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Bacteriophage taxonomy and classification

Galina Novik*, Alena Ladutska and Dzianis Rakhuba Collection of Microorganisms, Institute of Microbiology, National Academy of Sciences of Belarus, 2 Academician

V.F.Kuprevich Street, 220141 Minsk, Republic of Belarus *Corresponding author:[email protected]

The chapter presents a retrospective survey of bacterial virus classification concepts, current state-of-the art in bacteriophage taxonomy, and overview of related problems and possible solution pathways.

Keywords: bacteriophages; phage taxonomy and classification

1. Introduction. Significance of bacteriophage systematics

Bacteriophages are one of the most numerous micro-inhabitants of Earth planet. One liter of sea water contains around 1010 of viral particles [1], one gram of marine sediments – from 107 to 109 organisms [2; 3; 4]. Oceanic bacteriophages are major species controlling development of bacterial populations and they serve as huge depots of vital macroelements, like nitrogen and phosphorus [5]. Bacterial viruses are principal natural transmitters of genetic information across World Ocean ensuring annual transduction of 1025-1028 base pairs of nucleotides [6; 7]. Taking into account ubiquitous distribution of bacteriophages in biosphere, their enormous ecological impact and expanding databank on properties of earlier described and newly isolated bacterial viruses, main objective of classification is stock-piling available knowledge on phage characteristics, its generalization and categorization. It is essential primarily for subdividing bacterial viruses into groups possessing common features which ideally should reflect evolutionary links between different bacteriophages. Within the framework of more specific tasks classification of bacteriophages is indispensable for:

• identification of new phages isolated from natural sources; • maintenance of bacteriophage collections and databases; • detection of viruses causing economic losses in biotechnological processes, aiming to enforce strict

propagation control; • identification of bacterial viruses used further for phagotyping pathogens in medical studies and as therapeutic

agents; • optimization of training programs in the area of microbiology and biotechnology; • deciphering phylogenetic relationships between individual phages.

Moreover, classification of bacteriophages is a prerequisite for development of novel trend in bacteriophage research – comparative genomics able to locate position of specific virus in general taxonomic hierarchy of microorganisms Comparative genomics methodology reveals common features of protein and RNA molecules, regulatory sequences allowing to deduce the conclusion on degree of evolutionary proximity between organisms and on the pathways of evolutionary transformations in viral population [8].

2. Historical background of bacteriophage classification

Felix d’Herelle recognized as a discoverer of bacteriophages assumed the existence of only one phage with multiple races designated as Bacteriophagum intestinale [9]. Yet, subsequent studies have revealed a whole spectrum of viruses with distinct bacterial specificity so that monophage concept was eventually rejected. In 1933, Burnet showed that enterobacterial phages represent a heterogeneous group and they may be differentiated by the following criteria: particle size defined during filtration, serological properties, host range and storage stability [10]. Later Ruska was the first to apply electron microscopy for viral taxonomic studies and, as a result, he proposed classification scheme comprising 3 morphological phage types [11]. It was followed by the concept based on the type of nucleic acid, capsid form, presence or lack of external lipid envelope and number of capsomeres [12]. This scheme abbreviated as LTH in 1965 was formally accepted by Provisional Committee on Nomenclature of Viruses (PCNV) and enlarged by inclusion of phages containing double-stranded RNA and filamentous phages. Simultaneously Bradley offered his systemizing version guided by principles of general morphology and types of nucleic acid [13]. Figure 1 shows that according to Bradley’s methodology all bacterial viruses are subdivided into 6 morphological groups: A – phages composed of capsid and long tail with contractile sheath; B – phages composed of capsid and long tail with rigid sheath;

Antimicrobial research: Novel bioknowledge and educational programs (A. Méndez-Vilas, Ed.)

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C – phages composed of capsid and short tail; D – phages represented by grand-size nucleocapsid with fibrous or spiky surface structures; E – phages incorporating one nucleocapsid; F – rod-like or filamentous phages; All phages referred to group E contain RNA. Among viruses pooled under symbol D both RNA and DNA-containing variants are found. Other types include only DNA-containing phages.

