THE IMPORTANCE OF ANTIMICROBIAL COMPOUNDS PRODUCED BY BENEFICIAL BACTERIA ON THE BIOCONTROL OF PHYTOPATHOGENS
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Facultad de Ciencias
ACTA BIOLÓGICA COLOMBIANA Departamento de Biología
http://www.revistas.unal.edu.co/index.php/actabiol Sede Bogotá
ARTÍCULO DE REVISIÓN / REVIEW ARTICLE MICROBIOLOGÍA
THE IMPORTANCE OF ANTIMICROBIAL COMPOUNDS
PRODUCED BY BENEFICIAL BACTERIA ON THE BIOCONTROL
OF PHYTOPATHOGENS
Importancia de compuestos antimicrobianos producidos por
bacterias benéficas en el biocontrol de fitopatógenos
Catherine CESA-LUNA1 , Antonino BAEZ1 , Verónica QUINTERO-HERNÁNDEZ2 , Joel DE LA CRUZ-ENRÍQUEZ1 , Ma Dolores
CASTAÑEDA-ANTONIO1 , Jesús MUÑOZ-ROJAS1 *
1
Grupo de Ecología y Supervivencia de Microorganismos (GESM), Laboratorio de Ecología Molecular Microbiana (LEMM), Centro
de Investigaciones en Ciencias Microbiológicas (CICM), Instituto de Ciencias (IC), Benemérita Universidad Autónoma de Puebla
(BUAP), Edificio IC11, Ciudad Universitaria, Colonia Jardines de San Manuel, Puebla, Puebla 72570, México.
2
CONACYT-GESM, LEMM, CICM, IC, BUAP, Edificio IC11, Ciudad Universitaria, Colonia Jardines de San Manuel, Puebla, Puebla
72570, México.
*For correspondence: joymerre@yahoo.com.mx
Received: 16th December 2018, Returned for revision: 08th April 2019, Accepted: 29th April 2019.
Associate Editor: Carolina Firacative.
Citation/Citar este artículo como: Cesa-Luna C, Baez A, Quintero-Hernández V, De la Cruz-Enríquez J, Castañeda-Antonio MD, Muñoz-Rojas J.
The importance of antimicrobial compounds produced by beneficial bacteria on the biocontrol of phytopathogens. Acta biol. Colomb. 2020;25(1):
140-154. DOI: http://dx.doi.org/10.15446/abc.v25n1.76867
ABSTRACT
Bacteria produce antimicrobial compounds to compete for nutrients and space in a particular habitat. Antagonistic interactions
can be evaluated by several methodologies including the double-layer agar and simultaneous inhibition assays. Among the well-
known inhibitory substances produced by bacteria are the broad-spectrum antibiotics, organic acids, siderophores, antifungal, and
bacteriocins. The most studied bacterial genera able to produce these inhibitory substances are Enterococcus, Lactococcus, Streptomyces,
Bacillus, Pseudomonas, Klebsiella, Escherichia, and Burkholderia. Some beneficial bacteria can promote plant growth and degrade toxic
compounds in the environment representing an attractive solution to diverse issues in agriculture and soil pollution, particularly
in fields with damaged soils where pesticides and fertilizers have been indiscriminately used. Beneficial bacteria may increase plant
health by inhibiting pathogenic microorganisms; some examples include Gluconacetobacter diazotrophicus, Azospirullum brasilense,
Pseudomonas fluorescens, Pseudomonas protegens, and Burkholderia tropica. However, most studies showing the antagonistic potential of
these bacteria have been performed in vitro, and just a few of them have been evaluated in association with plants. Several inhibitory
substances involved in pathogen antagonism have not been elucidated yet; in fact, we know only 1 % of the bacterial diversity in a
natural environment leading us to assume that many other inhibitory substances remain unexplored. In this review, we will describe
the characteristics of some antimicrobial compounds produced by beneficial bacteria, the principal methodologies performed to
evaluate their production, modes of action, and their importance for biotechnological purposes.
Keywords: Antagonism, antibiotic, competition, inhibition, PGPR.
RESUMEN
Las bacterias producen compuestos antimicrobianos para competir por nutrientes y espacio en un hábitat particular. Las interacciones
antagónicas pueden evaluarse mediante varias metodologías, incluido el agar de doble capa y los ensayos de inhibición simultánea. Las
sustancias inhibidoras mejor conocidas producidas por bacterias incluyen antibióticos, ácidos orgánicos, sideróforos, antifúngicos y
bacteriocinas. Entre los géneros bacterianos más estudiados que producen sustancias inhibidoras se incluyen Enterococcus, Lactococcus,
Streptomyces, Bacillus, Pseudomonas, Klebsiella, Escherichia y Burkholderia. Algunas bacterias beneficiosas tienen la capacidad de promover
el crecimiento de las plantas y degradar compuestos tóxicos en el ambiente, por lo que podrían incrementar el rendimiento de
los cultivos y disminuir problemas de contaminación del suelo, especialmente donde los pesticidas y fertilizantes han sido utilizados
140 - Acta biol. Colomb., 25(1):140-154, Enero - Abril 2020
Antimicrobial compounds of beneficial bacteria for biocontrol
indiscriminadamente. Algunas bacterias beneficiosas pueden aumentar la salud de las plantas al inhibir microorganismos patógenos,
por ejemplo, Gluconacetobacter diazotrophicus, Azospirullum brasilense, Pseudomonas fluorescens, Pseudomonas protegens y Burkholderia tropica.
