Download Bacteriophages of Soft Rot Enterobacteriaceae

FEMS Microbiology Letters, 363, 2016, fnv230
doi: 10.1093/femsle/fnv230
Advance Access Publication Date: 1 December 2015
Minireview
M I N I R E V I E W – Virology
Bacteriophages of Soft Rot Enterobacteriaceae—
a minireview
Robert Czajkowski∗
Laboratory of Plant Protection and Biotechnology, Department of Biotechnology, Intercollegiate Faculty of
Biotechnology, University of Gdansk and Medical University of Gdansk, Kladki 24, 80-822 Gdansk, Poland
∗
Corresponding author: Department of Biotechnology, Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk,
Kladki 24, 80-822 Gdansk, Poland. Tel: +48-58-5236426; Fax: +48-58-5236360; E-mail: [email protected]
One sentence summary: Lytic bacteriophages may be important for biological control of soft rot Enterobacteriaceae.
Editor: Andrew Millard
ABSTRACT
Soft rot Enterobacteriaceae (Pectobacterium spp. and Dickeya spp., formerly pectinolytic Erwinia spp.) are ubiquitous
necrotrophic bacterial pathogens that infect a large number of different plant species worldwide, including economically
important crops. Despite the fact that these bacteria have been studied for more than 50 years, little is known of their
corresponding predators: bacteriophages, both lytic and lysogenic. The aim of this minireview is to critically summarize
recent ecological, biological and molecular research on bacteriophages infecting Pectobacterium spp. and Dickeya spp. with
the main focus on current and future perspectives in that field.
Keywords: Erwinia; Pectobacterium; Dickeya; viruses; lytic cycle; lysogeny
INTRODUCTION
Bacteriophages (phages) are viruses that infect bacterial cells of
a narrow range of bacterial species. They were described for the
first time at the beginning of the 20th century by Frederick W.
Twort, in 1915 in England, and Felix d’Herelle, in France in 1917
(Hadley 1928; Abedon 2008). Bacteriophages are known to be extremely abundant in the biosphere; they are present everywhere
where host bacteria persist. Their population in a given environments may be as high as 108 –109 phage particles per milliliter of
water or gram of soil (Seeley and Primrose 1982; Havelaar 1987;
Marsh and Wellington 1994).
Bacteriophages consist of single- or double-stranded, linear
or circular DNA or RNA molecules bundled inside protein or
lipoprotein coats named capsids. Some bacteriophages may also
possess certain structures that facilitate their interaction with
bacterial hosts or serve to inject genetic material into host cells
(Bradley 1965). Up till now, ca. 6000 different individual bacteriophages have been described and visualized by transmission
electron microscopy (TEM) (Ackermann 2007, 2011), of which
about 2000 (ca. 30%) target members of the Enterobacteriaceae. In
contrast, the number of characterized bacteriophages infecting
the soft rot Enterobacteriaceae (SRE) bacteria (Pectobacterium spp.
and Dickeya spp.) is much fewer at less than 20. SRE are among
the top 10 most important bacterial plant pathogens in agriculture (Mansfield et al. 2012). They cause diseases, along with concomitant yield losses, of various economically important crops
such as potato, tomato, carrot, onion, pineapple, maize, rice, hyacinth, chrysanthemum and calla lily (Perombelon and Kelman
1980; Toth et al. 2011). SRE bacteria occur in a wide variety of
ecological niches ranging from bulk and rhizosphere soils, rain
water and sewage to different underground and aboveground
tissues of host and non-host plants (Perombelon 1991). They
also occur externally and internally in insects (Nadarasah and
Stavrinides 2011). Consequently, SRE bacteriophages, as natural
predators of these bacteria, are equally widespread and can be
readily isolated from these sources and habitats.
Received: 4 November 2015; Accepted: 27 November 2015
C FEMS 2015. All rights reserved. For permissions, please e-mail: [email protected]
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FEMS Microbiology Letters, 2016, Vol. 363, No. 2
Historically, SRE bacteriophages isolated from various
sources were occasionally used in phage typing assays for
tracing the presence of host bacteria in epidemiological studies, especially to characterize unnamed environmental SRE
isolates (Gross et al. 1991; Toth et al. 1999). For this purpose, a
defined number of phage isolates were tested against a panel
of unknown SRE strains to determine whether the phages form
plaques on bacterial lawns in vitro. It was assumed that bacterial
strains that were susceptible to the same bacteriophages were
more related to each other than the strains that were resistant
or more prone to be infected by different phages, hence could be
identified (Anderson and Williams 1956). However, phage typing
is seldom used nowadays due to its low resolution, tendency
for false positive and false negative results, and the development of new and better SRE detection methods (Czajkowski
et al. 2015a,b).