Fig. 1 Bradley’s bacteriophage classification scheme (the picture was drawn by Rakhuba Dzianis) One year later Tikhonenko proposed a similar scheme of bacteriophage classification [14]. The only distinction was that groups D and E were merged. The resulting version in Tikhonenko’s interpretation divided bacteriophages into 5 morphological types:

• filamentous phages; • phages crowned with tail analogs; • short-tailed phages; • phages with long stiff tail; • phages characterized by complex tail with contractile sheath

A decisive contribution in contemporary bacteriophage taxonomic hierarchy was made by foundation of International Committee on Taxonomy of Viruses (ICTV) in 1973 and subsequent branching of Bacterial Virus Subcommittee. It is supervising further efforts to systemize available data on properties of bacterial viruses and to reform existing classification approaches.

3. Current classification of bacteriophages

Up-to-date classification scheme encompasses 1 order, 13 families and 34 genera of bacteriophages [15]. The families are distinguished taking into account the type of nucleic acid and virion morphology. Over 40 criteria are engaged for phage differentiation into genera and species.

3.1 Tailed bacteriophages. The order Caudovirales

Tailed bacteriophages represent the most numerous and widely distributed group of bacterial viruses [16]. At least 5500 phages were investigated by electron microscopy [17]. They appear to belong to most ancient viral group [18, 19]. Phage capsid in this order is composed of protein coat and linear double-stranded DNA. Such phages have no outer envelope and they are distinguished by binary symmetry, i.e. cube symmetry for phage head and spiral-shaped symmetry for the tail. Phage head in this order forms regular or elongated eicosahedron. Capsid proteins make up capsomers hardly visible by direct electron microscopic examination. The tail is arranged as a spiral structure or composed of discs and often is


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terminated by special elements facilitating adsorption to the surface of bacterial cell – basal plate, spikes and/or fibers. DNA may incorporate atypical bases, like 5-hydromethylcytosine in coliphage T4. Genome of tailed bacteriophage usually consists of the so-called modules-interchangeable structural units. As a rule, genes responsible for similar functions are grouped into clusters [20; 21; 22]. The available data on biology of tailed bacteriophages indicate that they represent monophyletic evolutionary group since they possess resembling morphological, physical-chemical and physiological properties. This reason motivated their affiliation to a separate order – Caudovirales (lat. Cauda meaning tail). However, structure of proteins-capsid constituents differs considerably among various tailed phages. Significant distinctions are also found in DNA primary structure, host range, serological and physiological characteristics [23]. Based on tail peculiarities the order Caudovirales was differentiated into 3 families: Myoviridae – phages with a long contracting tail composed of inner hollow tube and sheath. It embraces about 1250 phages (~ 25% of all bacterial viruses) presented in Figure 2.

Fig. 2 Enterobacteria phage T4 – the most studied phage of Myoviridae family (the picture was drawn by Rakhuba Dzianis) Siphoviridae – phages with a long non-contractile tail. This family includes around 3000 phages (~ 55% of bacterial viruses) illustrated by Figure 3.


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Fig. 3 Enterobacteria phage Lambda and Enterobacteria phage T5 - the most studied phages of Siphoviridae family (the picture was drawn by Rakhuba Dzianis) Podoviridae – phages with a short rigid tail. It comprises approximately 700 phages (~ 20% of the total) drawn in Figure 4.

Fig. 4 Enterobacteria phage T7 – one of the best studied phages of Podoviridae family (the picture was drawn by Rakhuba Dzianis)


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Two latter families are closely related and reasons for isolation of short tailed phages as a separate family may be objected. This skeptical viewpoint is grounded on the arguments stating that the only distinction between 2 families is tail length determined by presence or absence of synthesis control systems. For instance, phage T7 and Salmonella phage P22 are referred to Podoviridae family because both are short-tailed. Yet, genome analysis of phage P22 has revealed its strong resemblance to bacteriophage lambda characterized by a long non-contractile tail. The similarity is striking so that recombination of two genomes yields functioning hybrids [24]. Some aspects of phage genome structure and replication cycle serve as criteria discriminating tailed bacteriophages at the genus level. Most important criteria include: presence of DNA or RNA polymerase in bacteriophage, atypical nucleotides, nucleotide sequence, cos and pac sites, production of concatemers [25]. So far 40 genera of bacteriophages comprising about 750 species classified on the basis of DNA-DNA hybridization, morphological traits, serological properties and nucleotide sequences have been identified as shown in the Table below. Table Bacteriophage genera of Caudovirales order

Myoviridae Siphoviridae PodoviridaeGenera Type species Genera Type species Genera Type species T4-like viruses

