Tectiviridae

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Natalya Yutin - One of the best experts on this subject based on the ideXlab platform.

  • Adomaviruses: an emerging virus family provides insights into DNA virus evolution
    bioRxiv, 2018
    Co-Authors: Nicole L Welch, Natalya Yutin, Jennifer A. Dill, Alvin C. Camus, Yuk-ying S. Pang, John T. Schiller, Ping An, Paul G. Cantalupo, James M. Pipas, Eric Delwart
    Abstract:

    Diverse eukaryotic dsDNA viruses, including adenoviruses, are thought to have evolved from bacteriophages of the family Tectiviridae. The evolutionary relationship of the small circular dsDNA tumor viruses of the families Papillomaviridae and Polyomaviridae to other DNA virus families remains uncertain. Metagenomic surveys of fish reveal 5 previously unknown circular dsDNA viruses that could become founding members of a distinct viral family. These viruses encode predicted superfamily 3 helicases that are related to the replicative helicases of polyomaviruses and papillomaviruses. Additionally, the new viruses encode a gene cluster coding for homologs of adenovirus-like maturation proteases and putative homologs of adenovirus major and minor capsid proteins. We show that these predicted capsid protein are indeed incorporated into the adomavirus virions. Such combination of genes from unrelated virus families is unprecedented among known DNA viruses. We propose the name "Adomaviridae" for this emerging virus family.

  • Vast diversity of prokaryotic virus genomes encoding double jelly-roll major capsid proteins uncovered by genomic and metagenomic sequence analysis
    Virology Journal, 2018
    Co-Authors: Natalya Yutin, Mart Krupovic, Disa Bäckström, Thijs J. G. Ettema, Eugene V. Koonin
    Abstract:

    Background Analysis of metagenomic sequences has become the principal approach for the study of the diversity of viruses. Many recent, extensive metagenomic studies on several classes of viruses have dramatically expanded the visible part of the virosphere, showing that previously undetected viruses, or those that have been considered rare, actually are important components of the global virome. Results We investigated the provenance of viruses related to tail-less bacteriophages of the family Tectiviridae by searching genomic and metagenomics sequence databases for distant homologs of the tectivirus-like Double Jelly-Roll major capsid proteins (DJR MCP). These searches resulted in the identification of numerous genomes of virus-like elements that are similar in size to tectiviruses (10–15 kilobases) and have diverse gene compositions. By comparison of the gene repertoires, the DJR MCP-encoding genomes were classified into 6 distinct groups that can be predicted to differ in reproduction strategies and host ranges. Only the DJR MCP gene that is present by design is shared by all these genomes, and most also encode a predicted DNA-packaging ATPase; the rest of the genes are present only in subgroups of this unexpectedly diverse collection of DJR MCP-encoding genomes. Only a minority encode a DNA polymerase which is a hallmark of the family Tectiviridae  and the putative family "Autolykiviridae". Notably, one of the identified putative DJR MCP viruses encodes a homolog of Cas1 endonuclease, the integrase involved in CRISPR-Cas adaptation and integration of transposon-like elements called casposons. This is the first detected occurrence of Cas1 in a virus. Many of the identified elements are individual contigs flanked by inverted or direct repeats and appear to represent complete, extrachromosomal viral genomes, whereas others are flanked by bacterial genes and thus can be considered as proviruses. These contigs come from metagenomes of widely different environments, some dominated by archaea and others by bacteria, suggesting that collectively, the DJR MCP-encoding elements have a broad host range among prokaryotes. Conclusions The findings reported here greatly expand the known host range of (putative) viruses of bacteria and archaea that encode a DJR MCP. They also demonstrate the extreme diversity of genome architectures in these viruses that encode no universal proteins other than the capsid protein that was used as the marker for their identification. From a supposedly minor group of bacterial and archaeal viruses, these viruses are emerging as a substantial component of the prokaryotic virome.

  • ANNALS OF THE NEW YORK ACADEMY OF SCIENCES Issue:DNA Habitats and Their RNA Inhabitants Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses
    2016
    Co-Authors: Eugene V. Koonin, Mart Krupovic, Natalya Yutin
    Abstract:

