Bacteriophage

A bacteriophage (/bækˈtɪərioʊfeɪdʒ/), also known informally as a

phage (/ˈfeɪdʒ/), is a virus that infects and replicates within bacteria
and archaea. The term was derived from "bacteria" and the Greek
φαγεῖν (phagein), meaning "to devour". Bacteriophages are
composed of proteins that encapsulate a DNA or RNA genome, and
may have structures that are either simple or elaborate. Their genomes
may encode as few as four genes (e.g. MS2) and as many as hundreds
of genes. Phages replicate within the bacterium following the injection
of their genome into its cytoplasm.

Bacteriophages are among the most common and diverse entities in

the biosphere.[1] Bacteriophages are ubiquitous viruses, found
wherever bacteria exist. It is estimated there are more than 1031
bacteriophages on the planet, more than every other organism on
Earth, including bacteria, combined.[2] Viruses are the most abundant
biological entity in the water column of the world's oceans, and the
second largest component of biomass after prokaryotes,[3] where up
to 9x108 virions per millilitre have been found in microbial mats at the Atomic structural model of
surface,[4] and up to 70% of marine bacteria may be infected by bacteriophage T4
phages.[5]

Phages have been used since the late 20th century as an alternative to
antibiotics in the former Soviet Union and Central Europe, as well as
in France.[6][7] They are seen as a possible therapy against multi-drug-
resistant strains of many bacteria (see phage therapy).[8] On the other
hand, phages of Inoviridae have been shown to complicate biofilms
involved in pneumonia and cystic fibrosis and to shelter the bacteria
from drugs meant to eradicate disease, thus promoting persistent
infection.[9]

Contents
Classification
History
The structure of a typical myovirus
Uses bacteriophage
Phage therapy
Other
Replication
Attachment and penetration
Synthesis of proteins and nucleic acid
Virion assembly
Release of virions
Communication
Genome structure
Systems biology
In the environment
Model bacteriophages
See also
References
Bibliography Anatomy and infection cycle of
External links phage T4.

Classification
Bacteriophages occur abundantly in the biosphere, with different genomes, and lifestyles. Phages are classified
by the International Committee on Taxonomy of Viruses (ICTV) according to morphology and nucleic acid.

Bacteriophage P22, a member of the

Podoviridae by morphology due to its
short, non-contractile tail
 ICTV classification of prokaryotic (bacterial and archaeal) viruses[1]
Order Family Morphology Nucleic acid Examples
Belfryvirales Turriviridae Enveloped, isometric Linear dsDNA
Nonenveloped,
Ackermannviridae Linear dsDNA
contractile tail
Nonenveloped,
Myoviridae Linear dsDNA T4, Mu, P1, P2
contractile tail

Caudovirales Nonenveloped,
Siphoviridae noncontractile tail Linear dsDNA λ, T5, HK97, N15
(long)
Nonenveloped,
Podoviridae noncontractile tail Linear dsDNA T7, T3, Φ29, P22
(short)
Halopanivirales Sphaerolipoviridae Enveloped, isometric Linear dsDNA
Enveloped, Circular ssDNA, circular
Haloruvirales Pleolipoviridae
pleomorphic dsDNA, or linear dsDNA
Nonenveloped,
Kalamavirales Tectiviridae Linear dsDNA
isometric
Nonenveloped,
Levivirales Leviviridae Linear ssRNA MS2, Qβ
isometric
Enveloped, rod- Acidianus filamentous
Lipothrixviridae Linear dsDNA
shaped virus 1
Ligamenvirales
Nonenveloped, rod- Sulfolobus islandicus
Rudiviridae Linear dsDNA
shaped rod-shaped virus 1
Mindivirales Cystoviridae Enveloped, spherical Segmented dsRNA Φ6
Nonenveloped,
Petitvirales Microviridae Circular ssDNA ΦX174
isometric
Nonenveloped,
Tubulavirales Inoviridae Circular ssDNA M13
filamentous
Nonenveloped,
Vinavirales Corticoviridae Circular dsDNA PM2
isometric
Unassigned Enveloped, bottle-
Ampullaviridae Linear dsDNA
shaped
Nonenveloped, lemon-
Bicaudaviridae Circular dsDNA
shaped
Nonenveloped, rod-
Clavaviridae Circular dsDNA
shaped