Enterobacteria phage T4

c2-like viruses

Lactococcus phage c2

PhiKMV-like viruses

Pseudomonas phage phiKMV

KVP40-like viruses

Vibrio parahaemolytius

phage KVP40

L5-like viruses

Mycobacterium phage L5

SP6-like viruses

Enterobacteria phage SP6

P2-like viruses

Enterobacteria phage P2

Lambda-like

viruses

Enterobacteria phage lambda

T7-like viruses


HP1-like viruses

Haemophilus phage HP1

N15-like viruses

Enterobacteria phage N15

AHJD-like viruses

Staphylococcus phage AHJD

SPO1-like viruses

Bacillus phage SPO1

PhiC31-like

viruses

Streptomyces phage phiC31

Phi29-like viruses

Bacillus phage phi29

Twort-like viruses

Staphylococci phage Twort

PsiM1-like

viruses

Methanobacterium phage psiM1

BPP-1-like viruses

Salmonella phage BPP-1

Bcep781-like viruses

Burkholderia cepacia phage

Bcep 781

sk1-like viruses

- Epsilon15-like viruses

Salmonella phage epsilon15

BcepMu-like viruses

Burkholderia cenocepacia

phage BcepMu

Sfi11-like viruses

- LUZ24-like

viruses Pseudomonas phage LUZ24

Felix O1-like viruses

Salmonella phage Felix O1

r1t-like viruses

Lactococcus phage r1t

N4-like viruses

Enterobacteria phage N4

HAP1-like viruses

Halomonas aquamarina

phage phiHAP1

Sfi21-like viruses

- P22-like viruses


I3-like viruses

Mycobacterium phage I3

SPbeta-like

viruses

Bacillus phage SPbeta

Phieco32-like viruses

Enterobacteria phage Phieco32

Mu-like viruses

Enterobacteria phage Mu

T1-like viruses


P1-like viruses


T5-like viruses


PB1-like viruses

Pseudomonas phage PB1

phiCD119-like viruses

Clostridium difficile phage

phiCD119

PhiH-like viruses

Halobacterium phage phiH

PhiKZ-like viruses

Pseudomonas aeruginosa phage

phiKZ


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3.2 Non-tailed phages

Among non-tailed bacteriophages only 190 have been described to date which corresponds to nearly 4% of total number of identified and classified viruses [26]. They are arranged into 10 families often represented by a single genus and species. Phages devoid of a tail are morphologically grouped into 3 types:

• Phages having polyhedral capsids – in the form of eicosahedrons or similar shape with cubic symmetry. • Filamentous phages showing spiral symmetry. • Phages with capsids of diverse shape and no visible axes of symmetry.

Many bacterial viruses in this group contain lipid envelopes or intracapsid lipid vesicles resulting in low buoyant density and sensitivity of virions to chloroform and ether.

3.3 DNA-containing bacteriophages with polyhedral capsids

Microviridae family. Virions have eicosahedral shape and size about 27 nm. Capsid consisting of 12 capsomers surrounds circular molecule of double stranded DNA. Phages – members of this family infect a relatively broad spectrum of bacteria belonging to different genera: Bdellovibrio, Chlamydia, Spiroplasma and enterobacteria. Genome sequencing data enabled to divide the family into 2 subfamilies encompassing phages showing specificity towards proteobacteria, or Chlamydia and Sphiroplasma [27]. Corticoviridae family. Currently it is represented by a single bacteriophage PM2 characterized by intracapsid lipoprotein vesicle encircling double stranded DNA molecule [28]. PM2 was the first chronologically reported bacteriophage containing lipid components. Tectiviridae family. Viral particles of this phage family are distinguished by a rigid capsid and thin lipid vesicle located inside it. When phage is adsorbed onto the surface of host cell the vesicle is transformed to generate a hollow tube used for DNA injection [29; 30]. Most popular research object in this family – bacteriophage PRD1 displays a relatively broad host specificity range, including E. coli, P. aeruginosa, S. enteric, yet, it is capable to infect only strains carrying conjugative plasmids of N, P or W type [31]. These plasmids encode bacteriophage receptor [32]. Capsid constructed from 240 molecules of protein P3 has eicosahedral configuration, and its vertexes are crowned with spikes consisting of proteins P2, P5 and P31 [33; 34; 35; 36]. Membrane vesicle surrounding double-stranded DNA molecule is within the capsid [34]. Membrane protein content constitutes approximately 50%.