Currently, the diversity and ecology of mainly lytic but also
temperate SRE bacteriophages are of specific scientific interest
because of their therapeutic potential and role in host evolution
and fitness. In this review, special attention is given to recent
literature concerning specific SRE bacteriophages, all with
double-stranded DNA, which are the usual types isolated from
SRE habitats and thus most frequently studied. The final part of
the review includes a future perspective on the field.
CLASSIFICATION OF SRE BACTERIOPHAGES
Bacteriophages are classified on the basis of their morphology
(tail type, polyhedral, filamentous or pleomorphic capsid) and
their nucleic acid composition (dsDNA, ssDNA, dsRNA or ssRNA)
(Ackermann 2011). The order Caudovirales, containing more than
97% of all described bacteriophages known to infect bacteria, includes tailed forms with icosahedral heads and double-stranded
DNA genomes of variable size in the range of ca. 18 000 to 500 000
nucleotides. There are at least 350 distinct phages recognized
in the Caudovirales order to date (Ackermann 1998; Fokine and
Rossmann 2014). More than 99% of all SRE bacteriophages described also belong to the order Caudovirales, and occur in three
families: Podoviridae, Siphoviridae and Myoviridae. The families
within Caudovirales are largely distinguished on the basis of tail
morphology.
All known bacteriophages may be also characterized by their
host range. The range is defined as a collection of hosts belonging to different genera and species which a specific bacteriophage can infect and kill (Hyman et al. 2010). It is not
agreed on however, what the narrow and/or broad host range
means. It is generally accepted that a bacteriophage has a
broad host range if it is able to infect at least two or three
distinct bacterial species and a narrow host range if it can infect only certain strains within one bacterial species (Hyman
et al. 2010).
INITIAL SRE BACTERIOPHAGE ISOLATIONS
Although the existence of SRE bacteriophages has been known
for more than 50 years, only recently has a more wide-ranging
appreciation been gained of their ecology, host interaction, genomic diversity and evolution. Recent advances can be attributed to the development of whole-genome sequencing technologies but is also due to the perception that phage therapy can
contribute to the societal-driven need to find alternative strategies for controlling bacterial infections in humans, animals and
plants.
One of the first SRE bacteriophages to be studied was the
generalized transducing phage EC2 in Dickeya dadantii strain
3937 (formerly Erwinia chrysanthemi strain 3937) described in
1984, to be used in molecular biological studies of the host
bacterium (Resibois et al. 1984). At that time, not much effort was put into isolating new lytic or lysogenic bacteriophages for biological control. The EC2 phage has been a useful tool for generating mutations at defined loci in D. dadantii and D. solani genomes (Potrykus et al. 2014). Although EC2
has been used extensively worldwide, little is known about
its ecological, genomic and morphological features and to our
knowledge it has not been further characterized or its genome
sequenced.
Proof-of-concept experiments to test therapeutic phage applications were successfully performed with lytic bacteriophages against Pectobacterium carotovorum subsp. carotovorum
(Eayre, Bartz and Concelmo 1995), for prevention of potato tuber
decay caused by P. atrosepticum (Balogh et al. 2010), and control of
P. carotovorum subsp. carotovorum infections in calla lily (Ravensdale et al. 2007). Interestingly, Soleimani-Delfan et al. (2015) have
recently isolated lytic bacteriophages against D. dadantii from
the Caspian Sea, a place where one would not expect pectinolytic bacteria to be present (Soleimani-Delfan et al. 2015). Each
of these studies showed that lytic bacteriophages could be readily isolated from different sources including freshwater (Eayre,
Bartz and Concelmo 1995) and both bulk and rhizosphere soil
(Czajkowski et al. 2014).