Finnlakeviridae dsDNA FLiP[10]

Nonenveloped, lemon-
Fuselloviridae Circular dsDNA
shaped
Globuloviridae Enveloped, isometric Linear dsDNA
Guttaviridae Nonenveloped, ovoid Circular dsDNA
Enveloped,
Plasmaviridae Circular dsDNA
pleomorphic
Portogloboviridae Enveloped, isometric Circular dsDNA
Spiraviridae Nonnveloped, rod- Circular ssDNA
shaped
 Enveloped, rod-
Tristromaviridae Linear dsDNA
shaped

It has been suggested that members of Picobirnaviridae infect bacteria, but not mammals.[11]

Another proposed family is "Autolykiviridae" (dsDNA).[12]

History
In 1896, Ernest Hanbury Hankin reported that something in the waters of the
Ganges and Yamuna rivers in India had a marked antibacterial action against
cholera and it could pass through a very fine porcelain filter.[13] In 1915,
British bacteriologist Frederick Twort, superintendent of the Brown Institution
of London, discovered a small agent that infected and killed bacteria. He
believed the agent must be one of the following:

1. a stage in the life cycle of the bacteria

2. an enzyme produced by the bacteria themselves, or
3. a virus that grew on and destroyed the bacteria[14]

Twort's research was interrupted by the onset of World War I, as well as a

shortage of funding and the discoveries of antibiotics. Félix d'Herelle

Independently, French-Canadian microbiologist Félix d'Hérelle, working at

the Pasteur Institute in Paris, announced on 3 September 1917, that he had discovered "an invisible,
antagonistic microbe of the dysentery bacillus". For d’Hérelle, there was no question as to the nature of his
discovery: "In a flash I had understood: what caused my clear spots was in fact an invisible microbe… a virus
parasitic on bacteria."[15] D'Hérelle called the virus a bacteriophage, a bacteria-eater (from the Greek phagein
meaning "to devour"). He also recorded a dramatic account of a man suffering from dysentery who was
restored to good health by the bacteriophages.[16] It was D'Herelle who conducted much research into
bacteriophages and introduced the concept of phage therapy.[17]

More than a half a century later, in 1969, Max Delbrück, Alfred Hershey, and Salvador Luria were awarded
the Nobel Prize in Physiology or Medicine for their discoveries of the replication of viruses and their genetic
structure.[18]

Uses

Phage therapy

Phages were discovered to be antibacterial agents and were used in the former Soviet Republic of Georgia
(pioneered there by Giorgi Eliava with help from the co-discoverer of bacteriophages, Félix d'Herelle) during
the 1920s and 1930s for treating bacterial infections. They had widespread use, including treatment of soldiers
in the Red Army. However, they were abandoned for general use in the West for several reasons:

Antibiotics were discovered and marketed widely. They were easier to make, store, and to
prescribe.
Medical trials of phages were carried out, but a basic lack of understanding raised questions
about the validity of these trials.[19]
 Publication of research in the Soviet Union was mainly in the Russian or Georgian languages
and for many years, was not followed internationally.