Sin embargo, la mayoría de los estudios que muestran el potencial antagónico de estas bacterias se han realizado in vitro, y pocos
de ellos se han evaluado en asociación con plantas. Varias sustancias inhibitorias implicadas en el antagonismo de los patógenos
aún son desconocidas; de hecho, sabemos que solo se ha aislado el 1 % de la diversidad bacteriana en un ambiente natural, lo que
sugiere que hay muchas otras sustancias inhibitorias que no han sido exploradas. En esta revisión describimos las características de
algunos compuestos antimicrobianos producidos por bacterias beneficiosas, las principales metodologías usadas para evaluar su
producción, modos de acción y su importancia para fines biotecnológicos.
Palabras clave: Antagonismo, antibiótico, competencia, inhibición, PGPR.
INTRODUCTION of these inhibitory substances. Next, we will provide some
Microbial communities interact in different ways, either examples of diverse bacterial inhibitory substances including
synergistically or antagonistically. To survive the adversities (i) bacteriocins, (ii) siderophores and (iii) other metabolites
and coexist with other microorganisms, bacteria are such as broad-spectrum antibiotics, covering their structural
continually fighting for nutrients and niche space (Hibbing characteristics and modes of action. Finally, given the
et al., 2010). When it comes to bacterial antagonism, it is importance of the inhibitory substances for biotechnological
essential to define a producer strain as the one capable of purposes, their applications, as well as the use of beneficial
producing toxic compounds that inhibit the growth of other bacteria as bio-inoculants, will be discussed.
non-producing strains, generally sensitive to the substance
(Russel et al., 2017). Competition between bacteria can be
influenced by the production of these toxic substances and METHODS TO EVALUATE MICROBIAL ANTAGONISM
producer strains are benefited compared to non-producing Different methods can evaluate microbial inhibition, the
or sensitive strains by dominating the niche in which they most used comprise the double-layer agar and simultaneous
are located (Khare and Tavazoie, 2015). However, producer inhibition assays (Molina-Romero et al., 2017a; b). Assays
and sensitive strains interact differently when they are in a in liquid media have also been frequently reported and
structured environment than in an unstructured one (Kelsic represent a variant of simultaneous active interaction (Kreth
et al., 2015; Chacón et al., 2018). In an unstructured et al., 2008). All those methods have been used to evaluate
environment where a population of sensitive strains has the antagonism among bacterial or fungal strains, however,
been established, producers are not able to invade because to determine the antagonism against nematodes and viruses
they pay the price for toxin production (i.e., energetic other methodologies have been developed; one example
cost of plasmid carriage, production, and resistance to is the microscopic observation to evaluate the paralysis of
the molecule), decreasing their growth compared to the nematodes with inhibitory substances and diminution of
growth experienced by the sensitive strains. In a structured disease symptoms produced by virus when the plant was
environment such as the surface of an agar plate, producers inoculated with a beneficial bacteria (Wong et al., 2016; Su et
and sensitive strains grow in separate colonies and toxins al., 2017a; b) . This review only describes the most common
diffuse from the producing colony towards the sensitive methodologies used to evaluate microbial inhibition.
neighbors making resources more available to the producer
strains, due to their excessive accumulation. Therefore, Double-layer agar
producer strains numbers increase compared to the In the double-layer agar method bacteria never interact
sensitives, even if their growth rate is lower (Stubbendieck between them; however, bacteria explored as sensitive
et al., 2016). should be able to grow in the presence of metabolites
Different inhibitory substances produced by bacteria previously produced by the antagonistic strain grown on
have been reported. Some of them include broad-spectrum the first agar-layer (Mukherjee and Ghosh, 2014). The
antibiotics, organic acids, siderophores, and volatile organic double-layer agar method consists of growing a producer
compounds, antifungals, bacteriocins, among others strain on the surface of an agar-medium during 24-48 h.
(Riley, 2009; Li et al., 2013; Meena and Kanwar, 2015; After incubation time, producer colonies are removed with a
Sindhu et al., 2016). Several inhibitory substances have sterile glass slide and the remain cells are killed by exposing
not been elucidated yet; in fact, we only know 1 % of the the glass Petri dish to the vapor of chloroform during 1.5
bacterial diversity in a natural environment, leading us to h. Plates are left in a laminar flow cabinet until the residual
assume that many other inhibitory substances remain chloroform is evaporated and the second layer of soft agar
to be explored. In this review, we will begin by describing the inoculated with the indicator strain is poured over the
principal methodologies used to evaluate the production first layer of agar, where the producer strain had grown
Acta biol. Colomb., 25(1):140-154, Enero - Abril 2020 - 141
Catherine Cesa-Luna, Antonino Baez, Verónica Quintero-Hernández, Joel De La Cruz-Enríquez, Ma Dolores Castañeda-Antonio,
Jesús Muñoz-Rojas
previously. Plates are incubated at the optimal temperature It is essential to highlight that the production of an
for each microorganism analyzed. Inhibition halos formed inhibitory substance could be different in each bacterial
in the upper layer are considered indicative of antibacterial growth conditions, growth phase and the kind of culture
activity (see Fig. 1). media used for this assay (Anacarso et al., 2014). This could
be because gene expression depends on environmental
Simultaneous inhibition and nutrient-availability conditions (McArthur and Bibb,
In the simultaneous inhibition assay, both bacterial 2008). Though, some strains can produce their inhibitory
species are co-interacting all the time during the assay. For substances constitutively independently of the growth
this methodology, overnight cultures of strains explored as conditions (Muñoz-Rojas et al., 2005).
