DESCRIPTION OF VIRUSES

Order Caudovirales

Introduction

Introduction

Taxonomic Structure of the Order

Order

Caudovirales

Family

    Myoviridae

Genus

        “T4-like Viruses”

Genus

        “P1-like Viruses”

Genus

        “P2-like Viruses”

Genus

        “Mu-like Viruses”

Genus

        “SP01-like Viruses”

Genus

        “H-like Viruses”

Family

    Siphoviridae

Genus

        “-like Viruses”

Genus

        “T1-like Viruses”

Genus

        “T5-like Viruses”

Genus

        “L5-like Viruses”

Genus

        “c2-like Viruses”

Genus

        “M1-like Viruses”

Family

    Podoviridae

Genus

        “T7-like Viruses”

Genus

        “P22-like Viruses”

Genus

        “29-like Viruses”

General

The order consists of the three families of tailed bacterial viruses infecting Bacteria and Archaea: the Myoviridae (long contractile tails), Siphoviridae (long non-contractile tails), and Podoviridae (short non-contractile tails). Tailed bacterial viruses are an extremely large group with highly diverse virion, genomic, and replicative properties. Over 4,500 descriptions have been published (accounting for 96% of reported bacterial viruses): 24% in the Myoviridae, 62% in the Siphoviridae, and 14% in the Podoviridae. However, data on virion structure, genome organization, and replicative properties are available for only a small number of well-studied species. The great evolutionary age, large population sizes, and extensive horizontal gene transfer between bacterial cells and viruses have erased or obscured many taxonomic and phylogenetic relationships amongst tailed viruses. However, enough common morphological and replication features survive to indicate their fundamental relatedness.

Taxon names are Latinized at the order and family levels, ending in -virales and -viridae, respectively. At the genus level, thus far, only vernacular names have been established, ending in “-like viruses”.

Virion Properties

Morphology

The virion has no envelope and consists of a capsid or head (a protein shell containing one molecule of linear dsDNA) and a helix-based tail (a protein tube for adsorption and DNA injection into host cells). Head and tail are joined by a connector.

Heads are icosahedra or elongated derivatives thereof (proposed triangulation numbers T = 1, 3, 4, 7 and 13). Capsomers are hexagonal or pentagonal and seldom visible, heads usually appear smooth and thin-walled (2-3  nm). Estimated capsomer numbers vary between 17 and 812. A commonly reported structure is a capsid with 72 capsomers (T = 7). Isometric heads are 45-170  nm in diameter. Elongated heads derive from icosahedra by addition of rows of capsomers and are bipyramidal antiprisms up to 230  nm long. DNA forms a tightly packed coil inside the head. Tails have three- or six-fold symmetry, and are helical or consist of stacked disks of subunits, varying between 3 and 825  nm in length, usually provided with base plates, spikes, or terminal fibers. Some viruses have collars, head or collar appendages, transverse tail disks, or other attachments.

Physicochemical and Physical Properties

Virion Mr ranges from 29 to 470 106; S20w is 226-1230S. Both values may be higher, as the largest viruses have not been studied in this respect. Buoyant density in CsCl is about 1.49  g/cm3. Most tailed viruses are stable at pH 5-9: a few are stable at pH 2 or pH 11. Heat sensitivity is variable and resembles that of the host. Many viruses are inactivated by heating at 56-60°C for 30 min. Tailed viruses are rather resistant to UV irradiation. Heat and UV inactivation generally follow first-order kinetics. Many tailed viruses are ether- and chloroform-sensitive. Inactivation by nonionic detergents is variable and partly concentration dependent.

Nucleic Acid

Virions contain one molecule of linear dsDNA. Genome sizes range from 19 to about 700  kbp, corresponding to Mr values of 11-490 106. Relative DNA content is about 45%. G+C contents range between 27 and 72% and usually resemble those of host DNA. Some viral DNAs contain unusual bases which partially or completely replace normal nucleotides (e.g. 5-hydroxymethylcytosine), or are glycosylated or associated with internal proteins or basic polyamines.

Proteins

The number of structural proteins varies between 7 and 42. The Mr range is 4-200 103. All phages seem to have a lysozyme and a holin located at the tail tip; the spikes of some capsule-specific viruses have endoglycosidase activity. Certain viruses code for or contain DNA or RNA transcriptases, dihydrofolate reductase, or thymidylate synthetase.

Lipids

Most virions contain no lipid. Up to 15% lipid has been found in a few viruses of mycobacteria; its presence in others is doubtful.

Carbohydrates

Glycoproteins, glycolipids, hexosamine, and a polysaccharide have been found in individual viruses.