The use of phages has continued since the end of the Cold War in Russia,[20] Georgia and elsewhere in
Central and Eastern Europe. The first regulated, randomized, double-blind clinical trial was reported in the
Journal of Wound Care in June 2009, which evaluated the safety and efficacy of a bacteriophage cocktail to
treat infected venous ulcers of the leg in human patients.[21] The FDA approved the study as a Phase I clinical
trial. The study's results demonstrated the safety of therapeutic application of bacteriophages, but did not show
efficacy. The authors explained that the use of certain chemicals that are part of standard wound care (e.g.
lactoferrin or silver) may have interfered with bacteriophage viability.[21] Shortly after that, another controlled
clinical trial in Western Europe (treatment of ear infections caused by Pseudomonas aeruginosa) was reported
in the journal Clinical Otolaryngology in August 2009.[22] The study concludes that bacteriophage
preparations were safe and effective for treatment of chronic ear infections in humans. Additionally, there have
been numerous animal and other experimental clinical trials evaluating the efficacy of bacteriophages for
various diseases, such as infected burns and wounds, and cystic fibrosis associated lung infections, among
others.[22]

Meanwhile, bacteriophage researchers have been developing engineered viruses to overcome antibiotic
resistance, and engineering the phage genes responsible for coding enzymes that degrade the biofilm matrix,
phage structural proteins, and the enzymes responsible for lysis of the bacterial cell wall.[4][5][6] There have
been results showing that T4 phages that are small in size and short-tailed, can be helpful in detecting E.coli in
the human body.[23]

Therapeutic efficacy of a phage cocktail was evaluated in a mice model with nasal infection of multidrug-
resistant (MDR) A. baumannii. Mice treated with the phage cocktail showed a 2.3-fold higher survival rate
than those untreated in seven days post infection.[24] In 2017 a patient with a pancreas compromised by MDR
A. baumannii was put on several antibiotics, despite this the patient's health continued to deteriorate during a
four-month period. Without effective antibiotics the patient was subjected to phage therapy using a phage
cocktail containing nine different phages that had been demonstrated to be effective against MDR A.
baumannii. Once on this therapy the patient's downward clinical trajectory reversed, and returned to health.[25]

D'Herelle "quickly learned that bacteriophages are found wherever bacteria thrive: in sewers, in rivers that
catch waste runoff from pipes, and in the stools of convalescent patients."[26] This includes rivers traditionally
thought to have healing powers, including India's Ganges River.[27]

Other

Food industry – Since 2006, the United States Food and Drug Administration (FDA) and United States
Department of Agriculture (USDA) have approved several bacteriophage products. LMP-102 (Intralytix) was
approved for treating ready-to-eat (RTE) poultry and meat products. In that same year, the FDA approved
LISTEX (developed and produced by Micreos) using bacteriophages on cheese to kill Listeria monocytogenes
bacteria, in order to give them generally recognized as safe (GRAS) status.[28] In July 2007, the same
bacteriophage were approved for use on all food products.[29] In 2011 USDA confirmed that LISTEX is a
clean label processing aid and is included in USDA.[30] Research in the field of food safety is continuing to
see if lytic phages are a viable option to control other food-borne pathogens in various food products.

Dairy industry – Bacteriophages present in the environment can cause fermentation failures of cheese starter
cultures. In order to avoid this, mixed-strain starter cultures and culture rotation regimes can be used.[31]
Diagnostics – In 2011, the FDA cleared the first bacteriophage-based product for in vitro diagnostic use.[32]
The KeyPath MRSA/MSSA Blood Culture Test uses a cocktail of bacteriophage to detect Staphylococcus
aureus in positive blood cultures and determine methicillin resistance or susceptibility. The test returns results
in about five hours, compared to two to three days for standard microbial identification and susceptibility test
methods. It was the first accelerated antibiotic-susceptibility test approved by the FDA.[33]

Counteracting bioweapons and toxins – Government agencies in the West have for several years been
looking to Georgia and the former Soviet Union for help with exploiting phages for counteracting bioweapons
and toxins, such as anthrax and botulism.[34] Developments are continuing among research groups in the U.S.
Other uses include spray application in horticulture for protecting plants and vegetable produce from decay
and the spread of bacterial disease. Other applications for bacteriophages are as biocides for environmental
surfaces, e.g., in hospitals, and as preventative treatments for catheters and medical devices before use in
clinical settings. The technology for phages to be applied to dry surfaces, e.g., uniforms, curtains, or even
sutures for surgery now exists. Clinical trials reported in Clinical Otolaryngology[22] show success in
veterinary treatment of pet dogs with otitis.