sensitive are placed over the surface of an agar plate by the
spread-plating method (Sanders, 2012; Molina-Romero et al.,
2017b), and a 20 µl-drop of the producer strain is placed on INHIBITORY SUBSTANCES PRODUCED BY BACTERIA
the middle of the agar plate. After the drop dried, Petri plates The most studied bacterial genera capable of producing
are inverted and incubated at the right temperature for the inhibitory substances are Enterococcus, Lactococcus,
microorganism analyzed. Surrounding halos of the producer Streptomyces, Bacillus, Pseudomonas, Klebsiella, Escherichia,
strain are indicative of antibacterial activity (see Fig. 2). and Burkholderia, and several articles have been published
(Khabbaz et al., 2015; Sekhar and Thomas, 2015; Tontou et
Antagonism in liquid media al., 2016; Huo et al., 2018). In this section, we will focus on
In this assay, the producer and the sensitive strains are some inhibitory substances produced by beneficial bacteria.
grown in a defined liquid media, both separately and together
in co-culture. Bacterial growth observed in the mixed culture Siderophores
is compared to the observed in the individual culture. When Iron, unlike other elementary nutritional sources such
a producer bacterium inhibits the growth of a sensitive strain, as nitrogen, phosphorus, potassium, among others, is
the bacterial number of the sensitive strain decreases sharply not freely available in host organisms and is, therefore, an
in the mixed culture. In this experiment, the bacterial number is important limiting factor for the growth of microorganisms.
determined by counting CFU/ml using a selective medium, Production of siderophores confers producing
the media selection play an essential role in the screening of microorganisms a competitive advantage over other bacteria
co-interacting strains (Muñoz-Rojas et al., 2005). in the environment, excluding them from their ecological
niche (Beneduzi et al., 2012).
Figure 1. Double-layer agar assay. In this process the producer strain is grown in the middle of a glass plate with a specific culture media (a). After
incubation of 48 h bacterial colonies are removed (b) and killed under chloroform vapors (c). Once the remaining chloroform is evaporated (d), a
double layer of soft agar (inoculated with an indicator strain) is poured (e). Once more the plates are incubated to look for an inhibition halo (f).
142 - Acta biol. Colomb.,25(1):140-154, Enero - Abril 2020Antimicrobial compounds of beneficial bacteria for biocontrol
Figure 2. Simultaneous inhibition assay. An indicator strain is massively grown on the surface of an agar plate and a drop of the producer strain
is placed in the middle of the plate. Once the drop dried, plates are incubated and the inhibition halo surrounding the producer strain is observed
as shown in the last step.
Siderophores are small molecules (< 1500 Da) produced the complex is separated via reduction of Fe(III) to Fe (II)
under iron-limited conditions and secreted to chelate (Ahmed and Holmström, 2014).
iron from the environment. By diffusion, siderophores can It has been reported that siderophore-producing bacteria
attract the ferric ion with high affinity into the cell and exert extensive biocontrol action against soil and root
also return it to the cell surface (Aguado-Santacruz et al., borne phytopathogens through the release of siderophores
2012). These molecules are mainly produced by Gram- (Sah et al., 2017), Therefore, siderophore-producing
negative bacteria, fungi, yeast and some graminaceous bacteria protect plants from phytopathogens by acting as
plants (phytosiderophores). Bacterial siderophores have competitors, reducing the iron availability necessary for
been classified into different families according to their the pathogen growth (Beneduzi et al., 2012). Siderophore-
functional group: hydroxamates, catecholates, phenolates, producing bacteria also benefit plants by supplying them
and carboxylates. Additionally, there are some groups of with iron when its availability is low in the environment,
siderophores that contain a mix of the main functional groups promoting plant-growth and improving phytoremediation
(Beneduzi et al., 2012; Ahmed and Holmström, 2014). (Chen et al., 2017). Siderophores produced by bacteria
Some bacteria produce only one class of siderophores; could be able to chelate other metals such as Cu, Cd, Ni, Zn,
however, other bacteria can secrete different types of and others (Johnstone and Nolan, 2015; Chen et al., 2017).
siderophores, making them more efficient to colonize Moreover, bacterial siderophores have shown that protect
different environments. For example, some species of the plants by triggering induced systemic resistance (ISR)
genus Pseudomonas produce hydroxamates as ferribacti- (Trapet et al., 2016). Some crops that have benefited from
ne and pseudobactin, and other species produce molecules siderophore-producing bacteria include potato, sunflower,
denominated pyoverdines of the type catechol (Pahari et sorghum, oat, cotton, peanut, pigeon pea and cucumber
al., 2017). About 270 siderophores have been structurally (Dimkpa, 2016).
characterized, and their mechanism of transport has been Several studies have reported the role of siderophores in
described, and some variations have been found betwe- biological control (Sayyed and Patel, 2011). Pseudomonas sp.
