Hans-Wolfgang Ackermann

Taxonomy of bacterial viruses: establishment of tailed virus genera and the other Caudovirales

SummaryBacterial viruses have been classified into 13 families and 1 unassigned genus. A new order, Caudovirales, has now been established, comprising the three families of tailed bacterial viruses, based on similarities in tailed virus morphology, replication, and assembly. In addition, genera have been established for some species in each tailed virus family, based on properties involving viral DNA replication and packaging, and on some features specific to particular genera (e.g., DNA-termini linked proteins, virus-encoded polymerases, and ability to establish temperate infections). At present, there are six genera in the family Myoviridae (viruses with contractile tails), six in the family Siphoviridae (viruses with long, noncontractile tails), and three in the family Podoviridae (viruses with short noncontractile tails). In recognition that the definitions of tailed virus genera represent a “work in progress” and to keep the nomenclature flexible, tailed virus genera have been assigned vernacular names based on their type species.

A catalogue of T4-type bacteriophages

SummaryThe T4-type of bacteriophages is broadly defined on the basis of particle morphology. It occurs in enterobacteria (125 representatives), acinetobacters, aeromonads, pseudomonads, and vibrios (16 isolates). In addition, 18 apparently unrelated phages with prolate heads and contractile tails are found in a wide range of bacteria. A descriptive catalogue of these phages is presented. The T4-type probably originated in precursors of enterobacteria.

Isolation and characterization of Thermus bacteriophages

Summary.One-hundred-fifteen bacteriophage strains were isolated from alkaline hot springs in Iceland, New Zealand, Russia (Kamchatka), and the U.S.A. The phages belonged to the Myoviridae, Siphoviridae, Tectiviridae, and Inoviridae families. Over 50% of isolates were isometric or filamentous. One type of siphovirus had giant tails of over 800 nm in length. Phages were further characterized by host range, genome size, DNA restriction endonuclease digestion patterns, and temperature and pH sensitivity. Myoviruses and tectiviruses had a worldwide distribution. Most phages were narrowly host-specific and all were highly resistant against heating and alkaline and acidic pH. This is the first time that tectiviruses and filamentous phages are reported for bacteria of the Thermus-Deinococcus phylum. The presence of tectiviruses, inoviruses, and myoviruses is attributed to acquisition from ancestral γ-proteobacteria by horizontal gene transfer.

The species concept and its application to tailed phages.

SummaryA recently proposed polythetic definition of virus species appears easily applicable to bacteriophages. Criteria for classification of tailed phages are evaluated. Morphology, DNA homology, and serology are the most important criteria for delineation of species, but no single criterion is satisfactory. Dot-blot hybridization and seroneutralization may suggest false relationships by detecting common sequences in the DNA of otherwise unrelated phages. Species of tailed phages can be defined by a combination of morphology and DNA homology or serology. A procedure for identification of novel phages is outlined. Phage names should include elements of host names.

Frequency of morphological phage descriptions in 1995

SummaryAt least 4500 bacterial viruses have been examined in the electron microscope since 1959. About 4400 phages (96%) are tailed and only 162 phages (4%) are cubic, filamentous, or pleomorphic. Phages belong to 12 virus families and occur in about 130 bacterial genera. Phages are listed by morphotypes and host genera.Siphoviridae or phages with long, noncontractile tails include about 60% of tailed phages.

Taxonomy of prokaryotic viruses: update from the ICTV bacterial and archaeal viruses subcommittee

The prokaryotic virus community is represented on the International Committee on Taxonomy of Viruses (ICTV) by the Bacterial and Archaeal Viruses Subcommittee. In 2008, the three caudoviral families Myoviridae, Podoviridae, and Siphoviridae included only 18 genera and 36 species. Under the able chairmanship of Rob Lavigne (KU Leuven, Belgium), major advances were made in the classification of prokaryotic viruses and the order Caudovirales was expanded dramatically, to reflect the genome-based relationships between phages. Today, the order includes six subfamilies, 80 genera, and 441 species. This year, additional changes in prokaryotic virus taxonomy have been brought forward under the new subcommittee chair, Andrew M. Kropinski (University of Guelph, Canada). These changes are:

Phage morphology recapitulates phylogeny: the comparative genomics of a new group of myoviruses.

Among dsDNA tailed bacteriophages (Caudovirales), members of the Myoviridae family have the most sophisticated virion design that includes a complex contractile tail structure. The Myoviridae generally have larger genomes than the other phage families. Relatively few “dwarf” myoviruses, those with a genome size of less than 50 kb such as those of the Mu group, have been analyzed in extenso. Here we report on the genome sequencing and morphological characterization of a new group of such phages that infect a diverse range of Proteobacteria, namely Aeromonas salmonicida phage 56, Vibrio cholerae phages 138 and CP-T1, Bdellovibrio phage φ1422, and Pectobacterium carotovorum phage ZF40. This group of dwarf myoviruses shares an identical virion morphology, characterized by usually short contractile tails, and have genome sizes of approximately 45 kb. Although their genome sequences are variable in their lysogeny, replication, and host adaption modules, presumably reflecting differing lifestyles and hosts, their structural and morphogenesis modules have been evolutionarily constrained by their virion morphology. Comparative genomic analysis reveals that these phages, along with related prophage genomes, form a new coherent group within the Myoviridae. The results presented in this communication support the hypothesis that the diversity of phages may be more structured than generally believed and that the innumerable phages in the biosphere all belong to discrete lineages or families.