3.4 RNA-containing bacteriophages with polyhedral capsids

Leviviridae family. A distinctive feature of this family is presence of mono-stranded RNA and virus specificity to coliform bacteria harbouring plasmids encoding F-pili serving as phage adsorption receptors. Viral genome comprises partly overlapping genes and viral RNA functions as m-RNA immediately after injection. 2 genera were identified in this family using serological methods. Cystoviridae family. To date only one bacteriophage was enlisted into this family but recently 8 similar viruses were isolated. They display specificity to phytopathogenic Pseudomonas syringae. Virion in the form of eicosahedron is surrounded by the envelope. The viruses are distinguished by presence of RNA-polymerase complex and 3 molecules of double stranded RNA [37; 38].

3.5 Filamentous bacteriophages

Inoviridae family. This family genetically based on mono-stranded DNA is subdivided into 2 genera. Genus Inovirus unites 29 phage species morphologically represented by long flexible or stiff filaments, and their length is determined by size of the genome [38]. The phages infect enterobacteria, bacteria of genus Thermus, clostridia and propionibacteria. Virions are sensitive to chloroform and ultrasonic treatment, they show enhanced resistance to temperature. Genus Plectrovirus consists of 15 phages capable to infect only the Mycoplasmas. Virions are short straight rods. Lipotrixviridae family. This taxonomic group comprises 6 viruses of extremely thermophilic archaebacteria. Rod-shaped capsid enclosed with lipoprotein envelope contains nucleosome-like core [39]. Type of nucleic acid – double stranded DNA. Rudiviridae family. So far 2 viruses of different length have been affiliated to this family. They form straight uncoated rods terminated by special adsorption elements. Nucleic acid type – double stranded DNA. Families Rudiviridae and Lipotrixviridae have homologous sites in their genomes, which substantiates attempts to unify them in one suprafamily [40].

3.6 Pleomorphic bacteriophages

Plasmaviridae family. Currently this family includes a sole member – MVL2 (L2) – infecting bacteria of genus Acholeplasma. The virus lacking clear-cut capsid consists of solid nucleoproteid core surrounded by membrane. Type of nucleic acid – double stranded DNA.


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Fuselloviridae family. Viruses of this family are characterized by tapered capsid ending up in short spikes. Outer envelope is made up by 2 hydrophobic proteins and lipids of host cell. Type of nucleic acid – double stranded DNA. Most thoroughly studied organism in this taxonomic group is virus SSV1 existing as prophage in Sulfolobus shibatae. To date attempts to choose suitable host for propagation of this phage have failed, yet it was found that prophage might be activated by UV or mytocin C [41].