en Gram-positive and Gram-negative bacteria. For example, strain B10 was the first bacteria showing biocontrol of plant
in Gram-positive bacteria, the Fe (III)-siderophore complex pathogens. In particular, the synthesis of siderophores by
is bound to a periplasmic binding protein (that is anchored fluorescent Pseudomonas promote plant growth and inhibit
to the cell membrane) and eventually the complex is the growth of phytopathogens such as Erwinia carotovora,
transported to the cytoplasm by ATP-dependent transporter Ralstonia solanacearum, and Fusarium oxysporum. Pyoverdines,
systems. In contrast, Gram-negative bacteria carry out a mainly produced by Pseudomonas aeruginosa and Pseudomonas
more complicated process due to the presence of the outer fluorescens, have demonstrated to be adequate to control
membrane; involving TonB-dependent outer membrane Pythium and Fusarium species. Pseudomonads also produce
receptors which recognize Fe (III)-siderophore complexes pyochelin, which is thought to contribute to the protection
(Krewulak and Vogel, 2008). Once the complex binds to the of tomato plants from Pythium, as reported in Pseudomonas
outer membrane receptor at the cellular surface, it crosses aeruginosa 7NSK2 (Siddiqui, 2006).
the membrane through an energy-dependent mechanism It has been reported that some strains of Pseudomonas
carried out by membrane receptor proteins, periplasmic putida produce siderophores increasing yield and
binding proteins, and inner membrane transport proteins; biosynthesis of the major essential oil components when
then, the complex is released into the periplasmic space they are inoculated to Mentha piperita (peppermint) (Santoro
and transported across the cytoplasmic membrane, where et al., 2015).
Acta biol. Colomb., 25(1):140-154, Enero - Abril 2020 - 143Catherine Cesa-Luna, Antonino Baez, Verónica Quintero-Hernández, Joel De La Cruz-Enríquez, Ma Dolores Castañeda-Antonio,
Jesús Muñoz-Rojas
Burkholderia species are known to produce siderophores al., 2007); a bacteriocin recombinantly produced could be
that inhibit multiple phytopathogens, for example, highly concentrated in only two steps of purification but the
Paraburkholderia tropica (formerly Burkholderia tropica) characterization may turn out unsatisfactory due to difficulties
(Tenorio-Salgado et al., 2013). Other strains such as presented in the following assays, as was the case with the
Azospirullum brasilense have also shown biocontrol properties. crystallization and X-ray assays of the bacteriocin LlpA (Parret
This bacterium produces catechol type siderophores having et al., 2004). Consequently, in most of the cases, the structure
in vitro activity against the fungus Colletotrichum acutatum, one or modes of action are not described, which encourages us to
of the most critical pathogens in strawberry crop (Tortora intensify the study of these intriguing molecules.
et al., 2011). Rhizobium species also produce catecholates, Several classifications of bacteriocins have been proposed;
inhibiting the growth of fungal pathogens including in this review we show them as bacteriocins from Gram-
Fusarium oxysporum, Fusarium solani, Ustulina zonata, and Fomes positive and Gram-negative bacteria (see Fig. 3), choosing
lamonensis. Indeed, using Rhizobium strains in pea production the primary examples and mechanisms of action such as
has helped to decrease the presence of Fusarium oxysporum nisin, colicins, tailocins, pyocins, among others (Rebuffat,
in infested soils, improving crop growth (Siddiqui, 2006). 2016; Silva et al., 2018).
Rhizobactin from Rhizobium meloti is another example;
although it is not known if this siderophore participates in Gram-positive bacteriocins
biocontrol, agronomically is very interesting since it allows Bacteriocins produced by Gram-positive bacteria are
the bacteria to be more competitive in the environment generally cationic, amphiphilic, membrane permeabilizing
(Saha et al., 2016). Species of Azotobacter also produce proteins, with an approximate size ranging from < 5 to >
different siderophores including aminochelin, azotochelin, 30 kDa. Several classifications of these bacteriocins have
protochelin and azotobactin which protect crops from been proposed mainly according to their biochemical
pathogens such as Aspergillus, Alternaria, F. oxysporum, among characteristics (Kemperman et al., 2003). The mechanism
others (Baars et al., 2015). of action of Gram-positive bacteriocins is still under
investigation, but it is accepted that they disrupt membranes
Bacteriocins through electrostatic interactions or by interacting with
These molecules belong to the most abundant and anionic membrane phospholipids causing pore formation
diverse class of antimicrobial agents, constituting an (e.g. wedge-like and barrel-steve complexes), which results in
unusual microbial weapon. At first, bacteriocins were the rapid efflux of the cytoplasmic compounds. In bacteriocins
defined as ribosomally synthesized peptides directed against such as nisin and enterocin, it has been proposed that the
bacteria closely related to the producer strain (Silva et al., antimicrobial activity is due to the presence of two structural
2018), differing from traditional antibiotics precisely to their domains (one located at N-terminus and one at C-terminus)
“relatively” narrow spectrum; however, later in this review where N-terminal rings play an essential role in binding the
we will describe some examples of bacteriocins with broad- lipid II (main peptidoglycan transporter) preventing
spectrum activity showing that beyond inhibiting only related the correct synthesis of the cell wall (Gillor et al., 2009).
strains, bacteriocins may inhibit other prokaryotes and also Members of the genus Bacillus are known to produce
fungi or parasites (De la Fuente-Salcido et al., 2015). For this different bacteriocins, especially the lipopeptide type
reason, we propose to define them as antimicrobial peptides (Abriouel et al., 2011). The well-known bacteriocins
that may or may not act on strains related to the producer produced by the genus Bacillus are subtilin and coagulin.
