Download Bacteriocins from plant pathogenic bacteria

MINIREVIEW
Bacteriocins from plant pathogenic bacteria
Ingrid Holtsmark1,2, Vincent G.H. Eijsink2 & May Bente Brurberg1
1
Plant Health and Plant Protection Division, Norwegian Institute for Agricultural and Environmental Research, Høgskoleveien, Norway; and 2Institute for
Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Norway
Correspondence: May Bente Brurberg,
Plant Health and Plant Protection Division,
Norwegian Institute for Agricultural and
Environmental Research, Høgskoleveien 7,
1432 Ås, Norway. Tel.: 147 92609364;
fax: 147 64946110; e-mail:
[email protected]
Received 15 October 2007; accepted 30
October 2007.
First published online 7 December 2007.
DOI:10.1111/j.1574-6968.2007.01010.x
Editor: Richard Staples
Abstract
Many bacteria produce antimicrobial substances such as nonribosomally synthesized antibiotics and ribosomally synthesized proteinaceous compounds referred
to as bacteriocins. Secretion of antimicrobials is generally thought to contribute to
the competitiveness of the producing organism, but there are indications that these
compounds in some cases may have regulatory roles too. Bacteriocins most often
act on closely related species only and are thus of interest for application as
targeted narrow-spectrum antimicrobials with few side effects. Although the
application of bacteriocins in plant disease control is an attractive option, very
little is known about the occurrence and roles of these compounds in plant
pathogenic bacteria and their natural competitors occurring in the same biotopes.
This study presents an overview of current knowledge of bacteriocins from plant
pathogenic bacteria.
Keywords
bacteriocin; plant pathogen; peptide;
michiganin; lantibiotic.
Introduction
The rhizosphere- and plant-associated biotopes are densely
populated by numerous microbial species. The ability of a
pathogen to survive under varying and competitive conditions as well as the ability to succeed in the interaction with
its host are important elements of a plant pathogen’s
ecological fitness. In the competition for nutrients, bacteria
employ numerous strategies. One widespread strategy is the
production of antimicrobial compounds including compounds targeting closely related bacteria in the same nutritional niche. Such antimicrobial compounds are of great
interest because they affect bacterial population dynamics
and, consequently, survival and virulence (Riley & Wertz,
2002; Gardner et al., 2004). Furthermore, some antimicrobial compounds may have additional regulatory functions
(e.g. Hauge et al., 1998; Eijsink et al., 2002; Kodani et al.,
2005; Linares et al., 2006). Finally, the exploitation of
narrow-spectrum antimicrobial compounds is an attractive
strategy for the targeted combat of bacterial infections, e.g.
in plant disease control (Montesinos, 2007).
The two main categories of antimicrobials from bacteria
are the bacteriocins (ribosomally synthesized proteinaceous
substances; usually narrow spectrum) and the antibiotics
FEMS Microbiol Lett 280 (2008) 1–7
(secondary metabolites; usually broader spectrum). The
important ecological roles as well as the great application
potential of bacteriocins are well recognized in some fields
such as the food fermentation industry (Cotter et al., 2005).
While these aspects in principal are equally important in
plant pathology, very little is known about bacteriocin
production by bacterial plant pathogens and their close
relatives. In this review, we summarize current knowledge
in the field.
Bacteriocin classification
Several attempts have been made to form a useful classification scheme for bacteriocins from Gram-positive bacteria
(Klaenhammer 1993; Eijsink et al., 2002; Cotter et al., 2005;
de Jong et al., 2006; Heng & Tagg, 2006). Class I bacteriocins
are lantibiotics, i.e. peptides that contain thioether bridges
and unusual, posttranslationally modified amino acids.
Currently, lantibiotics are divided into types A (relatively
linear and flexible, cationic peptides), B (more globular,
rigid peptides with no or negative net charge) and C
(two-component bacteriocins) (Chatterjee et al., 2005). Class
I bacteriocins have a range of activities generally resulting
in membrane destabilization, pore formation and/or
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2
inhibition of cell-wall synthesis through binding to specific
lipids (Chatterjee et al., 2005; Hasper et al., 2006). Class II
bacteriocins form a large and highly diverse group of
nonmodified peptides (Eijsink et al., 2002). They affect
target cells in similar ways as class I bacteriocins, but their
receptors seem to be proteins rather than lipids (Diep et al.,
2007). Class III bacteriocins are not peptides but heat-labile
proteins that are categorized according to their ability to lyse
cells. Other classes of bacteriocins recognized in Grampositive bacteria comprise bacteriocins that carry essential
lipid or carbohydrate moieties and the cyclic peptides
(De Jong et al., 2006; Heng & Tagg, 2006).