    Diverse eukaryotes including animals and protists are hosts to a broad variety of viruses with double-stranded (ds) DNA genomes, from the largest known viruses, such as pandoraviruses and mimiviruses, to tiny polyomaviruses. Recent comparative genomic analyses have revealed many evolutionary connections between dsDNA viruses of eukaryotes, bacteriophages, transposable elements, and linear DNA plasmids. These findings provide an evolu-tionary scenario that derives several major groups of eukaryotic dsDNA viruses, including the proposed order “Megavirales, ” adenoviruses, and virophages from a group of large virus-like transposons known as Polintons (Mav-ericks). The Polintons have been recently shown to encode two capsid proteins, suggesting that these elements lead a dual lifestyle with both a transposon and a viral phase and should perhaps more appropriately be named polin-toviruses. Here, we describe the recently identified evolutionary relationships between bacteriophages of the family Tectiviridae, polintoviruses, adenoviruses, virophages, large and giant DNA viruses of eukaryotes of the proposed order “Megavirales, ” and linearmitochondrial and cytoplasmic plasmids.We outline an evolutionary scenario under which the polintoviruses were the first group of eukaryotic dsDNA viruses that evolved from bacteriophages and became the ancestors of most large DNA viruses of eukaryotes and a variety of other selfish elements. Distinct lines of origin are detectable only for herpesviruses (from a different bacteriophage root) and polyoma/papillomaviruses (from single-stranded DNA viruses and ultimately from plasmids). Phylogenomic analysis of giant viruses provide

  • evolution of double stranded dna viruses of eukaryotes from bacteriophages to transposons to giant viruses
    Annals of the New York Academy of Sciences, 2015
    Co-Authors: Eugene V. Koonin, Mart Krupovic, Natalya Yutin
    Abstract:

    Diverse eukaryotes including animals and protists are hosts to a broad variety of viruses with double-stranded (ds) DNA genomes, from the largest known viruses, such as pandoraviruses and mimiviruses, to tiny polyomaviruses. Recent comparative genomic analyses have revealed many evolutionary connections between dsDNA viruses of eukaryotes, bacteriophages, transposable elements, and linear DNA plasmids. These findings provide an evolutionary scenario that derives several major groups of eukaryotic dsDNA viruses, including the proposed order “Megavirales,” adenoviruses, and virophages from a group of large virus-like transposons known as Polintons (Mavericks). The Polintons have been recently shown to encode two capsid proteins, suggesting that these elements lead a dual lifestyle with both a transposon and a viral phase and should perhaps more appropriately be named polintoviruses. Here, we describe the recently identified evolutionary relationships between bacteriophages of the family Tectiviridae, polintoviruses, adenoviruses, virophages, large and giant DNA viruses of eukaryotes of the proposed order “Megavirales,” and linear mitochondrial and cytoplasmic plasmids. We outline an evolutionary scenario under which the polintoviruses were the first group of eukaryotic dsDNA viruses that evolved from bacteriophages and became the ancestors of most large DNA viruses of eukaryotes and a variety of other selfish elements. Distinct lines of origin are detectable only for herpesviruses (from a different bacteriophage root) and polyoma/papillomaviruses (from single-stranded DNA viruses and ultimately from plasmids). Phylogenomic analysis of giant viruses provides compelling evidence of their independent origins from smaller members of the putative order “Megavirales,” refuting the speculations on the evolution of these viruses from an extinct fourth domain of cellular life.

Eugene V. Koonin - One of the best experts on this subject based on the ideXlab platform.

  • Vast diversity of prokaryotic virus genomes encoding double jelly-roll major capsid proteins uncovered by genomic and metagenomic sequence analysis
    Virology Journal, 2018
    Co-Authors: Natalya Yutin, Mart Krupovic, Disa Bäckström, Thijs J. G. Ettema, Eugene V. Koonin
    Abstract:

    Background Analysis of metagenomic sequences has become the principal approach for the study of the diversity of viruses. Many recent, extensive metagenomic studies on several classes of viruses have dramatically expanded the visible part of the virosphere, showing that previously undetected viruses, or those that have been considered rare, actually are important components of the global virome. Results We investigated the provenance of viruses related to tail-less bacteriophages of the family Tectiviridae by searching genomic and metagenomics sequence databases for distant homologs of the tectivirus-like Double Jelly-Roll major capsid proteins (DJR MCP). These searches resulted in the identification of numerous genomes of virus-like elements that are similar in size to tectiviruses (10–15 kilobases) and have diverse gene compositions. By comparison of the gene repertoires, the DJR MCP-encoding genomes were classified into 6 distinct groups that can be predicted to differ in reproduction strategies and host ranges. Only the DJR MCP gene that is present by design is shared by all these genomes, and most also encode a predicted DNA-packaging ATPase; the rest of the genes are present only in subgroups of this unexpectedly diverse collection of DJR MCP-encoding genomes. Only a minority encode a DNA polymerase which is a hallmark of the family Tectiviridae  and the putative family "Autolykiviridae". Notably, one of the identified putative DJR MCP viruses encodes a homolog of Cas1 endonuclease, the integrase involved in CRISPR-Cas adaptation and integration of transposon-like elements called casposons. This is the first detected occurrence of Cas1 in a virus. Many of the identified elements are individual contigs flanked by inverted or direct repeats and appear to represent complete, extrachromosomal viral genomes, whereas others are flanked by bacterial genes and thus can be considered as proviruses. These contigs come from metagenomes of widely different environments, some dominated by archaea and others by bacteria, suggesting that collectively, the DJR MCP-encoding elements have a broad host range among prokaryotes. Conclusions The findings reported here greatly expand the known host range of (putative) viruses of bacteria and archaea that encode a DJR MCP. They also demonstrate the extreme diversity of genome architectures in these viruses that encode no universal proteins other than the capsid protein that was used as the marker for their identification. From a supposedly minor group of bacterial and archaeal viruses, these viruses are emerging as a substantial component of the prokaryotic virome.