bacterium, which may also be active against other bacterial Regarding this genus, Bacillus licheniformis ZJU12 was
genera, fungi and/or parasites. found to produce a bacteriocin-like peptide with a broad
It is believed that 99 % of all bacteria may produce at antagonistic spectrum. This peptide was able to inhibit
least one bacteriocin and the only argument why we do not the growth of some pathogenic microorganisms such as
know more bacteriocins is because they are poorly studied S. aureus, M. flavus, and some fungal phytopathogens such
(Klaenhammer, 1988). Before studying a bacteriocin per se as Fusarium oxysporum; an interesting fact is that no adverse
it is necessary to find a producer strain which is possible by effects to mice have been detected in toxicity tests, which
performing antagonism assays (Muñoz-Rojas et al., 2005), indicate a great prospect to use for biocontrol (He et al.,
and once the producer strain is found these molecules can 2006). Bacillus thuringiensis was considered as a model
be isolated and purified by diverse methodologies. We will organism for producing antimicrobial compounds. Most of
notice that the chemical nature and biosynthesis mechanisms the bacteriocins synthesized by B. thuringiensis have a broad-
of bacteriocins may vary significantly so characterize a spectrum, inhibiting phytopathogens such as Aspergillus
bacteriocin could become complicated. For example, in and P. aeruginosa, being employed mainly for the control of
many studies it is only possible to obtain a partially-purified plagues (Ugras et al., 2013; Salazar-Marroquín et al., 2016).
preparation because the activity or the concentration of In a recent study, it was reported a bacteriocin produced
the bacteriocin is lost after the purification steps (Gálvez et by an insect originated bacterium, Bacillus thuringiensis subsp.
144 - Acta biol. Colomb.,25(1):140-154, Enero - Abril 2020Antimicrobial compounds of beneficial bacteria for biocontrol
Figure 3. Bacteriocins classification. This figure shows the main examples of bacteriocins produced by Gram-positive and Gram-negative
bacteria.
kurstaki Bn1; this bacteriocin was named as thuricin Bn1 and synthesized antimicrobial peptides. Their production is
inhibits the growth of P. syringae, a plant pathogen (Ugras et through a precursor peptide, including an N-terminal leader
al., 2013). peptide and core peptides that may or may not undergo post-
translational modifications. Microcins are characterized by
Gram-negative bacteriocins showing heat, pH, and proteases tolerance, and do not
Unlike bacteriocins from Gram-positive bacteria, Gram- require a lysis process to be secreted outside; indeed, they
negative bacteriocins are more extensive and carry out are secreted through the type I ABC (ATP binding cassette)
different mechanisms of action. One of the most known and transporter secretion system. Their mechanisms of action
extensively studied bacteriocin from Gram-negative bacteria include pore-forming, DNase or RNase functions, and
is colicin, identified in E. coli (Riley and Wertz, 2002). Colicins inhibitors of protein synthesis (Yang et al., 2014; Kaur
are plasmid-encoded antimicrobial peptides secreted by E. and Kaur, 2015).
coli and other related enterobacterial strains; their molecular The genus Pseudomonas is also characterized for producing
weight varies between 20 kDa and 60 kDa and inhibit closely bacteriocins, well-known as pyocins. Pyocins target cells
related strains such as Salmonella and other strains of E. coli. through specific receptors. Based on their structure,
Production of colicins occurs mainly during times of stress pyocins are classified as R, F or S-types. R-type pyocins are
like nutrient or oxygen depletion (Kaur and Kaur, 2015). nuclease-protease resistant and it is thought that they have
Structures of colicins are organized in three different evolved from phage tails because their structure resembles
domains: the translocation domain (T) N-terminally located, non-flexible and contractile tails of bacteriophages. Their
the receptor binding (R) located in the central region, mechanism of action is through depolarization of the
and the cytotoxic domain (C) located at C-terminus, allowing cytoplasmic membrane by pore formation. F-type pyocins
to perform diverse mechanisms to kill bacterial cell (Cursino are high molecular weight protease-resistant proteins which
et al., 2002; Yang et al., 2014). Colicins target cells specifically structure is similar to R-type pyocins, except for the flexible
through cell surface receptors so they can bind the outer and non-contractile rod-like structure. S-type pyocins are
membrane proteins by interacting with Tol or Ton complex colicin-like, protease-sensitive, and their structure consists
periplasmic proteins and kill the sensitive strain, mainly in two components: the more significant component
through pore-formation, non-specific DNA degradation, executes the killing activity (DNase, tRNase or channel-
murein and lipopolysaccharide biosynthesis inhibition (by forming activities) while the smaller component, by showing
interfering with lipid carrier regeneration), and inhibition of sequence homology with colicin E2, is considered as an
protein biosynthesis (Riley, 2009; Kaur and Kaur, 2015). immunity protein. S-type pyocins cause cell death by DNA
Other examples of bacteriocins produced by Gram- breakdown (pyocin AP41, S1, S2, S3) and pore formation
negative bacteria are microcins. These molecules are (pyocin S5) (Michel-Briand and Baysse, 2002; Parret and
hydrophobic, low molecular weight, and ribosomally De Mot, 2002).