The SEPTIC bacterium sensing and identification method uses the ion emission and its dynamics during phage
infection and offers high specificity and speed for detection.[35]

Phage display is a different use of phages involving a library of phages with a variable peptide linked to a
surface protein. Each phage genome encodes the variant of the protein displayed on its surface (hence the
name), providing a link between the peptide variant and its encoding gene. Variant phages from the library
may be selected through their binding affinity to an immobilized molecule (e.g., botulism toxin) to neutralize it.
The bound, selected phages can be multiplied by reinfecting a susceptible bacterial strain, thus allowing them
to retrieve the peptides encoded in them for further study.[36]

Antimicrobial drug discovery – Phage proteins often have antimicrobial activity and may serve as leads for
peptidomimetics, i.e. drugs that mimic peptides.[37] Phage-ligand technology makes use of phage proteins for
various applications, such as binding of bacteria and bacterial components (e.g. endotoxin) and lysis of
bacteria.[38]

Basic research – Bacteriophages are important model organisms for studying principles of evolution and
ecology.[39]

Replication
Bacteriophages may have a lytic cycle or a lysogenic cycle. With lytic phages such as the T4 phage, bacterial
cells are broken open (lysed) and destroyed after immediate replication of the virion. As soon as the cell is
destroyed, the phage progeny can find new hosts to infect. Lytic phages are more suitable for phage therapy.
Some lytic phages undergo a phenomenon known as lysis inhibition, where completed phage progeny will not
immediately lyse out of the cell if extracellular phage concentrations are high. This mechanism is not identical
to that of temperate phage going dormant and usually, is temporary.

In contrast, the lysogenic cycle does not result in immediate lysing of the host cell. Those phages able to
undergo lysogeny are known as temperate phages. Their viral genome will integrate with host DNA and
replicate along with it, relatively harmlessly, or may even become established as a plasmid. The virus remains
dormant until host conditions deteriorate, perhaps due to depletion of nutrients, then, the endogenous phages
(known as prophages) become active. At this point they initiate the reproductive cycle, resulting in lysis of the
host cell. As the lysogenic cycle allows the host cell to continue to survive and reproduce, the virus is
replicated in all offspring of the cell. An example of a bacteriophage known to follow the lysogenic cycle and
the lytic cycle is the phage lambda of E. coli.[40]
Sometimes prophages may provide
benefits to the host bacterium
while they are dormant by adding
new functions to the bacterial
genome, in a phenomenon called
lysogenic conversion. Examples
are the conversion of harmless
strains of Corynebacterium
diphtheriae or Vibrio cholerae by
bacteriophages, to highly virulent
ones that cause diphtheria or
cholera, respectively.[41][42]
Strategies to combat certain
bacterial infections by targeting
these toxin-encoding prophages
have been proposed.[43]
Diagram of the DNA injection process