  • ANNALS OF THE NEW YORK ACADEMY OF SCIENCES Issue:DNA Habitats and Their RNA Inhabitants Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses
    2016
    Co-Authors: Eugene V. Koonin, Mart Krupovic, Natalya Yutin
    Abstract:

    Diverse eukaryotes including animals and protists are hosts to a broad variety of viruses with double-stranded (ds) DNA genomes, from the largest known viruses, such as pandoraviruses and mimiviruses, to tiny polyomaviruses. Recent comparative genomic analyses have revealed many evolutionary connections between dsDNA viruses of eukaryotes, bacteriophages, transposable elements, and linear DNA plasmids. These findings provide an evolu-tionary scenario that derives several major groups of eukaryotic dsDNA viruses, including the proposed order “Megavirales, ” adenoviruses, and virophages from a group of large virus-like transposons known as Polintons (Mav-ericks). The Polintons have been recently shown to encode two capsid proteins, suggesting that these elements lead a dual lifestyle with both a transposon and a viral phase and should perhaps more appropriately be named polin-toviruses. Here, we describe the recently identified evolutionary relationships between bacteriophages of the family Tectiviridae, polintoviruses, adenoviruses, virophages, large and giant DNA viruses of eukaryotes of the proposed order “Megavirales, ” and linearmitochondrial and cytoplasmic plasmids.We outline an evolutionary scenario under which the polintoviruses were the first group of eukaryotic dsDNA viruses that evolved from bacteriophages and became the ancestors of most large DNA viruses of eukaryotes and a variety of other selfish elements. Distinct lines of origin are detectable only for herpesviruses (from a different bacteriophage root) and polyoma/papillomaviruses (from single-stranded DNA viruses and ultimately from plasmids). Phylogenomic analysis of giant viruses provide

  • evolution of double stranded dna viruses of eukaryotes from bacteriophages to transposons to giant viruses
    Annals of the New York Academy of Sciences, 2015
    Co-Authors: Eugene V. Koonin, Mart Krupovic, Natalya Yutin
    Abstract:

    Diverse eukaryotes including animals and protists are hosts to a broad variety of viruses with double-stranded (ds) DNA genomes, from the largest known viruses, such as pandoraviruses and mimiviruses, to tiny polyomaviruses. Recent comparative genomic analyses have revealed many evolutionary connections between dsDNA viruses of eukaryotes, bacteriophages, transposable elements, and linear DNA plasmids. These findings provide an evolutionary scenario that derives several major groups of eukaryotic dsDNA viruses, including the proposed order “Megavirales,” adenoviruses, and virophages from a group of large virus-like transposons known as Polintons (Mavericks). The Polintons have been recently shown to encode two capsid proteins, suggesting that these elements lead a dual lifestyle with both a transposon and a viral phase and should perhaps more appropriately be named polintoviruses. Here, we describe the recently identified evolutionary relationships between bacteriophages of the family Tectiviridae, polintoviruses, adenoviruses, virophages, large and giant DNA viruses of eukaryotes of the proposed order “Megavirales,” and linear mitochondrial and cytoplasmic plasmids. We outline an evolutionary scenario under which the polintoviruses were the first group of eukaryotic dsDNA viruses that evolved from bacteriophages and became the ancestors of most large DNA viruses of eukaryotes and a variety of other selfish elements. Distinct lines of origin are detectable only for herpesviruses (from a different bacteriophage root) and polyoma/papillomaviruses (from single-stranded DNA viruses and ultimately from plasmids). Phylogenomic analysis of giant viruses provides compelling evidence of their independent origins from smaller members of the putative order “Megavirales,” refuting the speculations on the evolution of these viruses from an extinct fourth domain of cellular life.

Mart Krupovic - One of the best experts on this subject based on the ideXlab platform.