GENOMICS OF SRE BACTERIOPHAGES
Of all bacteriophage genomes available in international
databases, less than 6% are of phages infecting plant-pathogenic
bacteria and the total number of genomes of SRE-infecting bacteriophages is less than 20 (EMBL-EBI Genomes Pages –Phage,
http://www.ebi.ac.uk/genomes/phage.html). The first complete
genomes of lytic bacteriophages infecting species of the SRE
bacteria, D. solani (Adriaenssens et al. 2012a,b) and P. carotovorum subsp. carotovorum (Lee et al. 2012a,b), were published
as recently as 2012. However, since 2012 there has been a
rapid increase in the availability of the SRE phage genomes
and 13 genomes are currently (October 2015) published in
the NCBI Genbank database. The majority of these are draft
sequences, although several are complete and annotated. A
common feature they share is the genome organization but
they also all contain a large number of open reading frames
encoding hypothetical (or conserved hypothetical) protein
genes for which no homology can be found in sequence
databases. Lack of similarity to any known sequences is a
major obstacle in bacteriophage research (van den Bossche et al.
2014).
BACTERIOPHAGES OF DICKEYA SPP.
Up till now, only four lytic bacteriophages restricted to Dickeya spp. namely, phages LIMEstone1 and LIMEstone2 of D.
solani (Adriaenssens et al. 2012a,b) and phages D3 and D5
of several Dickeya spp. (Czajkowski, Ozymko and Lojkowska
2014; Czajkowski et al. 2014), have been described in the literature, together with two broad host range lytic bacteriophages (PD10.3 and PD23.1) infecting not only members of
D. solani but also P. wasabiae and P. carotovorum subsp. carotovorum (Czajkowski et al. 2015a,b). All these bacteriophages
are morphologically and genomically related to each other
(Table 1).
Myoviridae/Caudovirales
Myoviridae/Caudovirales
Myoviridae/Caudovirales
Myoviridae/Caudovirales
Myoviridae/Caudovirales
Myoviridae/Caudovirales
Podoviridae/Caudovirales
Siphoviridae/Caudovirales
Myoviridae/Caudovirales
Myoviridae/Caudovirales
Myoviridae/Caudovirales
Podoviridae/Caudovirales
Nd.
EC2
LIMEstone1
LIMEstone2
D3
D5
PD10.3
PD23.1
PP1
My1
PM1
PM2
ZF40
Peat1
phiTE
Host
Nd.
Pba
Pba
Pcc
Pcc, Pcb,
Head diameter: 55 nm
Tail length: 90 nm
Head diameter: 90 nm
Tail length: 86 nm, head
diameter: 58 nm
Nd.
Pcc
Pcc
Tail length: 120 nm
Head diameter: 60 nm
Nd.
Pcc
Pcc, Pwa, D. solani
Head diameter: 85 nm
Tail length: 121 nm
Head diameter: 86 nm
Tail length: very short
(unmeasurable)
Pcc, Pwa, D. solani
D. solani, D. dianthicola,
D. zeae, D. dadantii, D.
chrysanthemi
Head diameter: 100 nm
Tail length: 117 nm
Head diameter: 100 nm
Tail length: 140 nm
D. solani, D. dianthicola,
D. zeae, D. dadantii, D.
chrysanthemi
D. solani
Head diameter: 91 nm
Tail length: 114 nm
Head diameter: 91 nm
Tail length: 130 nm
D. solani
D. dadantii, D. solani
Tail length: 114 nm
Nd.
Morphology
Nd. – not determined.
Pcc – Pectobacterium carotovorum subsp. carotovorum.
Pcb - Pectobacterium carotovorum subsp. brasiliense.
Pwa – Pectobacterium wasabiae.
Pba – Pectobacterium atrosepticum.
Family/order
Nd.
Phage
Lytic/temperate
Temperate
Lytic
Temperate
Lytic
Lytic
Lytic
Lytic
Lytic
Lytic
Lytic
Lytic
Lytic/temperate
Lytic/temperate
Temperate
Source
The United
Kingdom
Canada
Ukraine
Chinese
cabbage soil,
South Korea
Soil, South
Korea
Chinese
cabbage soil,
South Korea
Chinese
cabbage soil,
South Korea
Potato tuber,
Poland
Potato stem,
Poland
Arable soil,
Poland
Garden soil,
Poland
Soil sample,
Belgium
Soil sample,
Belgium
D. dadantii host
142 349
45 633
48 454
170 286
55 098
122 024
44 400
188 540
192 291
155 346
152 308
Nd.
152 427
62 000
Genome size
(bp.)
242 ORFs
61 ORFs
68 ORFs
291 ORFs
63 ORFs
149 ORFs
48 ORFs
223 ORFs
226 ORFs
196 ORFs
191 ORFs
Nd.