Attachment and
penetration

Bacterial cells are protected by a cell wall of polysaccharides, which

are important virulence factors protecting bacterial cells against both
immune host defenses and antibiotics.[44] To enter a host cell,
bacteriophages bind to specific receptors on the surface of bacteria,
including lipopolysaccharides, teichoic acids, proteins, or even
flagella. This specificity means a bacteriophage can infect only certain
bacteria bearing receptors to which they can bind, which in turn,
determines the phage's host range. Polysaccharide-degrading
enzymes, like endolysins are virion-associated proteins to
enzymatically degrade the capsular outer layer of their hosts, at the
initial step of a tightly programmed phage infection process. Host
growth conditions also influence the ability of the phage to attach and
invade them.[45] As phage virions do not move independently, they
must rely on random encounters with the correct receptors when in In this electron micrograph of
solution, such as blood, lymphatic circulation, irrigation, soil water, bacteriophages attached to a
etc. bacterial cell, the viruses are the
size and shape of coliphage T1
Myovirus bacteriophages use a hypodermic syringe-like motion to
inject their genetic material into the cell. After contacting the
appropriate receptor, the tail fibers flex to bring the base plate closer to the surface of the cell. This is known as
reversible binding. Once attached completely, irreversible binding is initiated and the tail contracts, possibly
with the help of ATP, present in the tail,[5] injecting genetic material through the bacterial membrane.[46] The
injection is accomplished through a sort of bending motion in the shaft by going to the side, contracting closer
to the cell and pushing back up. Podoviruses lack an elongated tail sheath like that of a myovirus, so instead,
they use their small, tooth-like tail fibers enzymatically to degrade a portion of the cell membrane before
inserting their genetic material.

Synthesis of proteins and nucleic acid

Within minutes, bacterial ribosomes start translating viral mRNA into protein. For RNA-based phages, RNA
replicase is synthesized early in the process. Proteins modify the bacterial RNA polymerase so it preferentially
transcribes viral mRNA. The host's normal synthesis of proteins and nucleic acids is disrupted, and it is forced
to manufacture viral products instead. These products go on to become part of new virions within the cell,
helper proteins that contribute to the assemblage of new virions, or proteins involved in cell lysis. In 1972,
Walter Fiers (University of Ghent, Belgium) was the first to establish the complete nucleotide sequence of a
gene and in 1976, of the viral genome of bacteriophage MS2.[47] Some dsDNA bacteriophages encode
ribosomal proteins, which are thought to modulate protein translation during phage infection.[48]

Virion assembly

In the case of the T4 phage, the construction of new virus particles involves the assistance of helper proteins
that act catalytically during phage morphogenesis.[49] The base plates are assembled first, with the tails being
built upon them afterward. The head capsids, constructed separately, will spontaneously assemble with the
tails. During assembly of the phage T4 virion, the morphogenetic proteins encoded by the phage genes interact
with each other in a characteristic sequence. Maintaining an appropriate balance in the amounts of each of
these proteins produced during viral infection appears to be critical for normal phage T4 morphogenesis.[50]
The DNA is packed efficiently within the heads. The whole process takes about 15 minutes.

Release of virions

Phages may be released via cell lysis, by extrusion, or, in a few cases, by budding. Lysis, by tailed phages, is
achieved by an enzyme called endolysin, which attacks and breaks down the cell wall peptidoglycan. An
altogether different phage type, the filamentous phage, make the host cell continually secrete new virus
particles. Released virions are described as free, and, unless defective, are capable of infecting a new
bacterium. Budding is associated with certain Mycoplasma phages. In contrast to virion release, phages
displaying a lysogenic cycle do not kill the host but, rather, become long-term residents as prophage.

Communication

Research in 2017 revealed that the bacteriophage Φ3T makes a short viral protein that signals other
bacteriophages to lie dormant instead of killing the host bacterium. Arbitrium is the name given to this protein
by the researchers who discovered it.[51][52]

Genome structure
Given the millions of different phages in the environment, phage genomes come in a variety of forms and
sizes. RNA phage such as MS2 have the smallest genomes, of only a few kilobases. However, some DNA
phage such as T4 may have large genomes with hundreds of genes; the size and shape of the capsid varies
along with the size of the genome.[53] The largest bacteriophage genomes reach a size of 735 kb.[54]