  • Vast diversity of prokaryotic virus genomes encoding double jelly-roll major capsid proteins uncovered by genomic and metagenomic sequence analysis
    Virology Journal, 2018
    Co-Authors: Natalya Yutin, Mart Krupovic, Disa Bäckström, Thijs J. G. Ettema, Eugene V. Koonin
    Abstract:

    Background Analysis of metagenomic sequences has become the principal approach for the study of the diversity of viruses. Many recent, extensive metagenomic studies on several classes of viruses have dramatically expanded the visible part of the virosphere, showing that previously undetected viruses, or those that have been considered rare, actually are important components of the global virome. Results We investigated the provenance of viruses related to tail-less bacteriophages of the family Tectiviridae by searching genomic and metagenomics sequence databases for distant homologs of the tectivirus-like Double Jelly-Roll major capsid proteins (DJR MCP). These searches resulted in the identification of numerous genomes of virus-like elements that are similar in size to tectiviruses (10–15 kilobases) and have diverse gene compositions. By comparison of the gene repertoires, the DJR MCP-encoding genomes were classified into 6 distinct groups that can be predicted to differ in reproduction strategies and host ranges. Only the DJR MCP gene that is present by design is shared by all these genomes, and most also encode a predicted DNA-packaging ATPase; the rest of the genes are present only in subgroups of this unexpectedly diverse collection of DJR MCP-encoding genomes. Only a minority encode a DNA polymerase which is a hallmark of the family Tectiviridae  and the putative family "Autolykiviridae". Notably, one of the identified putative DJR MCP viruses encodes a homolog of Cas1 endonuclease, the integrase involved in CRISPR-Cas adaptation and integration of transposon-like elements called casposons. This is the first detected occurrence of Cas1 in a virus. Many of the identified elements are individual contigs flanked by inverted or direct repeats and appear to represent complete, extrachromosomal viral genomes, whereas others are flanked by bacterial genes and thus can be considered as proviruses. These contigs come from metagenomes of widely different environments, some dominated by archaea and others by bacteria, suggesting that collectively, the DJR MCP-encoding elements have a broad host range among prokaryotes. Conclusions The findings reported here greatly expand the known host range of (putative) viruses of bacteria and archaea that encode a DJR MCP. They also demonstrate the extreme diversity of genome architectures in these viruses that encode no universal proteins other than the capsid protein that was used as the marker for their identification. From a supposedly minor group of bacterial and archaeal viruses, these viruses are emerging as a substantial component of the prokaryotic virome.

  • Bacteriophage GC1, a Novel Tectivirus Infecting Gluconobacter Cerinus, an Acetic Acid Bacterium Associated with Wine-Making
    Viruses, 2018
    Co-Authors: Cécile Philippe, Mart Krupovic, Fety Jaomanjaka, Olivier Claisse, Melina Petrel, Claire Le Marrec
    Abstract:

    The Gluconobacter phage GC1 is a novel member of the Tectiviridae family isolated from a juice sample collected during dry white wine making. The bacteriophage infects Gluconobacter cerinus, an acetic acid bacterium which represents a spoilage microorganism during wine making, mainly because it is able to produce ethyl alcohol and transform it into acetic acid. Transmission electron microscopy revealed tail-less icosahedral particles with a diameter of ~78 nm. The linear double-stranded DNA genome of GC1 (16,523 base pairs) contains terminal inverted repeats and carries 36 open reading frames, only a handful of which could be functionally annotated. These encode for the key proteins involved in DNA replication (protein-primed family B DNA polymerase) as well as in virion structure and assembly (major capsid protein, genome packaging ATPase (adenosine triphosphatase) and several minor capsid proteins). GC1 is the first tectivirus infecting an alphaproteobacterial host and is thus far the only temperate tectivirus of gram-negative bacteria. Based on distinctive sequence and life-style features, we propose that GC1 represents a new genus within the Tectiviridae, which we tentatively named "Gammatectivirus". Furthermore, GC1 helps to bridge the gap in the sequence space between alphatectiviruses and betatectiviruses.

  • ANNALS OF THE NEW YORK ACADEMY OF SCIENCES Issue:DNA Habitats and Their RNA Inhabitants Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses
    2016
    Co-Authors: Eugene V. Koonin, Mart Krupovic, Natalya Yutin
    Abstract:

    Diverse eukaryotes including animals and protists are hosts to a broad variety of viruses with double-stranded (ds) DNA genomes, from the largest known viruses, such as pandoraviruses and mimiviruses, to tiny polyomaviruses. Recent comparative genomic analyses have revealed many evolutionary connections between dsDNA viruses of eukaryotes, bacteriophages, transposable elements, and linear DNA plasmids. These findings provide an evolu-tionary scenario that derives several major groups of eukaryotic dsDNA viruses, including the proposed order “Megavirales, ” adenoviruses, and virophages from a group of large virus-like transposons known as Polintons (Mav-ericks). The Polintons have been recently shown to encode two capsid proteins, suggesting that these elements lead a dual lifestyle with both a transposon and a viral phase and should perhaps more appropriately be named polin-toviruses. Here, we describe the recently identified evolutionary relationships between bacteriophages of the family Tectiviridae, polintoviruses, adenoviruses, virophages, large and giant DNA viruses of eukaryotes of the proposed order “Megavirales, ” and linearmitochondrial and cytoplasmic plasmids.We outline an evolutionary scenario under which the polintoviruses were the first group of eukaryotic dsDNA viruses that evolved from bacteriophages and became the ancestors of most large DNA viruses of eukaryotes and a variety of other selfish elements. Distinct lines of origin are detectable only for herpesviruses (from a different bacteriophage root) and polyoma/papillomaviruses (from single-stranded DNA viruses and ultimately from plasmids). Phylogenomic analysis of giant viruses provide