4. Problems related to bacteriophage classification

It was stated earlier that historically bacteriophage classification was based on host spectrum, physical-chemical characteristics of virions, including capsid dimension and shape, tail presence and its structure, sensitivity to organic solvents, type of nucleic acid and genome size. Systemizing approaches ultimately resulted in a comprehensive taxonomic system regularly updated by International Committee on Taxonomy of Viruses (ICTV). A mandatory part of ICTV classification system is examination of bacteriophage virion morphology using electron microscopy technique. Yet, with steady progress of molecular-genetic classification methods a growing number of studies tends to ignore virion visualization in favor of genome sequencing. This assumption is supported by the fact that a lot of bacteriophages with a fully sequenced genome deposited at GenBank library are not classified in compliance with ICTV criteria. According to Rohwer and Edwards as the share of sequenced genomes will grow, the proportion of ICTV non-affiliated viruses will increase likewise [42]. One of the main reasons of this tendency allegedly lies in failed attempts to identify by electron microscopy numerous prophages which genomes were detected in the course of bacterial DNA sequencing. Another drawback of ICTV phage classification system is that it takes into account only vertical transfer of genetic data in the course of evolution. However, mosaic structure of bacteriophage genomes results in high frequency of horizontal gene transfer between non-homologous alleles [20; 21; 22]. Recent advances in molecular biology and genetics applied for identification of microorganisms have completely overturned existing concepts reflecting diversity of microbial kingdom and its evolutionary pathways [43; 44]. However, for several reasons application of these methods for bacteriophage identification appears problematic. Primarily it is caused by lack in bacteriophages of own rRNA used as genetic marker during identification of bacteria. Moreover, investigation of bacteriophage genome deposited at GenBank library did not reveal any gene common for all phages and potentially eligible for the role of the marker [42]. It means that so far the problem of a single genetic criterion for bacteriophage identification remains unsolved. The above mentioned mosaic peculiarity of phage genomes results from non-homologous recombination of DNA fragments in both phages. Such recombination modules are often represented by single genes or gene loci corresponding to specific protein domain. This genetic exchange is one of the driving forces of bacteriophage evolution. It appears natural therefore that molecular-genetic identification approaches successfully realized for bacteria are futile in respect to bacteriophages. To ascertain on a global scale the evolutionary progress of bacterial viruses it is essential to screen massive genetic information stockpiled by world bacteriophage population. On one hand, it seems an unrealistic objective since the estimated number of bacteriophages exceeds 1030 and the total figure of sequenced genomes so far is about 2200. On the other hand, mechanisms of horizontal gene transfer ensure ubiquitous distribution of genes across biosphere, and as a consequence, genetic diversity will be well represented in any local phage population. According to Hendrix [20] about 10% of sequences derived from new phages carry sites similar to those found in genomes of earlier sequenced phages. It may be assumed that the task of authentic evaluation reflecting the scope of genetic diversity in global viral population is not so enormous as it was originally perceived. Various researchers proposed to use identity of capsid structural proteins as phage classification character [45; 46; 47; 48]. Unfortunately, structural proteins of bacteriophages are distinguished by marked polymorphism and are devoid of conservative sites similar to 16s rRNA in prokaryotes. These shortcomings drastically reduce their attractiveness in terms of further bacteriophage identification. Rowher and Edwards [42] proposed a model called ‘Phage proteomic tree’. This method envisages analysis of phage proteome predicted from DNA sequence, using BLAST or PROTDIST software, and the result is transformed into distance matrix. Detailed consideration of genomes available in GenBank library allowed to chart a tree depicting relations between phage proteins. As an argument in favor of this system the authors state that it overcomes some contradictions of ICTV classification scheme, namely the above mentioned phage P22 is referred to Siphoviridae family. Also according to this classification, bacteriophage PRD1 earlier affiliated by ICTV to Tectiviridae family due to presence of lipid membrane in its structure is transferred into subspecies of Podoviridae family possessing similar protein complex for DNA replication. Another approach advocated by research team from Pittsbourg Institute of Bacteriophages is based on the assumption that it is impossible to establish taxonomic system with strict hierarchy for bacterial viruses owing to mosaic arrangement of their genomes [49]. Within the framework of this system higher taxons defined as ‘modules’ will be grounded on the type of phage nucleic acid – ssDNA, dsDNA, ssRNA, dsRNA. Further subdivision will be based on definite phage characteristics, like tailed and filamentous phages. Construction of this system should be guided by the following 3 principles. First, members of the taxonomic group must show affinity in cohesion mechanisms. Second,


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genome sequence is essential to enter the examined phage into a definite taxon. Third, formed divisions may have a reticulate structure, i.e. the same phage may be included into different taxons. Such approach provides more flexibility with respect to bacteriophage positioning in taxonomic system, yet complexity of the system will tend to grow with every added entry. Proux et al offered their version of taxonomic classification based on comparative genomics of phage structural proteins [50]. This system implies that genes encoding capsid proteins are most ancient and conservative. Comparative examination of DNA sequences and proteins in bacteriophages of lactic acid bacteria resulted in differentiation of 2 genera and 4 species, whereas analysis of non-structural genes allowed to group all tested phages under 1 species designation. In compliance with this method it was suggested to reclassify bacteriophages of lactic acid bacteria into 5 distinct genera. Apart from the afore-mentioned aspects concerning use of molecular genetic identification methods with regard to bacterial viruses, the problem is aggravated by the fact that application of genome sequencing for phage differentiation omits morphological parameters set by ICTV system. Such approach seems irrational because it neglects the postulate that all phenotypic manifestations in bacteriophages are a consequence of genome expression.

5. Conclusions

Summing up, the presented data provide evidence of striking contradictions between “old” and “new” systems of bacteriophage classification. ICTV taxonomic scheme is not capable to classify bacteriophages resting inside host cell in prophage state whereas molecular-genetic identification methods cannot always supply authentic information on bacteriophage affinity owing to absence of genetic marker common for all bacterial viruses.

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