Acta biol. Colomb., 25(1):140-154, Enero - Abril 2020 - 145Catherine Cesa-Luna, Antonino Baez, Verónica Quintero-Hernández, Joel De La Cruz-Enríquez, Ma Dolores Castañeda-Antonio,
Jesús Muñoz-Rojas
Pyocins have shown a limited spectrum against other demonstrating that some of them only have activity against
Pseudomonas species, in particular, they target Burkholderia fungi, as is the case of iturines (Rojas-Solís et al., 2013);
cepacia complex strains; however, R-type pyocins have on the other hand, lipopeptides such as surfactins do have
been shown to kill a diversity of P. aeruginosa strains as activity against bacteria and fungi (Meena and Kanwar,
well as Campylobacter species, Neisseria gonorrhea, Neisseria 2015). Other antibiotics described are the polyketides (PK)
meningitides, Haemophilus ducreyi, Pseudomonas fluorescens, and which contain in their structure multiple -hydroxyketone or
Pseudomonas putida (Naz et al., 2015). Another example is -hydroxyaldehyde as functional groups. Some of them have
putadicin T01 produced by Pseudomonas putida which has a broad-spectrum antibacterial activity such as andrimid
shown a broad-spectrum against not only Gram-negative (Matilla et al., 2016) but others are only effective against
but also Gram-positive bacteria like Bacillus megaterium and fungi, for example, pyoluteorin and amphotericin B (Gomes
Enterococcus faecalis, representing another opportunity for the et al., 2013; Matilla and Krell, 2017) (see table 1).
treatment of pathogenic bacteria (Ghrairi et al., 2014). A new family of antibacterial proteins was recently
Similar phage tail-like bacteriocins have been reported, discovered, defined as lectin-like bacteriocins. These
particularly in plant-associated pseudomonad species. molecules are characterized by containing two carbohydrate-
These molecules known as “tailocins”, are large bactericidal binding domains of the monocot mannose-binding lectin
structures with contractile (myotailocins) and flexible (MMBL) family. Some lectin-like bacteriocins from P. putida,
tails (siphotailocins) (Ghequire and De Mot, 2015; Yao et P. syringae, and P. fluorescens were described: putidacin L1
al., 2017). Both carry out a mechanism similar to phage or LlpABW from P. putida; LlpAPss642 from P. syringae; and
infection: first, they reproduce the initial steps of the infection LlpA1Pf-5 from P. fluorescens. These lectin-like bacteriocins
cycle by binding a cell receptor, and then the cytoplasmic can kill several Pseudomonas species but they are not active
membrane is punctured, where massive ion release occurs. outside this genus (Parret et al., 2005). Similarly, the lectin-
Recent studies have revealed that tailocins are not like bacteriocin LlpAXcm761from Xanthomonas citri pv.
restricted to the genus Pseudomonas. For example, malvacearum LMG 761 can inhibit diverse species within the
Burkholderia cenocepacia BC0425 produces a broad-spectrum genus Xanthomonas (McCaughey et al., 2014).
tailocin (BceTMilo); it is suggested that BceTMilo binds
to a D-glucose receptor for its adsorption through the PLANT-ASSOCIATED BENEFICIAL BACTERIA
Pseudomonas aeruginosa cell surface (Yao et al., 2017). In nature, interactions between microorganisms and
plants may occur. For example, plant growth-promoting
Other inhibitory compounds produced by bacteria bacteria (PGPB) enhance plant growth through different
Bacteria also produce other metabolites such as volatile mechanisms that include: direct mechanisms such as
compounds and broad-spectrum antibiotics. Volatile biological nitrogen fixation, phytohormone production,
compounds are vital in bacterial communication processes, production of 1-Aminocyclopropane-1-carboxylate
but recent research indicates that these compounds, when deaminase (ACC), phosphate solubilization and production
secreted by bacteria, could perform antagonism over other of volatile organic compounds; and indirect mechanisms such
microorganisms (Chaurasia et al., 2005; Kai et al., 2016). as induction of systemic resistance (ISR), production of lytic
One of the volatile compounds produced by bacteria, enzymes and pathogen inhibition through the production
mainly from the genus Pseudomonas, is hydrocyanic acid of inhibitory substances (Lucy et al., 2004; Lugtenberg and
and it has been demonstrated that it participates in diverse Kamilova, 2009; Rojas-Solís et al., 2013; Molina-Romero
antibiotic activities; evidence of this is the biocontrol of et al., 2015). Other beneficial bacteria can degrade toxic
Thielaviopsis basicola (Matilla and Krell, 2017). Other volatile compounds from contaminated soil, and several strains
organic compounds (VOCs) produced by bacteria have have shown the capability to biodegrade toxic compounds
been described; however, the biological role of most of them ˇ et al., 2017). It is noteworthy that inoculation of
(Dvorák
remains to be deciphered (Tyc et al., 2017). beneficial bacteria in plants could diminish the damage
Metabolites such as broad-spectrum antibiotics may have produced by chemical fertilizers on the environment and the
antibacterial and/or antifungal properties. Some of them cost of production (Baez-Rogelio et al., 2017; Pazos-Rojas
include lipopeptides, generally produced by strains of the et al., 2018). Moreover, beneficial microorganisms allow an
genus Bacillus. These molecules have been characterized increase in the size of roots, a better nutrient absorption,
by having an amphiphilic structure, which consists of the and diminution in the lixiviation level of combined nitrogen.
binding of a hydrophilic cyclic peptide to a fatty acid chain Therefore, the addition of chemical fertilization could be
that can range from 12 to 14 carbon atoms (Meena and diminished because the plant improves the efficiency to take
Kanwar, 2015). A very interesting feature of these molecules the combined nitrogen (Dobbelaere et al., 2002a; Fuentes-
is the diversity of their structures which can influence Ramírez and Caballero-Mellado, 2005).
their antimicrobial activity. In fact, their effectiveness to Depending on the colonization site of the plant,
inhibit the growth of microorganisms has been proved, beneficial bacteria have been classified in rhizospheric,
146 - Acta biol. Colomb.,25(1):140-154, Enero - Abril 2020Antimicrobial compounds of beneficial bacteria for biocontrol
Table 1. Antibiotics produced by bacteria and their antimicrobial spectrum. Novel antibiotics with antibacterial, antifungal,
antihelmintic and antioomycete activity are included.