  • evolution of double stranded dna viruses of eukaryotes from bacteriophages to transposons to giant viruses
    Annals of the New York Academy of Sciences, 2015
    Co-Authors: Eugene V. Koonin, Mart Krupovic, Natalya Yutin
    Abstract:

    Diverse eukaryotes including animals and protists are hosts to a broad variety of viruses with double-stranded (ds) DNA genomes, from the largest known viruses, such as pandoraviruses and mimiviruses, to tiny polyomaviruses. Recent comparative genomic analyses have revealed many evolutionary connections between dsDNA viruses of eukaryotes, bacteriophages, transposable elements, and linear DNA plasmids. These findings provide an evolutionary scenario that derives several major groups of eukaryotic dsDNA viruses, including the proposed order “Megavirales,” adenoviruses, and virophages from a group of large virus-like transposons known as Polintons (Mavericks). The Polintons have been recently shown to encode two capsid proteins, suggesting that these elements lead a dual lifestyle with both a transposon and a viral phase and should perhaps more appropriately be named polintoviruses. Here, we describe the recently identified evolutionary relationships between bacteriophages of the family Tectiviridae, polintoviruses, adenoviruses, virophages, large and giant DNA viruses of eukaryotes of the proposed order “Megavirales,” and linear mitochondrial and cytoplasmic plasmids. We outline an evolutionary scenario under which the polintoviruses were the first group of eukaryotic dsDNA viruses that evolved from bacteriophages and became the ancestors of most large DNA viruses of eukaryotes and a variety of other selfish elements. Distinct lines of origin are detectable only for herpesviruses (from a different bacteriophage root) and polyoma/papillomaviruses (from single-stranded DNA viruses and ultimately from plasmids). Phylogenomic analysis of giant viruses provides compelling evidence of their independent origins from smaller members of the putative order “Megavirales,” refuting the speculations on the evolution of these viruses from an extinct fourth domain of cellular life.

Jacques Mahillon - One of the best experts on this subject based on the ideXlab platform.

  • Phages preying on Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis: past, present and future.
    Viruses, 2014
    Co-Authors: Annika Gillis, Jacques Mahillon
    Abstract:

    Many bacteriophages (phages) have been widely studied due to their major role in virulence evolution of bacterial pathogens. However, less attention has been paid to phages preying on bacteria from the Bacillus cereus group and their contribution to the bacterial genetic pool has been disregarded. Therefore, this review brings together the main information for the B. cereus group phages, from their discovery to their modern biotechnological applications. A special focus is given to phages infecting Bacillus anthracis, B. cereus and Bacillus thuringiensis. These phages belong to the Myoviridae, Siphoviridae, Podoviridae and Tectiviridae families. For the sake of clarity, several phage categories have been made according to significant characteristics such as lifestyles and lysogenic states. The main categories comprise the transducing phages, phages with a chromosomal or plasmidial prophage state, γ-like phages and jumbo-phages. The current genomic characterization of some of these phages is also addressed throughout this work and some promising applications are discussed here.

  • Prevalence, genetic diversity and host range of tectiviruses among members of the Bacillus cereus group
    Applied and Environmental Microbiology, 2014
    Co-Authors: Annika Gillis, Jacques Mahillon
    Abstract:

    Tectiviridae comprises non-enveloped tail-less phages with a double-layer capsid where the ~15 kb linear dsDNA is located within a lipid-containing membrane/vesicle covered by a rigid icosahedral protein capsid. Upon infection the lipid membrane becomes a tail-like structure used in genome delivery. GIL01/Bam35, GIL16, AP50 and Wip1 are tectiviruses preying on the Bacillus cereus group. These phages also exhibit a strong similarity to the B. cereus linear plasmid pBClin15. Tectiviruses infecting the B. cereus group are temperate phages able to replicate autonomously as linear plasmids inside the host cell. Despite the significant contributions of phages in different biological processes, little is known about the relations taking place between tectiviruses and their Gram-positive hosts. Therefore, this work focuses on characterizing the interactions between tectiviruses and the B. cereus group, by assessing their occurrence, genetic diversity and evaluating their host range. To study the occurrence of tectiviruses in the B. cereus group, 2,000 worldwide isolates, comprising all seven recognized members of this bacterial group, were evaluated using primers designed on two variable regions detected in previously described elements. The first variable region is located within the module that contains replication and regulatory genes (coordinates 3,162 - 4,442 in GIL01), referred to herein as the “RR region”, and codes for the C-terminal end of the DNA polymerase B protein (DNA polB, CDS 5 in GIL01) and for the N-terminal part of the LexA-like protein (CDS 6). The second variable region is located within the module containing the host recognition and cell lysis genes (coordinates 11,096 - 11,838 in GIL01), herein referred to as the “PL region”, and targets the N-acetyl-muramidase coding gene (mur1, CDS 26) and partially CDS 27 for which the predicted function is related to the pentameric spike base involved in host recognition. PCR screenings targeting the RR and PL regions, along with propagation tests, revealed that tectiviral elements occurred in less than 3 % of the isolates. Regardless of this limited distribution, 47 novel putative tectiviruses were discovered in the present work, beside the 10 members already known (including Sole, Sand, Sato, Emet and Lima). Overall, these findings (i) expand the view of tectiviral prophages occurrence in members of the B. cereus group, providing evidence for (ii) a greater genetic diversity than previously observed within the Tectiviridae. In addition, analyses of the selected variable regions, along with their host range, showed that tectiviruses in the B. cereus group can be clustered mainly into two different groups: the ones infecting B. anthracis and those isolated from other B. cereus group members. In order to address the host range of some novel tectiviruses, 120 strains, which did not harbor tectiviral-elements, were tested for sensitivity. The results showed that all the tested tectiviruses produced lysis in at least one B. cereus sensu lato strain. Moreover, no simple relationship was found between the infection patterns of the tectiviruses and their diversity. Moreover, the genomic data exposed that diversity and apparent relationships between tectiviruses will differ with the analyzed variable region and if genes are subjected to different evolutionary processes, like recombination. As a consequence, the PL region is proposed to be used in large tectiviral occurrence screenings, whereas the RR region could be used to analyze the bona fide diversity. From an evolutionary perspective, the results indicate that the DNA polB gene has undergone genetic recombination, although the actual contribution of this event remained to be further explored.

  • Phenotype sequencing uncovers mutations in candidate genes that mediate tectivirus-resistance in Bacillus thuringiensis
    2014
    Co-Authors: Annika Gillis, Marc Harper, Christopher W. Lee, Jacques Mahillon
    Abstract:

    The family Tectiviridae is a relative rare group that includes tail-less phages having a membrane beneath their icosahedral protein shell, formed of approximately equal amounts of virus-encoded proteins and lipids derived from the host cell plasma membrane. The 15 kb linear dsDNA genomes have long inverted terminal repeat sequences (~100 bp) and are coiled within the lipid membrane. This family contains two groups of phages: the lytic PRD1-like infecting Gram-negative enterobacteria, and the temperate ones preying on Gram-positive bacteria belonging to the Bacillus cereus group. Phages GIL01, GIL16, Bam35, AP50 and Wip1 are the fully-sequenced representatives of the second group. GIL01 and relatives are capable to reside as temperate phages that do not integrate into the host genome upon infection and remain as an autonomous linear plasmid in the cell. Therefore, it is important to understand the selective pressures undergone by the bacteria when facing this type of phages. The aim of this work was to study the primary interaction between these tectiviruses and their host, and the phenotypes of bacterial resistances triggered by the presence of these phages. For this purpose, Bacillus thuringiensis sv. israelensis strain GBJ002 was subjected to a selective pressure after repetitive propagation with clear plaque (CP) mutants of GIL01 and GIL16. The CP mutants showed an elevated efficiency of killing mainly because they propagate exclusively lytically. Twenty completely tectivirus-resistant bacterial mutants were isolated. These resistant bacteria showed differences in colony morphotype and displayed distinct adaptation features, such as biofilm formation, sporulation rate, swarming motility, exopolysaccharide production and some differences in metabolic profiles. These observations indicated that tectiviruses may drive life-trait changes and ecological adaptations in the B. cereus group members, as results of a phage-selective pressure. To unravel the genetic changes responsible for the phage-resistant phenotype, a whole genome sequencing method was approached. Using a pooled high-throughput sequencing analysis of multiple independent mutants, potential genes causing the tectivirus-resistant phenotype in B. thuringiensis were identified. Several genes associated with cell-wall metabolism and turn-over, as well as cell-surface proteins, have been pinpointed. Currently these candidate genes are been studied intensely to confirm their enrolment in the bacteriophage-resistant phenotype. These results have shed new light on the cell wall component(s) that could act as receptor(s) or mediate the interaction between these phages and their hosts. This approach will also permit to gain insights into the different strategies used by bacteria to elude phage infection.