201 ORFs
Nd.
Number of
ORFs
Table 1. Overview of the morphological and genomic features of bacteriophages infecting SRE (Pectobacterium spp. and Dickeya spp.) bacteria.
50.1%
48.9%
50.2%
34.8%
44.9%
40.61%
49.74%
49.25%
48.6%
49.7%
49.3%
Nd.
49.2%
Nd.
%GC
2 tRNAs (tRNA-Cys,
tRNA-Tyr)
No tRNAs
No tRNAs
12 tRNAs
1 tRNA (tRNA-Cys)
20 tRNAs
No tRNAs
2 tRNAs (tRNA-Met,
tRNA-Glu)
2 tRNAs (tRNA-Met,
tRNA-Glu)
1 tRNA (tRNA-Met)
1 tRNA (tRNA-Met)
Nd.
1 tRNA (tRNA-Met)
Nd.
tRNAs
JQ015307
KR604693
JQ177065
KF835987
KF534715
JX195166
JQ837901
KM209274KM209320
KM209229KM209273
KJ716335
KM209228
Nd.
HE600015
Nd.
Genbank
accession
number
Korol and
Tovkach (2012)
Kalischuk et al.
(2015)
Salmond et al.
(unpublished)
Lim et al. (2015)
Lee et al.
(2012a,b)
Lim et al. (2014)
Lee et al.
(2012a,b)
Czajkowski
et al. (2015a,b)
Czajkowski
et al. (2015a,b)
Czajkowski
et al. (2014)
Adriaenssens
et al. (2012a,b)
Resibois et al.
(1984)
Adriaenssens
et al. (2012a,b)
Reference
Czajkowski
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FEMS Microbiology Letters, 2016, Vol. 363, No. 2
LIMEstone1 and LIMEstone2 bacteriophages
Bacteriophages PD10.3 and PD23.1
LIMEstone 1 and LIMEstone 2 were the first lytic bacteriophages of D. solani to be described (Adriaenssens et al. 2012a,b).
They belong to the Caudovirales order and the Myoviridae family, demonstrating typical morphological features visualized by
TEM, such as icosahedral head and contractile tail. Both bacteriophages were restricted to D. solani isolates only and neither of them was able to infect other Dickeya or any Pectobacterium spp. The restriction fragment length patterns (RFLP) obtained by digestion of the LIMEstone 1 and LIMEstone 2 genomic DNA with Hind III restriction endonuclease showed two
closely related patterns differing in only two bands. Both phages
were tested in field trials for therapeutic potential to control
the blackleg disease of potato caused by D. solani (Adriaenssens
et al. 2012a,b). Application of LIMEstone 1 and LIMEstone2 on
potato tubers during planting successfully reduced infection
caused by D. solani up to 75% or more in comparison to phageuntreated control plants grown from D. solani infected seed
tubers.
The genome of LIMEstone 1 (Table 1) has been sequenced
and analyzed (Genbank accession number: HE600015). It demonstrates a typical T4-like genome organization and structure
(Comeau et al. 2007). What is more, the LIMEstone 1 genome
shares a relatively high homology with genomes of three other
bacteriophages of Enterobacteriaceae family members: Shigella
spp. phage phiSboM-AG3 (69.1% homology), Salmonella spp.
phage Vil (58.7% homology) and Escherichia coli phage CBA120
(59.4% homology). According to Comeau et al. (2007), there
is no straightforward explanation of this phenomenon as
these four bacteriophages have non-overlapping host ranges
(Adriaenssens et al. 2012a,b). On the basis of the LIMEstone
1 genomic and morphological features, Adriaenssens et al.
(2012a,b) proposed to establish a new genus named Viunalikevirus in the Myoviridae family. The genus would thus
far contain seven sequenced bacteriophages including LIMEstone 1. Viunalikeviruses would have icosahedral heads, contractive tails, four distinct tail spike proteins, conserved regulatory sequences and horizontally acquired tRNAs (Adriaenssens
et al. 2012a,b).