The best-known bacteriocins produced by Gram-negative
bacteria are the colicins produced by Escherichia coli. Colicins are a family of antimicrobial proteins with narrow host
ranges, acting primarily on other strains of E. coli and its
close enteric relatives (Riley & Gordon, 1999). The colicins
show large variation, in terms of both structure and their
effects on target cells, effects that include pore-formation,
inhibition of cell-wall synthesis, DNAse activity and RNAse
activity (Braun et al., 2002). Another group of protein
bacteriocins from Gram-negative bacteria comprises proteins that affect the target cell membrane by self-assembly
into particles that resemble tails of bacteriophages
(e.g. some subclasses of the pyocins produced by Pseudomonas aeruginosa; Michel-Briand & Baysse, 2002). Generally, protein bacteriocins from both Gram-negative and
Gram-positive bacteria show large variation, as illustrated
by some of the examples described below. Many members of
the Gram-negative Enterobacteriaceae also produce antimicrobial peptides called microcins. This group of antimicrobial peptides has its own subclassification and includes
compounds with and without posttranslational modifications (Duquesne et al., 2007). Another group of peptide
bacteriocins from Gram-negative bacteria comprises the
trifolitoxins that are discussed below. It should be noted
that genome analyses indicate that Gram-negative bacteria
also may produce ‘Gram-positive-like’ peptide bacteriocins
(Dirix et al., 2004).
Bacteriocins from plant pathogenic bacteria
Most plant pathogenic bacteria are Gram-negative bacteria,
and almost all known bacteriocins produced by these
bacteria are proteins. Among bacteria residing in the soil
and the rhizosphere as well as among saprophytic bacteria,
Gram-positive species are more frequent. In such bacteria,
many peptide bacteriocins, especially from Class I (lantibiotics), have been identified and characterized.
Protein bacteriocins
Genome sequencing of the plant pathogenic Pseudomonas
syringae pv. syringae revealed the presence of S-type pyocins
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I. Holtsmark et al.
(Feil et al., 2005), which are also found in strains of the
opportunistic human pathogen Pseudomonas aeruginosa.
These are high-molecular-weight bacteriocins (65–80 kDa)
that are related to colicins. S-type pyocins are complexes of
two components: a large component with killing activity
and a smaller immunity protein (Michel-Briand & Baysse,
2002). They act mainly on other species of Pseudomonas
(Sano et al., 1993). Very recently, Pectobacterium carotovorum (previously known as Erwinia carotovora ssp. carotovora)
was shown to produce a smaller colicin- and pyocin-like
antimicrobial protein of about 55 kDa, called carocin S1.
This protein was shown to inhibit other strains of the same
species probably by exerting DNAse activity (Chuang et al.,
2007; see also Kyeremeh et al., 2000). Colicin-like proteins
are also found in the genomes of both the sequenced strains
of Xylella fastidiosa (Simpson et al., 2000; van Sluys et al.,
2003) and in Xanthomonas oryzae pv. oryzae (Ochiai et al.,
2005).
As judged by genome sequences, many plant pathogenic
bacteria appear to contain genes encoding so-called RTXtoxins, in particular haemolysins, which are usually considered virulence factors of Gram-negative bacteria (Lally et al.,
1999; van Sluys et al., 2002). Interestingly, Oresnik et al.
(1999) showed that Rhizobium leguminosarum produces such
an RTX-type toxin of about 100 kDa. More importantly,
they also showed that this protein indeed provides a competitive advantage (in terms of nodule occupancy) in the
competition with some (not all) closely related strains. Hert
et al. (2005) showed that production of (noncharacterized)
protein bacteriocins enables Xanthomonas perforans to exert
an antagonistic effect on the tomato pathogen Xanthomonas
euvesicatoria, both in the laboratory and in field trials.