  • Snapshot of tectiviruses preying on the Bacillus cereus sensu lato group
    2013
    Co-Authors: Annika Gillis, Jacques Mahillon
    Abstract:

    Tectiviridae comprises non-enveloped tail-less phages with a double-layer capsid where the ~15 kb linear dsDNA is located within a lipid-containing membrane covered by a rigid icosahedral protein capsid. GIL01/Bam35, GIL16 and AP50 are temperate tectiviruses preying on the Bacillus cereus sensu lato group. These phages also exhibit a strong similarity to the B. cereus linear plasmid pBClin15. Despite the significant contributions of phages in different environments and biological processes, little is known about the interactions taking place between tectiviruses and their respective Gram-positive hosts. Therefore, this work aimed at characterizing the interactions between tectiviruses and the B. cereus sensu lato group, mainly by assessing their occurrence, diversity and exploiting their host range. To study the occurrence of tectiviral-elements, 2,000 strains belonging to the B. cereus s.l. group were assessed, using primers designed based on whole genome alignments of previously described tectiviral-elements. This strain collection included all recognized B. cereus s.l. species. PCR and propagation tests revealed that tectiviral-elements occurred in less than 3% of the examined strains. Despite its limited distribution, some novel tectiviruses were found, and partial DNA sequencing indicated that a greater diversity exists within the Tectiviridae. In an effort to address the host-range of some new tectiviruses found in this work, 120 strains belonging to the B. cereus s.l. group, which did not harbour tectiviral- elements, were tested for sensitivity. The results showed that nearly all the tectiviruses produced lysis in more than one strain, despite their narrow host-range. Beyond a fundamental contribution towards understanding the general infection structure and resistance patterns between tectiviruses and this B. cereus group, this study should provide information needed to develop tools for typing and controlling bacteria belonging to this group.

  • The enemy insight: tectiviruses preying on the Bacillus cereus sensu lato group
    2013
    Co-Authors: Annika Gillis, Pierre Wattiau, Jacques Mahillon
    Abstract:

    Tectiviridae comprises non-enveloped tail-less phages with a double-layer capsid where the ~15 kb linear dsDNA is located within a lipid-containing membrane covered by a rigid icosahedral protein capsid. GIL01/Bam35, GIL16 and AP50 are temperate tectiviruses preying on the B. cereus group. These phages also exhibit a strong similarity to the B. cereus linear plasmid pBClin15. Despite the significant contributions of phages in different environments and biological processes, little is known about the interactions taking place between tectiviruses and their respective Grampositive hosts. Therefore, this work aimed at characterizing the interactions between tectiviruses and the B. cereus sensu lato group, mainly by assessing their occurrence, diversity and exploiting their host range. To study the occurrence of tectiviral-elements, more than 2,300 strains belonging to the B. cereus group were assessed, using primers designed based on whole genome alignments of previously described tectiviral-elements. This strain collection included all recognized B. cereus sensu lato species, except Bacillus cytotoxicus. PCR and propagation tests revealed that tectiviral-elements occurred in less than 2.5% of the examined strains. Despite its limited distribution, some novel tectiviruses were found, and partial DNA sequencing indicated that a greater diversity exists within the Tectiviridae. In an effort to address the host-range of some new tectiviruses found in this work, 120 strains belonging to the B. cereus sensu lato group, which did not harbor tectiviral elements, were tested for sensitivity. The results showed that nearly all the tectiviruses produced lysis in more than one strain, despite their narrow host-range. Additionally, some life-trait changes and ecological adaptations were observed in known sensitive strains when they were challenged with tectiviruses. Beyond a fundamental contribution towards understanding the general infection structure and resistance patterns between tectiviruses and this B. cereus group, this study should provide information needed to develop tools for typing and controlling bacteria belonging to this group.

Jaana K. H. Bamford - One of the best experts on this subject based on the ideXlab platform.

  • Integral membrane protein P16 of bacteriophage PRD1 stabilizes the adsorption vertex structure
    2015
    Co-Authors: Silja T. Jaatinen, Dennis H. Bamford, Salla J. Viitanen, Jaana K. H. Bamford
    Abstract:

    The icosahedral membrane-containing double-stranded DNA bacteriophage PRD1 has a labile receptor binding spike complex at the vertices. This complex, which is analogous to that of adenovirus, is formed of the penton protein P31, the spike protein P5, and the receptor binding protein P2. Upon infection, the internal phage membrane transforms into a tubular structure that protrudes through a vertex and penetrates the cell envelope for DNA injection. We describe here a new class of PRD1 mutants lacking virion-associated integral membrane protein P16. P16 links the spike complex to the viral membrane and is necessary for spike stability. We also show that the unique vertex used for DNA packaging is intact in the P16-deficient particle, indicating that the 11 adsorption vertices and the 1 portal vertex are functionally and structurally distinct. PRD1 is the type organism of the Tectiviridae family (4, 5, 31). It is a broad-host-range bacterial virus that infects a variety of gram-negative hosts harboring an N, P, or W incompatibility group conjugative antibiotic resistance plasmid (46). The plas-mid encodes a type IV transenvelope DNA translocation com-plex, which functions as a receptor for PRD1. The PRD1 virion consists of an icosahedral protein capsid surrounding a