Genome Organization and Replication

Genome Organization

Genomes are linear, include between 27 and over 200 genes, and seem to consist of interchangeable blocks or “modules”. Genomes may have pac (packaging) and cos sites (cohesive or “sticky” ends), circular permutations and terminal redundancies, single-stranded gaps, or terminal proteins. Genomes of temperate phages generally contain a cluster of integration genes. Genes with related functions generally cluster together; however, some phages show evidence for considerable gene rearrangement during evolution. Functional genomic maps are very diverse and available for only a small number of tailed viruses.

Replication

In typical virulent infections (excluding Enterobacteria phage Mu (Mu) and Enterobacteria phage 29 (29)), after entering the host cell, viral DNA either may circularize or remain linear. DNA replication generally starts at fixed sites, is semiconservative, may be either bidirectional or unidirectional, and results in the formation of concatemers (multimeric DNA molecules) by recombination between linear phage DNAs or by rolling circle replication. Progeny viral DNA is cleaved from concatemeric DNA: (i) at unique sites to produce identical DNA molecules with cos sites or blunt-end termini, or (ii) at pac sites or at random to produce DNA molecules with circular permutations and terminal redundancies. Gene expression is largely time-ordered and sequential. “Early genes“ are involved in host cell regulation and viral DNA replication. “Late genes” specify structural proteins and lysis proteins. Transcription usually requires host RNA polymerase. Translational control is poorly understood and no generalizations are possible at the present state of knowledge. See Fig. 1.

A few viruses use terminal proteins to prime DNA replication and to package progeny viral DNA (29 and its relatives) and produce unit-length DNA instead of concatemers (Mu, 29).

Virion Assembly and DNA Packaging

Virion assembly is complex and includes separate pathways for each major structure (head, tail, tail fibers). Head assembly usually starts at the cell periphery with a portal and a scaffolding protein. A prohead is formed which matures by proteolytic cleavage of subunits and expands in the process. Simultaneously, progeny DNA is cut to unit size and packaged into phage heads. Virion assembly is completed by addition of a protein tail to, or assembly of a protein tail on, a matured DNA-filled head. Some viruses form intracellular arrays and many produce aberrant structures (polyheads, polytails, giant, multitailed, or misshapen particles). Progeny viruses are liberated by lysis of the host cell.

Antigenic Properties

Viruses are antigenically complex and efficient immunogens, inducing the formation of neutralizing and complement-fixing antigens. The existence of group antigens is likely in species or genera.

Biological Properties

Infection

Virions are virulent or temperate. Virulent infection normally results in production of progeny viruses and destruction of the host. Phages adsorb tail first to specific protein or lipoprotein host cell receptors, which are generally located on the cell wall. In a few cases, not represented by the genera described below, the primary adsorption sites are capsules, flagella, or pili. Cell walls are digested by bacterial virus lysozyme and viral DNA enters the cytoplasm by as yet unknown mechanisms. Empty virion shells remain outside the infected bacterium.

Latency

All three families include genera or species of temperate viruses. Viral genomes in lysogenized cells are integrated into host cell chromosomes or persist as extrachromosomal elements (plasmids). Integration is generally mediated by a “-type” integrase.

Host Range

Tailed viruses have been found in over 140 genera representing most branches of the Bacteria and Archaea phylogenetic trees. The viruses are usually host genus-specific; however, enterobacterial phages are specific for the family Enterobacteriaceae.

Transmission in Nature

Viruses are carried and transmitted by watery media or accidental contact with contaminated substrates or vectors. Specific vectors are not known.

Geographic Distribution

Tailed phages have a worldwide distribution and share the ecological niches of their hosts. The most important habitat is lysogenic bacteria. Some phages, although found over the world, are restricted to particular environments such as volcanic hot springs.

List of Taxonomic Demarcation Criteria

Family Demarcation Criteria

Myoviridae, Siphoviridae, and Podoviridae are differentiated by tail structure. Podoviridae are also distinguished from the other families by a simple assembly pathway.

Genus Demarcation Criteria

Genera are differentiated by genome organization (presence or absence of cos and pac sites, terminal redundancies and circular permutations, terminal proteins), and presence or absence of concatemers, unusual bases, and genes for DNA or RNA polymerases.

Species Demarcation Criteria

Species are differentiated by dimensions and fine structure, DNA homology, host range, serological relationships, and virulent or temperate nature.

Similarities with Other Taxa

Tailed bacterial viruses resemble Tectiviridae by the presence of a tail-type of structure for DNA injection, but differ from them by the permanent nature of their tails. Tailed viruses resemble Herpesviridae in morphogenesis (use of scaffolding proteins, packaging of DNA into preformed shells, maturation of procapsids by proteolytic cleavage and capsid expansion) and flow of replication. In addition, temperate tailed phages and Herpesviridae are able to establish latent infections.

Derivation of Names

Caudo: from Latin cauda, “tail”.

Myo: from Greek my, myos, “muscle”, referring to the contractile tail.

Sipho: from Greek siphon, “tube”, referring to the long tail.

Podo: from Greek pous, podos, “foot”, referring to the short tail.