Bacteriocins that exert their antimicrobial action by selfassembling into cytotoxic phage tail-like fibers have also
been observed in Gram-negative plant pathogens. One of
the best-studied cases is that of the carotovoricins produced
by Pectobacterium carotovorum. It has been shown that
carotovoricins produced by one Pectobacterium carotovorum
strain kill other Pectobacterium carotovorum strains and that
the killing spectra of these bacteriocins are determined by
the structure of the tail fibers (Nguyen et al., 2001; Yamada
et al., 2006). Phage-tail-like bacteriocins have also been
found in Ralstonia solanacearum (previously Pseudomonas
solanacearum) (Arwiyanto et al., 1993) and it has been
shown that avirulent bacteriocin producers reduce the
development of bacterial wilt on tobacco (Chen & Echandi,
1984). A phage-tail-like bacteriocin produced by Serratia
plymithicum has been found to inhibit growth of Erwinia
amylovora (Jabrane et al., 2002). Phage-tail-like bacteriocins
have also been found in Rhizobium (Lotz & Mayer, 1972). It
is conceivable that the particle-like bacteriocins found
during early work on Pseudomonas syringae by Haag &
Vidaver (1974) also belong to this type.
FEMS Microbiol Lett 280 (2008) 1–7
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Bacteriocins from plant pathogenic bacteria
There are a several examples of plant pathogens producing other protein bacteriocins that do not resemble the
‘standard’ types of antimicrobial proteins mentioned above
and/or that have not been sufficiently characterized to allow
some sort of classification. Xanthomonas campestris
pv. glycines, the causative agent of bacterial pustule on
soybean, produces a heterodimeric bacteriocin called glycinecin, which is encoded by two separate genes, glyA and
glyB, that give rise to a 39- and a 14-kDa subunit, respectively (Heu et al., 2001). The antagonistic range of this
bacteriocin has been found to mainly include other
pathovars of X. campestris, and also X. oryzae pv. oryzae,
which causes bacterial blight of rice (Heu et al., 2001).
Glycinecin shares no significant similarity with any protein
sequences known to date and acts by permeabilizing
the membranes of target cells (Pham et al., 2004). Another
case is the 30-kDa lectin-like putidacin (LlpA), produced by
a rhizosphere isolate of Pseudomonas sp. BW11M1.
This bacteriocin contains regions that resemble mannosebinding domains of lectins in monocotyledonous plants
(Parret et al., 2003). Putidacin has inhibitory activity against
strains of a number of Pseudomonas species, including
pathovars of Pseudomonas syringae. Interestingly, two
lectin-like bacteriocins with similar inhibitory spectra were
recently identified in the well-known biocontrol strain
Pseudomonas fluorescens Pf-5 (Parret et al., 2005). Finally,
Lavermicocca et al. (1999) purified a bacteriocin from
Pseudomonas syringae pv. ciccaronei, which potentially
consists of three proteins (45–76 kDa). These authors
showed that this bacteriocin effectively inhibits the causative
agent of olive knot disease, Pseudomonas syringae ssp.
savastanoi, in field trials.
Very little is known about protein bacteriocins from
Gram-positive plant pathogenic bacteria. The best-studied
case concerns ipomicin, a heat-sensitive 10-kDa protein
produced by the sweet-potato pathogen Streptomyces
ipomoea (Zhang et al., 2003). The antagonistic activity seems
limited to closely related strains, i.e. primarily other strains
of S. ipomoea. Holtsmark et al. (2007) recently showed that
the Gram-positive tomato pathogen Clavibacter michiganensis ssp. michiganensis secretes a 14-kDa protein that
inhibits growth of the closely related potato pathogen
Clavibacter michiganensis ssp. sepedonicus.
sources to control plant pathogens has recently been
reviewed by Montesinos (2007).
Trifolitoxins are peptide bacteriocins produced by Gramnegative species such as Agrobacterium tumefaciens and
R. leguminosarum. These bacteriocins consist of eleven
amino acids carrying several (partly unknown) posttranslational modifications (Scupham & Triplett, 2006). Several
studies confirm the role of these compounds in competition
with closely related species (Robleto et al., 1998; Herlache &
Triplett, 2002). These trifolitoxins are very interesting peptide bacteriocins, but more work is needed before they can
be compared with other peptide bacteriocins and classified.
