMB171, 4CC1, CT-43, and HD-1011) was tested, and the results showed that seven of the ten strains’ prophages were inducible. These induced phages belonged to the Siphoviridae family and exhibited a broad host spectrum against the non-original strains. The culture supernatants of the two strains (BMB171, 4CC1) could lyse Bt cells, but no virions were observed, which was speculated to be caused by lysin. The functional analysis of the putative complete prophage proteins indicated that some proteins, such as antibiotic resistance-associated proteins and restriction endonucleases, might increase the fitness of the Bt strains to different environments. The findings of this study provided understanding on the high prevalence and diversity of Bt prophages, as well as pointed out the role of prophages in the life cycle of Bt. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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15 pages, 1893 KiB  
Article
Classifying the Unclassified: A Phage Classification Method
by Cynthia Maria Chibani, Anton Farr, Sandra Klama, Sascha Dietrich and Heiko Liesegang
Viruses 2019, 11(2), 195; https://0-doi-org.brum.beds.ac.uk/10.3390/v11020195 - 24 Feb 2019
Cited by 40 | Viewed by 8995
Abstract
This work reports the method ClassiPhage to classify phage genomes using sequence derived taxonomic features. ClassiPhage uses a set of phage specific Hidden Markov Models (HMMs) generated from clusters of related proteins. The method was validated on all publicly available genomes of phages [...] Read more.
This work reports the method ClassiPhage to classify phage genomes using sequence derived taxonomic features. ClassiPhage uses a set of phage specific Hidden Markov Models (HMMs) generated from clusters of related proteins. The method was validated on all publicly available genomes of phages that are known to infect Vibrionaceae. The phages belong to the well-described phage families of Myoviridae, Podoviridae, Siphoviridae, and Inoviridae. The achieved classification is consistent with the assignments of the International Committee on Taxonomy of Viruses (ICTV), all tested phages were assigned to the corresponding group of the ICTV-database. In addition, 44 out of 58 genomes of Vibrio phages not yet classified could be assigned to a phage family. The remaining 14 genomes may represent phages of new families or subfamilies. Comparative genomics indicates that the ability of the approach to identify and classify phages is correlated to the conserved genomic organization. ClassiPhage classifies phages exclusively based on genome sequence data and can be applied on distinct phage genomes as well as on prophage regions within host genomes. Possible applications include (a) classifying phages from assembled metagenomes; and (b) the identification and classification of integrated prophages and the splitting of phage families into subfamilies. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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22 pages, 3378 KiB  
Article
Host Resistance, Genomics and Population Dynamics in a Salmonella Enteritidis and Phage System
by Angela Victoria Holguín, Pablo Cárdenas, Catalina Prada-Peñaranda, Laura Rabelo Leite, Camila Buitrago, Viviana Clavijo, Guilherme Oliveira, Pimlapas Leekitcharoenphon, Frank Møller Aarestrup and Martha J. Vives
Viruses 2019, 11(2), 188; https://0-doi-org.brum.beds.ac.uk/10.3390/v11020188 - 22 Feb 2019
Cited by 16 | Viewed by 6158
Abstract
Bacteriophages represent an alternative solution to control bacterial infections. When interacting, bacteria and phage can evolve, and this relationship is described as antagonistic coevolution, a pattern that does not fit all models. In this work, the model consisted of a microcosm of Salmonella [...] Read more.
Bacteriophages represent an alternative solution to control bacterial infections. When interacting, bacteria and phage can evolve, and this relationship is described as antagonistic coevolution, a pattern that does not fit all models. In this work, the model consisted of a microcosm of Salmonella enterica serovar Enteritidis and φSan23 phage. Samples were taken for 12 days every 48 h. Bacteria and phage samples were collected; and isolated bacteria from each time point were challenged against phages from previous, contemporary, and subsequent time points. The phage plaque tests, with the genomics analyses, showed a mutational asymmetry dynamic in favor of the bacteria instead of antagonistic coevolution. This is important for future phage-therapy applications, so we decided to explore the population dynamics of Salmonella under different conditions: pressure of one phage, a combination of phages, and phages plus an antibiotic. The data from cultures with single and multiple phages, and antibiotics, were used to create a mathematical model exploring population and resistance dynamics of Salmonella under these treatments, suggesting a nonlethal, growth-inhibiting antibiotic may decrease resistance to phage-therapy cocktails. These data provide a deep insight into bacterial dynamics under different conditions and serve as additional criteria to select phages and antibiotics for phage-therapy. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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14 pages, 4283 KiB  
Article
Phage Reduce Stability for Regaining Infectivity during Antagonistic Coevolution with Host Bacterium
by Yihui Yuan, Qin Peng, Shaowen Zhang, Tingting Liu, Shuo Yang, Qiuhan Yu, Yan Wu and Meiying Gao
Viruses 2019, 11(2), 118; https://0-doi-org.brum.beds.ac.uk/10.3390/v11020118 - 29 Jan 2019
Cited by 11 | Viewed by 4036
Abstract
The coevolution between phage and host bacterium is an important force that drives the evolution of the microbial community, yet the coevolution mechanisms have still not been well analyzed. Here, by analyzing the interaction between a Bacillus phage vB_BthS_BMBphi and its host bacterium, [...] Read more.