Recently, the isolation and characterization of broad host range
lytic bacteriophages infecting three dominant SRE species in
potato, namely D. solani, P. wasabiae and P. carotovorum subsp.
carotovorum, was reported (Czajkowski et al. 2015a,b). Despite
their similarity to LIMEstone 1, D3 and D5 phages in morphology, genome size and number of shared genes, the lytic phages
PD10.3 and PD23.1 differed from them in several ways. They
have smaller capsids than D3 and D5 but their genomes are
larger and their total number of ORFs is greater than those of
known SRE Viunalikevirus bacteriophages. They also have an additional tRNA gene (tRNA-Glu), which is absent from the D3
and D5 genomes (Table 1). Moreover, they also have a broader
host range (Czajkowski et al. 2015a,b). This later feature is of
particular interest because it possibly makes them more suitable as biological control agents, especially in complex environments where more than one SRE pathogen can be expected to
be present (Pérombelon 2002).
Bacteriophages D3 and D5
Czajkowski, Ozymko and Lojkowska (2014) isolated and described nine lytic bacteriophages that infected various members of Dickeya species. These bacteriophages also belonged to
the Myoviridae family in the Caudovirales order and all expressed
similar capsid morphologies. They were, however, isolated from
different locations in Poland and differed in their host range
against isolates of Dickeya spp. Their genomes demonstrated two
separate RFLP patterns upon digestion with Csp6I restriction endonuclease. Two of the bacteriophages (D3 and D5) had broad
host ranges infecting isolates of D. solani, D. dianthicola, D. dadantii
and D. zeae but not isolates belonging to other Pectobacterium spp.
The genomes of D3 and D5 were sequenced and annotated
(GenBank accession numbers: KM209228 and KJ716335, respectively). They both share the LIMEstone 1 genome organization
(Czajkowski et al. 2014) and based on their morphological and
genomic features could provisionally be classified as members
of the Viunalikevirus genus. In experiments to test their therapeutic potential, these bacteriophages efficiently decreased D.
solani populations in vitro and on potato tuber surfaces, indicating that they may be good biological control agents for
field use.
BACTERIOPHAGES OF PECTOBACTERIUM SPP.
Only seven bacteriophages against different Pectobacterium spp.
have been described thus far. They are My1 (Lee et al. 2012a,b),
PM1 (Lim et al. 2014), PM2 (Lim, Lee and Heu 2015), PP1 (Lee et al.
2012a,b; Lim et al. 2013), ZF40 (Korol and Tovkach 2012), Peat1
(Kalischuk, Hachey and Kawchuk 2015) and phiTe (Salmond et al.
unpublished) (Table 1). Only for four of them, PM1, PM2, PP1 and
ZF40, is there more information available than their annotated
genome sequences.
Bacteriophage PP1
The PP1 bacteriophage was sequenced in 2012 and used against
P. carotovorum subsp. carotovorum as a biological control agent a
year later (Lee et al. 2012a,b; Lim et al. 2013). The authors claimed
that it was the first sequenced bacteriophage of P. carotovorum
subsp. carotovorum. This is also the first and so far the only described Pectobacterium spp. bacteriophage which belongs to the
Podoviridae family. Its genome contains typical bacteriophagerelated genes but only one gene codes for the tail fiber protein which plays an important role in host recognition. The PP1
genome does not contain genes related to a lysogenic life cycle which is an advantage for biological control applications as
the phage cannot transfer pathogenicity-related genes from one
host to another. The stability of this bacteriophage was analyzed
at various pH values and temperatures indicating that PP1 can
be efficiently applied at pH 4–11 and at temperatures ranging
from 20◦ C to 40◦ C. In proof-of-concept biological control experiments, the PP1 exhibited protection against P. carotovorum subsp.
carotovorum on lettuce (Lim et al. 2013).
Bacteriophages PM1 and PM2
Both PM1 and PM2 bacteriophages were isolated and described
in 2014 by the same research group and both are lytic bacteriophages of P. carotovorum subsp. carotovorum (Lim et al. 2014,
2015). Taxonomically PM1 and PM1 are members of the Myoviridae family and were isolated from soil samples collected in a
Chinese cabbage field in Pyeongchang, South Korea following
enrichment in host bacterial cultures. Their genomes were sequenced and are deposited at NCBI (Table 1). The host range
of PM1 is not known but PM2 is lytic to P. carotovorum subsp.
carotovorum and P. carotovorum subsp. brasiliense strains and it is
Czajkowski
unable to infect P. wasabiae, P. carotovorum subsp. odoriferum, P.
betavasculorum and P. atrosepticum.