Holtsmark et al. (2006) described the first example of a
plant pathogen producing a known type of peptide bacteriocin, namely a lantibiotic belonging to class I, type B. This
bacteriocin, named michiganin A, is produced by the Grampositive tomato pathogen C. michiganensis ssp. michiganensis and inhibits growth of the closely related potato pathogen
C. michiganensis ssp. sepedonicus (Holtsmark et al., 2006,
2007; Fig. 1). Michiganin A resembles other type B lantibiotics such as actagardine (Zimmermann & Jung, 1997) and
mersacidin (Prasch et al., 1997), which are produced by an
Actinoplanes sp. and a Bacillus sp., respectively. These
lantibiotics are thought to exert their antimicrobial action
through interfering with the incorporation of lipid II into
peptidoglycan (Bauer & Dicks, 2005). Michiganin A was
found to inhibit C. michiganensis ssp. sepedonicus at concentrations in the 10–100 nM range (20–200 ng mL 1),
which are typical inhibitory concentrations for peptide
bacteriocins.
Regulatory roles?
It is widely assumed that antimicrobial substances secreted
by bacteria, be it bacteriocins or antibiotics, mainly have a
role in competition. However, there are now several examples in the literature that link bacteriocins and antibiotics
to other functions, such as signalling, virulence and
1
Ser
2
3
9
Ala
S
Ser
Dhb
7
4
Peptide bacteriocins
Whereas peptide bacteriocins are abundant in nature, including bacterial microbial soil ecosystems, and despite the
fact that genome searches reveal the presence of potential
bacteriocin genes in most bacterial genomes (e.g. Dirix et al.,
2004; Nes & Johnsborg, 2004; de Jong et al., 2006), very little
is known about peptide bacteriocins produced by plant
pathogens. The potential use of bacteriocins from other
FEMS Microbiol Lett 280 (2008) 1–7
Gly
8
5
6
S
10
Leu Abu 11
Ile
12
Glu
Ala
Cys
20
16
Ala
Ile
13
Trp Leu
18
Ala 19
17
Ala
Ile
14
15
Gly Abu
21
S
Arg
Fig. 1. Primary structure of Michiganin A. Abu-S is the threoninederived moiety of a methyllanthionine ring. Ala-S is either the serinebased half of a lanthionine ring or the cysteine-derived moiety of either
type of ring. The mass of the predicted mature michiganin A molecule is
2144.6 Da (Holtsmark et al., 2006).
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4
sporulation (e.g. Kuipers et al., 1995; Hauge et al., 1998;
Whitehead et al., 2002; Kodani et al., 2005; Linares et al.,
2006). For example, the potential regulatory role of classical
antibiotics was recently discussed by Linares et al. (2006) in
a study on the regulation of virulence in Pseudomonas
aeruginosa. Several class I and class II peptide bacteriocins
produced by Gram-positive bacteria are known to have an
additional function in that they act as an auto-inducing
peptide pheromone that stimulates bacteriocin production
(Kuipers et al., 1995; Brurberg et al., 1997; Hauge et al.,
1998; Eijsink et al., 2002). This enables concerted bacteriocin
production in bacterial subpopulations of the same species,
thus increasing competitive power. Kodani et al. (2005)
showed that a lanthionine produced by Streptomyces
tendae is involved in aerial hyphae formation and has
(limited) antimicrobial activity, providing another example
of a bacteriocin-like peptide with a regulatory function.
Most interestingly from a plant pathology point of view, Lee
et al. (2006) recently showed that the avirulence gene
product AvrXa21 produced by a number of X. oryzae pv.
oryzae strains seems to be a secreted peptide dependent on a
specific type of ATP-binding cassette transporter (RaxB;
Burdman et al., 2004) that is characteristic for the production of many peptide bacteriocins and cognate regulatory
pheromones. Whether the hypothesized peptide is a peptide
pheromone or a bacteriocin, or perhaps is multifunctional,
remains to be seen. Interestingly, both sequenced strains of
X. oryzae pv. oryzae contain several candidate peptide
bacteriocins/pheromones, as do the genomes of other
Gram-negative bacteria (Dirix et al., 2004; Table 1).