Antibiotic Type of molecule Activity Producer strain Reference
(Meena and Kanwar,
Surfactin Lipopeptide Antibacterial and antifungal B. subtilis, B. amyloliquefaciens
2015)
Iturin Lipopeptide Antifungal Bacillus subtilis (Rojas-Solís et al., 2013)
(Meena and Kanwar,
Fengycin Lipopeptide Antifungal B. subtilis, B. amyloliquefaciens
2015)
Streptomyces amritsarensis
Novel lipopeptide Lipopeptide Broad-spectrum antibacterial (Sharma et al., 2014)
sp. nov.
Polymixin Lipopeptide Antibacterial Bacillus polymyxa (Velkov et al., 2010)
(Meena and Kanwar,
Chromobacto mycin Lipopeptide Antifungal Chromobacterium sp.
2015)
Amphotericin B Polyketide Antifungal Streptomyces nodosus (Gomes et al., 2013)
Pyoluteorin Polyketide Antifungal, antioomycete Pseudomonas fluorescens Pf5 (Matilla and Krell, 2017)
Antibacterial, antifungal, Pseudomonas protegens sp.
2,4, diacetylphloro glucinol Polyketide (Weller et al., 2007)
antihelmintic nov.
Zwittermycin A Non-ribosomal peptide Antifungal, antioomycete Bacillus cereus UW85 (Matilla and Krell, 2017)
Serratia
Hybrid PK/Non-ribosomal
Andrimid Broad-spectrum antibacterial plymuthica (Matilla et al., 2016)
peptide
A153
endophytic, epiphytic, bacteria from rhizoplane, and others. Recently, it was described a new bacteriocin from
In the rhizosphere, region of the soil where diverse microbial Gluconacetobacter diazotrophicus, PAL5, named Gluconacin
communities live and are influenced by plant root exudates which has an antagonistic effect against phytopathogens
(Sylvia et al., 2005), bacteria are the most abundant such as X. albilineans (which produce leaf scald of sugarcane
microorganisms able to colonize and compete against the plants), and X. vasicola pv. vasculorum (causal agent of
microflora of the roots, causing a neutral, detrimental or gumming disease of sugarcane and leaf streak of corn)
beneficial effect to the plant, specifically plant growth; (Oliveira et al., 2018).
these beneficial bacteria have been termed as plant growth Although Azospirillum is not well known as a typical
promoting rhizobacteria (PGPR) (Vejan et al., 2016). biocontrol agent, some possible mechanisms to reduce
The main mechanism of the competition of PGPR is damage by pathogens have been described; for example, the
through the production of inhibitory substances (Beneduzi production of phenylacetic acid. One report also showed
the ability of A. brasilense to produce siderophores with
et al., 2012), resulting in an advantage for the elimination of
antifungal activity in vitro against Colletotrichum acutatum M11,
phytopathogens.
preventing the anthracnose caused by this fungus (Tortora
ANTAGONISM OF RHIZOBACTERIA AGAINST et al., 2011).
PHYTOPATOGENS Some plant-associated Pseudomonas inhibit several
phytopathogens such as Xanthomonas spp. (Garza-Ramos
Among the PGPR able to eliminate phytopathogens
et al., 2015) and diverse bacteriocins produced by this
are included Gluconacetobacter diazotrophicus (Muñoz-Rojas genus have been isolated and characterized. For example,
et al., 2005), Azospirullum brasilense (Méndez et al., 2014), P. syringae pv. ciccaronei NCPPB2355 produces a bacteriocin
Pseudomonas fluorescens (Laue et al., 2000), Pseudomonas protegens that inhibits P. syringae subsp. savastanoi, the causal agent of
(Ramette et al., 2011) and Burkholderia tropica (Bolívar-Anillo olive knot disease (Lavermicocca, 1999); P. fluorescens strain
et al., 2016); and some Bacillus strains are also known for BC8 produces the bacteriocin fluoricin-BC8 that inhibits P.
protecting plants from phytopathogens (Subramanian and solanacearum under in vitro conditions; Pseudomonas aeruginosa
Smith, 2015). For example, Gluconacetobacter diazotrophicus has RsB29 cause suppression of Fusarium wilt and rot of chickpea
shown in antagonism assays its ability to inhibit important (Sindhu et al., 2016); P. protegens CHA0 produces diverse
phytopathogens such as F. oxysporum, F. solani, C. fimbriata secondary metabolites that include hydrogen cyanide,
and C. falcatum possibly due to the production of pyoluteorin 2,4-diacetylphloroglucinol, pyoluteorin, and pyrrolnitrin to
(Logeshwaran et al., 2011). inhibit diverse phytopathogens such as Thievaloviopsis basicola
Acta biol. Colomb., 25(1):140-154, Enero - Abril 2020 - 147Catherine Cesa-Luna, Antonino Baez, Verónica Quintero-Hernández, Joel De La Cruz-Enríquez, Ma Dolores Castañeda-Antonio,
Jesús Muñoz-Rojas
and Pythium ultimum in tobacco and cucumber (Jousset et al., (Ramamoorthy, 2001). Many reports have shown the
2014; Sindhu et al., 2016). biocontrol potential of PGPR, but most of the assays are
Burkholderia species also inhibit essential phytopathogens. only performed in vitro, and their direct application in crops
For example, Burkholderia tropica produces siderophores has been little explored.