A suggested classification for two groups of Campylobacter myoviruses

Most Campylobacter bacteriophages isolated to date have long contractile tails and belong to the family Myoviridae. Based on their morphology, genome size and endonuclease restriction profile, Campylobacter phages were originally divided into three groups. The recent genome sequencing of seven virulent campylophages reveal further details of the relationships between these phages at the genome organization level. This article details the morphological and genomic features among the campylophages, investigates their taxonomic position, and proposes the creation of two new genera, the “Cp220likevirus” and “Cp8unalikevirus” within a proposed subfamily, the “Eucampyvirinae”

Genomic, Proteomic and Physiological Characterization of a T5-like Bacteriophage for Control of Shiga Toxin-Producing Escherichia coli O157:H7

Despite multiple control measures, Escherichia coli O157:H7 (STEC O157:H7) continues to be responsible for many food borne outbreaks in North America and elsewhere. Bacteriophage therapy may prove useful for controlling this pathogen in the host, their environment and food. Bacteriophage vB_EcoS_AKFV33 (AKFV33), a T5-like phage of Siphoviridae lysed common phage types of STEC O157:H7 and not non-O157 E. coli. Moreover, STEC O157:H7 isolated from the same feedlot pen from which the phage was obtained, were highly susceptible to AKFV33. Adsorption rate constant and burst size were estimated to be 9.31×10−9 ml/min and 350 PFU/infected cell, respectively. The genome of AKVF33 was 108,853 bp (38.95% G+C), containing 160 open reading frames (ORFs), 22 tRNA genes and 32 strong promoters recognized by host RNA polymerase. Of 12 ORFs without homologues to T5-like phages, 7 predicted novel proteins while others exhibited low identity (<60%) to proteins in the National Centre for Biotechnology Information database. AKVF33 also lacked the L-shaped tail fiber protein typical of T5, but was predicted to have tail fibers comprised of 2 novel proteins with low identity (37–41%) to tail fibers of E. coli phage phiEco32 of Podoviridae, a putative side tail fiber protein of a prophage from E. coli IAI39 and a conserved domain protein of E. coli MS196-1. The receptor-binding tail protein (pb5) shared an overall identify of 29–72% to that of other T5-like phages, with no region coding for more than 6 amino acids in common. Proteomic analysis identified 4 structural proteins corresponding to the capsid, major tail, tail fiber and pore-forming tail tip (pb2). The genome of AKFV33 lacked regions coding for known virulence factors, integration-related proteins or antibiotic resistance determinants. Phage AKFV33 is a unique, highly lytic STEC O157:H7-specific T5-like phage that may have considerable potential as a pre- and post-harvest biocontrol agent.

Evidence of a Dominant Lineage of Vibrio cholerae-Specific Lytic Bacteriophages Shed by Cholera Patients over a 10-Year Period in Dhaka, Bangladesh

ABSTRACT Lytic bacteriophages are hypothesized to contribute to the seasonality and duration of cholera epidemics in Bangladesh. However, the bacteriophages contributing to this phenomenon have yet to be characterized at a molecular genetic level. In this study, we isolated and sequenced the genomes of 15 bacteriophages from stool samples from cholera patients spanning a 10-year surveillance period in Dhaka, Bangladesh. Our results indicate that a single novel bacteriophage type, designated ICP1 (for the International Centre for Diarrhoeal Disease Research, Bangladesh cholera phage 1) is present in all stool samples from cholera patients, while two other bacteriophage types, one novel (ICP2) and one T7-like (ICP3), are transient. ICP1 is a member of the Myoviridae family and has a 126-kilobase genome comprising 230 open reading frames. Comparative sequence analysis of ICP1 and related isolates from this time period indicates a high level of genetic conservation. The ubiquitous presence of ICP1 in cholera patients and the finding that the O1 antigen of lipopolysaccharide (LPS) serves as the ICP1 receptor suggest that ICP1 is extremely well adapted to predation of human-pathogenic V. cholerae O1. IMPORTANCE The severe diarrheal disease cholera is caused by the bacterium Vibrio cholerae, which can be transmitted to humans from the aquatic environment. Factors that affect V. cholerae in the environment can impact the occurrence of cholera outbreaks; one of these factors is thought to be the presence of bacterial viruses, or bacteriophages. Bacteriophages that prey on V. cholerae in the environment, and potentially in humans, have not been extensively genetically characterized. Here, we isolated and sequenced the genomes of bacteriophages from cholera patient stool samples collected over a 10-year period in Dhaka, Bangladesh, a region that suffers from regular cholera outbreaks. We describe a unique bacteriophage present in all samples, infer its evolution by sequencing multiple isolates from different patients over time, and identify the host receptor that shows that the bacteriophage specifically predates the serogroup of V. cholerae responsible for the majority of disease occurrences. The severe diarrheal disease cholera is caused by the bacterium Vibrio cholerae, which can be transmitted to humans from the aquatic environment. Factors that affect V. cholerae in the environment can impact the occurrence of cholera outbreaks; one of these factors is thought to be the presence of bacterial viruses, or bacteriophages. Bacteriophages that prey on V. cholerae in the environment, and potentially in humans, have not been extensively genetically characterized. Here, we isolated and sequenced the genomes of bacteriophages from cholera patient stool samples collected over a 10-year period in Dhaka, Bangladesh, a region that suffers from regular cholera outbreaks. We describe a unique bacteriophage present in all samples, infer its evolution by sequencing multiple isolates from different patients over time, and identify the host receptor that shows that the bacteriophage specifically predates the serogroup of V. cholerae responsible for the majority of disease occurrences.