Bacteriophage ZF40, phiTe, My1 and Peat1
The information available in the literature regarding ZF40, phiTe,
My1 and Peat1 bacteriophages that infect Pectobacterium spp. is
incomplete. Except for annotated genome sequence data, little is known about their morphology, fitness or interaction with
host bacteria. Currently, the ZF40 bacteriophage is the only described temperate phage infecting P. carotovorum subsp. carotovorum. According to the composition of its proteome, the ZF40
bacteriophage was included in the group of P2-like phages belonging to the Myoviridae family in the order Caudovirales (Panshchina et al. 2007). Particulars for the other generalized transduction bacteriophage, phiTE, although recorded in the international databases of NCBI and JGI GOLD, have never been published (Salmond et al. unpublished information) and the only
information that is available is its genome sequence (Genbank
accession number: JQ015307). My1 is the only known bacteriophage infecting Pectobacterium spp., belonging to the Siphoviridae family and apart from the genome sequence published in
2012 there is no other information available concerning its other
features. The Peat 1 bacteriophage is, to date, the first and the
only genomically characterized phage infecting P. atrosepticum.
Its genome is small and contains only 61 predicted ORFs, the
functions of most of them have not yet been determined (Kalischuk, Hachey and Kawchuk 2015).
5
plant diseases caused by SRE, although undoubtedly the pilot
studies were and are very promising.
CONCLUSIONS AND FUTURE OUTLOOK
The efficient use of bacteriophages in research and in commercial application as plant disease control agents must be
supported not only by a comprehensive understanding of the
bacteriophages themselves but also of their interaction with
their hosts and in different environments. It is clear that future research on bacteriophages in general will be largely based
on genomic and proteomic analyses. The application of whole
genome sequencing technologies and related techniques will
certainly provide insights into new phage-specific genes and
proteins of as yet unknown properties. It can be expected that
thousands of new genomes of SRE-infecting bacteriophages will
shortly become available, which in turn will extend our knowledge of the diversity of phage genetics in general and also of
SRE phages in particular. Perhaps the new information will be
helpful in identifying new SRE bacteriophages that are potential
biological control agents. In the field of phage interaction studies, techniques like genomics, proteomics and transcriptomics
will dominate in research that aims to better understand the interaction of bacteriophages with their hosts and the surrounding environment, which is crucial both for basic studies and the
practical application of these agents for the benefit of agricultural production.
ACKNOWLEDGEMENTS
CURRENT APPLICATIONS OF SRE
BACTERIOPHAGES
Several commercial bacteriophage-based products against
pathogenic bacteria in food production and infection control
programs in humans were developed and are now in use (Monk
et al. 2010). Similarly, over the years lytic bacteriophages have
been isolated and evaluated in different studies and against
different plant pathogens. For example, they have been used
to control fire blight caused by E. amylovora, bacterial blotch of
mushrooms caused by Pseudomonas tolaasii and infections in
potato caused by Streptomyces scabies and Ralstonia solanacearum
(for review, see Jones et al. 2007). According to Monk et al. (2010),
there is only one bacteriophage-based product commercially
available on the market. This product is named AgriPhage
(Omnilytics) and it has been developed against bacterial speck
(P. syringe pv. tomato) and bacterial spot (Xanthomonas pruni).
Contrary, at this time there are no commercial biological control products based on SRE bacteriophages available on the market for controlling plant diseases caused by SRE bacteria. Several
research groups have performed controlled experiments with
SRE bacteriophages and reported their effectiveness for phage
therapy in controlling Pectobacterium spp. and Dickeya spp. infections in potato plants and tubers in vitro, in greenhouses and
in field trials. The preliminary results of these initial successful
investigations, however, should be treated with caution because
most of the work was performed only as proof-of-concept experiments with single phage isolates and without large-scale field
trails. Moreover, various phages were tested in different laboratories with different experimental setups and under different
environmental conditions so that global comparisons of the data
cannot be made. It is therefore too early to draw firm conclusions
about the possible use of lytic bacteriophages for the control of
Thanks are indebted to Solke H. De Boer (Canadian Food Inspection Agency, Charlottetown, Canada), Michel C. M. Pérombelon
(ex. James Hutton Institute, Dundee, Scotland) and Magdalena
Rajewska (University of Gdansk, Poland) for their valuable comments on the manuscript and their editorial work.
FUNDING
The work was financially supported by the National Science
Centre, Poland (Narodowe Centrum Nauki, Polska) via a postdoctoral research grant [DEC-2012/04/S/NZ9/00018] to R.C.
Conflict of interest. None declared.
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