The coevolution between phage and host bacterium is an important force that drives the evolution of the microbial community, yet the coevolution mechanisms have still not been well analyzed. Here, by analyzing the interaction between a Bacillus phage vB_BthS_BMBphi and its host bacterium, the coevolution mechanisms of the first-generation phage-resistant bacterial mutants and regained-infectivity phage mutants were studied. The phage-resistant bacterial mutants showed several conserved mutations as a potential reason for acquiring phage resistance, including the mutation in flagellum synthesis protein FlhA and cell wall polysaccharide synthesis protein DltC. All the phage-resistant bacterial mutants showed a deleted first transmembrane domain of the flagellum synthesis protein FlhA. Meanwhile, the regain-infectivity phage mutants all contained mutations in three baseplate-associated phage tail proteins by one nucleotide, respectively. A polymorphism analysis of the three mutant nucleotides in the wild-type phage revealed that the mutations existed before the interaction of the phage and the bacterium, while the wild-type phage could not infect the phage-resistant bacterial mutants, which might be because the synchronized mutations of the three nucleotides were essential for regaining infectivity. This study for the first time revealed that the synergism mutation of three phage baseplate-associated proteins were essential for the phages’ regained infectivity. Although the phage mutants regained infectivity, their storage stability was decreased and the infectivity against the phage-resistant bacterial mutants was reduced, suggesting the phage realized the continuation of the species by way of “dying to survive”. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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13 pages, 3201 KiB  
Article
The Characteristics and Genome Analysis of vB_AviM_AVP, the First Phage Infecting Aerococcus viridans
by Hengyu Xi, Jiaxin Dai, Yigang Tong, Mengjun Cheng, Feiyang Zhao, Hang Fan, Xinwei Li, Ruopeng Cai, Yalu Ji, Changjiang Sun, Xin Feng, Liancheng Lei, Sadeeq ur Rahman, Wenyu Han and Jingmin Gu
Viruses 2019, 11(2), 104; https://0-doi-org.brum.beds.ac.uk/10.3390/v11020104 - 26 Jan 2019
Cited by 24 | Viewed by 4251
Abstract
Aerococcus viridans is an opportunistic pathogen that is clinically associated with various human and animal diseases. In this study, the first identified A. viridans phage, vB_AviM_AVP (abbreviated as AVP), was isolated and studied. AVP belongs to the family Myoviridae. AVP harbors a double-stranded [...] Read more.
Aerococcus viridans is an opportunistic pathogen that is clinically associated with various human and animal diseases. In this study, the first identified A. viridans phage, vB_AviM_AVP (abbreviated as AVP), was isolated and studied. AVP belongs to the family Myoviridae. AVP harbors a double-stranded DNA genome with a length of 133,806 bp and a G + C content of 34.51%. The genome sequence of AVP showed low similarity (<1% identity) to those of other phages, bacteria, or other organisms in the database. Among 165 predicted open reading frames (ORFs), there were only 69 gene products exhibiting similarity (≤65% identity) to proteins of known functions in the database. In addition, the other 36 gene products did not match any viral or prokaryotic sequences in any publicly available database. On the basis of the putative functions of the ORFs, the genome of AVP was divided into three modules: nucleotide metabolism and replication, structural components, and lysis. A phylogenetic analysis of the terminase large subunits and capsid proteins indicated that AVP represents a novel branch of phages. The observed characteristics of AVP indicate that it represents a new class of phages. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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19 pages, 2999 KiB  
Article
Metagenomic Characterization of the Viral Community of the South Scotia Ridge
by Qingwei Yang, Chen Gao, Yong Jiang, Min Wang, Xinhao Zhou, Hongbing Shao, Zheng Gong and Andrew McMinn
Viruses 2019, 11(2), 95; https://0-doi-org.brum.beds.ac.uk/10.3390/v11020095 - 24 Jan 2019
Cited by 21 | Viewed by 5627
Abstract
Viruses are the most abundant biological entities in aquatic ecosystems and harbor an enormous amount of genetic diversity. Whereas their influence on marine ecosystems is widely acknowledged, current information about their diversity remains limited. We conducted a viral metagenomic analysis of water samples [...] Read more.