Bacteriophage genomes can be highly mosaic, i.e. the genome of many phage species appear to be composed
of numerous individual modules. These modules may be found in other phage species in different
arrangements. Mycobacteriophages, bacteriophages with mycobacterial hosts, have provided excellent
examples of this mosaicism. In these mycobacteriophages, genetic assortment may be the result of repeated
instances of site-specific recombination and illegitimate recombination (the result of phage genome acquisition
of bacterial host genetic sequences).[55] Evolutionary mechanisms shaping the genomes of bacterial viruses
vary between different families and depend upon the type of the nucleic acid, characteristics of the virion
structure, as well as the mode of the viral life cycle.[56]
Systems biology
The field of systems biology investigates the complex networks of interactions within an organism, usually
using computational tools and modeling.[57] For example, a phage genome that enters into a bacterial host cell
may express hundreds of phage proteins which will affect the expression of numerous host gene or the host's
metabolism. All of these complex interactions can be described and simulated in computer models.[57]

For instance, infection of Pseudomonas aeruginosa by the temperate phage PaP3 changed the expression of
38% (2160/5633) of its host's genes. Many of these effects are probably indirect, hence the challenge becomes
to identify the direct interactions among bacteria and phage.[58]

Several attempts have been made to map protein–protein interactions among phage and their host. For
instance, bacteriophage lambda was found to interact with its host, E. coli, by dozens of interactions. Again,
the significance of many of these interactions remains unclear, but these studies suggest that there most likely
are several key interactions and many indirect interactions whose role remains uncharacterized.[59]

In the environment
Metagenomics has allowed the in-water detection of bacteriophages that was not possible previously.[60]

Also, bacteriophages have been used in hydrological tracing and modelling in river systems, especially where
surface water and groundwater interactions occur. The use of phages is preferred to the more conventional dye
marker because they are significantly less absorbed when passing through ground waters and they are readily
detected at very low concentrations.[61] Non-polluted water may contain approximately 2×108 bacteriophages
per ml.[62]

Bacteriophages are thought to contribute extensively to horizontal gene transfer in natural environments,
principally via transduction, but also via transformation.[63] Metagenomics-based studies also have revealed
that viromes from a variety of environments harbor antibiotic-resistance genes, including those that could
confer multidrug resistance.[64]

Model bacteriophages
The following bacteriophages are extensively studied:

186 phage
λ phage
Φ6 phage
Φ29 phage
ΦX174
G4 phage
M13 phage
MS2 phage (23–28 nm in size)[65]
N4 phage
P1 phage
P2 phage
P4 phage
R17 phage
 T2 phage
T4 phage (169 kbp genome,[66] 200 nm long[67])
T7 phage
T12 phage

See also
Virophage, viruses that infect other viruses
Bacterivore
CrAssphage
DNA viruses
Phage ecology
Phage monographs (a comprehensive listing of phage and phage-associated monographs,
1921 – present)
Polyphage
RNA viruses
Transduction
Viriome
CRISPR
Phagemid

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External links
Häusler, T. (2006) "Viruses vs. Superbugs", Macmillan (http://www.thomashausler.com/viruses-
vs-superbugs/)
Animation of bacteriophage targeting E. coli bacteria (https://web.archive.org/web/2016030321
5841/http://www.egilsjolander.com/E_coli.mp4)
Phage.org general information on bacteriophages (https://web.archive.org/web/201306031637
53/http://www.phage.org/)
bacteriophages illustrations and genomics (http://bacteriophages.igmors.u-psud.fr/)
Bacteriophages get a foothold on their prey (http://www.ebi.ac.uk/pdbe/widgets/QuipStories/T4t
ail/T4tail.pdf)
NPR Science Friday podcast, "Using 'Phage' Viruses to Help Fight Infection", April 2008 (http
s://web.archive.org/web/20080417232145/http://www.sciencefriday.com/program/archives/200
804043)
Animation of a scientifically correct T4 bacteriophage targeting E. coli bacteria (https://www.you
tube.com/watch?v=V73nEGXUeBY)
Animation by Hybrid Animation Medical for a T4 Bacteriophage targeting E. coli bacteria (http
s://vimeo.com/8313889)
Bacteriophages: What are they. Presentation by Professor Graham Hatfull, University of
Pittsburgh (https://www.youtube.com/watch?v=3VjE1zddXWk) on YouTube

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