  • Probing protein interactions in the membrane-containing virus PRD1.
    Journal of General Virology, 2015
    Co-Authors: Sari Mattila, Hanna M. Oksanen, Jaana K. H. Bamford
    Abstract:

    PRD1 is a Gram-negative bacteria infecting complex tailless icosahedral virus with an inner membrane. This type virus of the family Tectiviridae contains at least 18 structural protein species, of which several are membrane associated. Vertices of the PRD1 virion consist of complexes recognizing the host cell, except for one special vertex through which the genome is packaged. Despite extensive knowledge of the overall structure of the PRD1 virion and several individual proteins at the atomic level, the locations and interactions of various integral membrane proteins and membrane-associated proteins still remain a mystery. Here, we demonstrated that blue native PAGE can be used to probe proteinprotein interactions in complex membrane-containing viruses. Using this technique and PRD1 as a model, we identified the known PRD1 multiprotein vertex structure composed of penton protein P31, spike protein P5, receptor-binding protein P2 and stabilizing protein P16 linking the vertex to the internal membrane. Our results also indicated that two transmembrane proteins, P7 and P14, involved in viral nucleic acid delivery, make a complex. In addition, we performed a zymogram analysis using mutant particles devoid of the special vertex that indicated that the lytic enzyme P15 of PRD1 was not part of the packaging vertex, thus contradicting previously published results.

  • Purified membrane-containing procapsids of bacteriophage PRD1 package the viral genome.
    Journal of Molecular Biology, 2009
    Co-Authors: Gabija Žiedaitė, Jaana K. H. Bamford, Hanna M. Kivelä, Dennis H. Bamford
    Abstract:

    Icosahedral-tailed double-stranded DNA (dsDNA) bacteriophages and herpesviruses translocate viral DNA into a preformed procapsid in an ATP-driven reaction by a packaging complex that operates at a portal vertex. A similar packaging system operates in the tailless dsDNA phage PRD1 (Tectiviridae family), except that there is an internal membrane vesicle in the procapsid. The unit-length linear dsDNA genome with covalently linked 5'-terminal proteins enters the procapsid through a unique vertex. Two small integral membrane proteins, P20 and P22, provide a conduit for DNA translocation. The packaging machinery also contains the packaging ATPase P9 and the packaging efficiency factor P6. Here we describe a method used to obtain purified packaging-competent PRD1 procapsids. The optimized in vitro packaging system allowed efficient packaging of defined DNA substrates. We determined that the genome terminal protein P8 is necessary for packaging and provided an estimation of the packaging rate.

  • Molecular Characterization of a Variant of Bacillus anthracis-Specific Phage AP50 with Improved Bacteriolytic Activity
    Applied and Environmental Microbiology, 2008
    Co-Authors: Shanmuga Sozhamannan, Michael Mckinstry, Shannon M. Lentz, Matti Jalasvuori, Farrell Mcafee, Angela Smith, Jason Dabbs, Hans-w. Ackermann, Jaana K. H. Bamford, Alfred J. Mateczun
    Abstract:

    The genome sequence of a Bacillus anthracis-specific clear plaque mutant phage, AP50c, contains 31 open reading frames spanning 14,398 bp, has two mutations compared to wild-type AP50t, and has a colinear genome architecture highly similar to that of gram-positive Tectiviridae phages. Spontaneous AP50c-resistant B. anthracis mutants exhibit a mucoid colony phenotype.

  • Preliminary crystallographic analysis of the major capsid protein P2 of the lipid-containing bacteriophage PM2.
    Acta Crystallographica Section F Structural Biology and Crystallization Communications, 2005
    Co-Authors: Nicola G. A. Abrescia, Jaana K. H. Bamford, Dennis H. Bamford, Hanna M. Kivelä, Jonathan M. Grimes, David I. Stuart
    Abstract:

    PM2 (Corticoviridae) is a dsDNA bacteriophage which contains a lipid membrane beneath its icosahedral capsid. In this respect it resembles bacteriophage PRD1 (Tectiviridae), although it is not known whether the similarity extends to the detailed molecular architecture of the virus, for instance the fold of the major coat protein P2. Structural analysis of PM2 has been initiated and virus-derived P2 has been crystallized by sitting-nanodrop vapour diffusion. Crystals of P2 have been obtained in space group P21212, with two trimers in the asymmetric unit and unit-cell parameters a = 171.1, b = 78.7, c = 130.1 A. The crystals diffract to 4 A resolution at the ESRF BM14 beamline (Grenoble, France) and the orientation of the non-crystallographic threefold axes, the spatial relationship between the two trimers and the packing of the trimers within the unit cell have been determined. The trimers form tightly packed layers consistent with the crystal morphology, possibly recapitulating aspects of the arrangement of subunits in the virus.