I. Holtsmark et al.
Table 1. Number of genes putatively encoding peptide bacteriocins in
the genomes of plant pathogenic bacteria
Number of small
protein bacteriocins
(size 100 aa)
Agrobacterium tumefasciens C58 Cereon
Agrobacterium tumefasciens C58 UWash
Aster yellows witches broom phytoplasma AYWB
Burkholderia cenocepacia AU 1054
Burkholderia cenocepacia HI2424
Burkholderia cepacia AMMD
Clavibacter michiganensis ssp.
michiganensis NCPPB 382
Pectobacterium athrosepticum SCRI1043
Leifsonia xyli ssp. xyli CTCB0
Onion yellows phytoplasma OY-M
Pseudomonas syringae pv. phaseolicola 1448A
Pseudomonas syringae pv. syringae B728a
Pseudomonas syringae pv. tomato DC3000
Ralstonia solanacearum GMI1000
Xanthomonas campestris
pv. campestris ATCC33913
Xanthomonas campestris pv. campestris 8004
Xanthomonas campestris pv. vesicatoria 8510
Xanthomonas axonopodis pv. citri 306
Xanthomonas oryzae KACC10331
Xanthomonas oryzae MAFF311018
Xylella fastidiosa 9a5c
Xylella fastidiosa Temecula1
21
32
2
15
17
15
8w
6
5
0
15
7
7
16
5
7
10
7
5
8
17
10
Concluding remarks and future prospects
Genome mining for bacteriocins was performed using BAGEL default
settings (de Jong et al., 2006). The numbers of putative bacteriocins
reported were scored as most significant by the program. In addition, the
searches yielded a number of potential bacteriocins with lower scores
(results not given).
w
Michiganin A (Holtsmark et al., 2006) was among the predicted
bacteriocins.
All in all, very little is known about bacteriocins produced by
plant pathogens and their close relatives, and the picture
emerging from existing data is erratic. This is remarkable
considering the obvious potential that bacteriocins or
bacteriocin-producing strains have for plant disease control
and considering the fact that both genome analyses and
experimental studies (e.g. Hu & Young, 1998) indicate that
bacteriocins are also abundantly present in plant pathogens.
Until recently, detection of new bacteriocins relied on
functional assays, in which potential bacteriocin producers
were screened for the production of antimicrobial activity
against a selection of indicator organisms. Because production of bacteriocins often is under strict regulatory control,
it can be a challenging task to identify these molecules by
screening for biological activities (see Brurberg et al., 1997
for further discussion). In this respect, the increasing
number of genome sequences provides a new valuable tool
for identifying bacteriocins from plant pathogens, following
a genome-mining strategy. Finding bacteriocin genes
directly is limited by the fact that bacteriocins, in particular
small protein bacteriocins, generally show limited sequence
conservation. However, one may exploit the fact that
bacteriocin genes often are located near genes encoding
proteins that contribute to their production, such as immunity proteins, two-component regulators, and specific
transporters. This is exploited by the excellent BAGEL program, a web-based bacteriocin genome mining tool that
identifies bacteriocins using knowledge-based bacteriocin
databases and motif databases (de Jong et al., 2006;http://
bioinformatics.biol.rug.nl/websoftware/bagel/bagel_start.php).
Table 1 shows the results of BAGEL searches for small
protein bacteriocins in 22 sequenced plant pathogen
genomes. The sequenced bacterial genomes are from 10
different genera, including two Gram-positive bacteria
(C. michiganensis ssp. michiganensis and Leifsonia xyli ssp.
xyli) and two phytoplasma (aster yellows witches broom and
onion yellows phytoplasma). All but one of the genomes
(onion yellows phytoplasma) contain a number of genes
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FEMS Microbiol Lett 280 (2008) 1–7
5
Bacteriocins from plant pathogenic bacteria
putatively encoding small protein bacteriocins. In total, 235
genes were found and of these nearly 80% (185) were
annotated as hypothetical proteins in the original genome
data.
As described above and as illustrated by Table 1, the
unravelling of the occurrence and roles of bacteriocins from
plant pathogens has only just begun. The potential advantages of creating more knowledge are obvious: firstly, new
narrow-spectrum antimicrobials may emerge that can contribute to covering agriculture’s need for more sustainable
and effective strategies for plant disease control. In principle,
such compounds may also find applications in medicine,
where the antibiotic-resistance problem creates an urgent
need for replacements. If economically sensible production
or synthetic routes can be established, bacteriocins may be
applied directly in some kind of semi-pure form. Otherwise,
one may deliver bacteriocins using nonvirulent production
strains. Finally, there is the option of bacteriocin producing
transgenic crop plants.
Because the production of bacteriocins and the competition and signalling between species seem tightly connected,
it is also possible that future bacteriocin research will reveal
new regulatory processes and pathways, thus yielding new
targets for alternative approaches for plant disease control.
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