Viruses are the most abundant biological entities in aquatic ecosystems and harbor an enormous amount of genetic diversity. Whereas their influence on marine ecosystems is widely acknowledged, current information about their diversity remains limited. We conducted a viral metagenomic analysis of water samples collected during the austral summer of 2016 from the South Scotia Ridge (SSR), near the Antarctic Peninsula. The taxonomic composition and diversity of the viral communities were investigated, and a functional assessment of the sequences was performed. Phylotypic analysis showed that most viruses belonged to the order Caudovirales, especially the family Podoviridae (41.92–48.7%), which is similar to the situation in the Pacific Ocean. Functional analysis revealed a relatively high frequency of phage-associated and metabolism genes. Phylogenetic analyses of phage TerL and Capsid_NCLDV (nucleocytoplasmic large DNA viruses) marker genes indicated that many sequences associated with Caudovirales and NCLDV were novel and distinct from known phage genomes. High Phaeocystis globosa virus virophage (Pgvv) signatures were found and complete and partial Pgvv-like were obtained, which influence host–virus interactions. Our study expands existing knowledge of viral communities and their diversities from the Antarctic region and provides basic data for further exploring polar microbiomes. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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13 pages, 4255 KiB  
Article
Isolation of A Novel Bacillus thuringiensis Phage Representing A New Phage Lineage and Characterization of Its Endolysin
by Yihui Yuan, Qin Peng, Shuo Yang, Shaowen Zhang, Yajuan Fu, Yan Wu and Meiying Gao
Viruses 2018, 10(11), 611; https://0-doi-org.brum.beds.ac.uk/10.3390/v10110611 - 06 Nov 2018
Cited by 13 | Viewed by 3994
Abstract
Phages, the parasites of bacteria, are considered as a new kind of antimicrobial agent due to their ability to lyse pathogenic bacteria. Due to the increase of available phage isolates, the newly isolated phage showed increasing genomic similarities with previously isolated phages. In [...] Read more.
Phages, the parasites of bacteria, are considered as a new kind of antimicrobial agent due to their ability to lyse pathogenic bacteria. Due to the increase of available phage isolates, the newly isolated phage showed increasing genomic similarities with previously isolated phages. In this study, the novel phage vB_BthS_BMBphi, infecting the Bacillus thuringiensis strain BMB171, is isolated and characterized together with its endolysin. This phage is the first tadpole-like phage infecting the Bacillus strains. Genomic analysis shows that the phage genome is dissimilar to all those of previously characterized phages, only exhibiting low similarities with partial regions of the B. thuringiensis prophages. Phylogenetic analysis revealed that the phage was distant from the other Bacillus phages in terms of evolution. The novel genome sequence, the distant evolutionary relationship, and the special virion morphology together suggest that the phage vB_BthS_BMBphi could be classified as a new phage lineage. The genome of the phage is found to contain a restriction modification system, which might endow the phage with immunity to the restriction modification system of the host bacterium. The function of the endolysin PlyBMB encoded by the phage vB_BthS_BMBphi was analyzed, and the endolysin could lyse all the tested Bacillus cereus group strains, suggesting that the endolysin might be used in controlling pathogenic B. cereus group strains. The findings of this study enrich the understanding of phage diversity and provide a resource for controlling the B. cereus group pathogenic bacteria. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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Review

Jump to: Editorial, Research

16 pages, 6874 KiB  
Review
Phages and Human Health: More Than Idle Hitchhikers
by Dylan Lawrence, Megan T. Baldridge and Scott A. Handley
Viruses 2019, 11(7), 587; https://0-doi-org.brum.beds.ac.uk/10.3390/v11070587 - 27 Jun 2019
Cited by 43 | Viewed by 8373
Abstract
Bacteriophages, or phages, are viruses that infect bacteria and archaea. Phages have diverse morphologies and can be coded in DNA or RNA and as single or double strands with a large range of genome sizes. With the increasing use of metagenomic sequencing approaches [...] Read more.
Bacteriophages, or phages, are viruses that infect bacteria and archaea. Phages have diverse morphologies and can be coded in DNA or RNA and as single or double strands with a large range of genome sizes. With the increasing use of metagenomic sequencing approaches to analyze complex samples, many studies generate massive amounts of “viral dark matter”, or sequences of viral origin unable to be classified either functionally or taxonomically. Metagenomic analysis of phages is still in its infancy, and uncovering novel phages continues to be a challenge. Work over the past two decades has begun to uncover key roles for phages in different environments, including the human gut. Recent studies in humans have identified expanded phage populations in both healthy infants and in inflammatory bowel disease patients, suggesting distinct phage activity during development and in specific disease states. In this review, we examine our current knowledge of phage biology and discuss recent efforts to improve the analysis and discovery of novel phages. We explore the roles phages may play in human health and disease and discuss the future of phage research. Full article
(This article belongs to the Special Issue Diversity and Evolution of Phage Genomes)
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