and volatile compounds that act as bio-controllers of Mono-inoculants have been developed for commercial
phytopathogens such as fungi and nematodes, making agriculture and are already being commercialized in several
it an excellent candidate to be used as a bio-inoculant in countries, mainly in Mexico and Argentina (Molina-Romero
crops. The ability to inhibit the growth of phytopathogenic et al., 2015). One of the most explored bacteria in crops
fungi by Burkholderia tropica was proven against Colletotrichum has been Azospirillum brasilense, which has been used in
gloeosporioides, Fusarium culmorum, Fusarium oxysporum and various crops showing successful results in more than 70 %
Sclerotium rolffsi by producing 18 volatile compounds that of cases (Dobbelaere et al., 2002b). Other bacteria used
included -pinene and limonene (Bolívar-Anillo et al., for the development of these inoculants are Rhizobium etli,
2016). Burkholderia gladioli strains have also shown inhibitory Pseudomonas fluorescens, Bradyrhizobium sp., Mesorhizobium
activity in vitro and in planta against T. ptyseos, a pink disease cicerii, Sinorhizobium meliloti, Rhizobium legumonisrum biovar trifoli
causative agent (Marín-Cevada et al., 2012). and Bradyrhizobium japonicum (Vivanco-Calixto et al., 2016).
Bacillus strains such as Bacillus thuringiensis ssp. tochigiensis The co-inoculation of microorganisms has already been
HD868 and Bacillus thuringiensis ssp. entomocidus HD9 reported and has apparently been more compelling, perhaps
(Subramanian and Smith, 2015) have been potentially because of the synergistic effect that occurs when they are in
accepted for protection against phytopathogens as co-interaction (Atieno et al., 2012; Zoppellari et al., 2014);
Aspergillus niger, Aspergillus fumigatus, Aspergillus flavus, for example, the co-inoculation of lettuce with Bacillus sp.
Cryphonectria parasitica, Fusarium oxysporum, Penicillium and Glomus intraradices (Vivas et al., 2003) and co-inoculation
digitatum, among others. B. thuringiensis NEB17 produces the of pea with Rhizobium and Bacillus megaterium (Elkoca et al.,
bacteriocin thuricin 17 (Th17) whose application in leaves 2010). Few formulations containing more than three species
soybean and corn stimulates the growth and it is the only of microorganisms in consortium have also been studied
bacteriocin studied extensively for plant growth promotion; (Molina-Romero et al., 2015), one of them is the inoculation
it also participates as a bacterial signal compound and is of sugarcane with a mixture of five diazotrophic bacteria
able to increase phytohormones production and response (Gluconacetobacter diazotrophicus, Herbaspirillum seropedicae, H.
to salt stress in Arabidopsis thaliana (Abriouel et al., 2011). rubrisubalbicans, Azospirillum amazonense, Burkholderia tropica)
B. amyloliquefaciens strain RC-2 produces a bacteriocin- (Oliveira et al., 2009). Although mono and co-inoculations
like substance able to inhibit C. dematium and other have resulted excellent for crops, all these formulations have
phytopathogens such as R. necatrix, P. oryzae, A. tumefaciens, been marketed mainly to promote plant growth and not for
and X. campestris pv. campestris (Abriouel et al., 2011). Bacillus biocontrol purposes; examples of this are Bradyrhizobium spp.
subtilis 14B reduced the percentage of infection in plants or A. brasilense inoculants which have been commercialized
caused by Agrobacterium tumefaciens and it was proposed for years to increase the yield of diverse crops (Fukami et
for biocontrol of crown gall disease in tomato plants al., 2016). For this reason, designing new formulations of
(Hammami et al., 2009). mono or multi-inoculants with beneficial bacteria capable
of eliminating phytopathogens is a challenge.
APPLICATION OF ANTAGONISTIC PGPB AS The design, formulation and optimization of a
BIO-INOCULANTS compelling mixture of bacteria to be used as inoculants is
Beneficial bacteria have shown diverse potential functions not an easy task; it requires studies of adhesion to seeds and
when used in intensive agriculture, for example, plant colonization in plants (Sundaramoorthy et al., 2012; Singh
growth. Furthermore, their ability to produce inhibitory et al., 2014; Baez-Rogelio et al., 2017). Also, antagonistic
compounds represents a potential for biological control. assays among the microbial strains of the mixture should
The strategy commonly used to kill phytopathogens is the be performed before the design and application of a multi-
use of chemical compounds such as pesticides. Nevertheless, species inoculant, because some antagonistic effects could
reducing the use of pesticides is truly important since they occur among bacteria (Molina-Romero et al., 2017b). It also
have been implied in ecological, environmental and human requires assays to guaranty the coexisting of bacterial strains
health damages (Baez-Rogelio et al., 2017). when they are in the formulation and associated with plants
Although antagonistic interactions in rhizosphere for and verify the plant growth promotion effectiveness (Muñoz-
biocontrol purposes have not been intensively studied, it Rojas et al., 2013). Several polymicrobial formations contain
has been proposed that PGPR interactions with other soil microbial strains capable of coexisting without antagonizing
microorganisms (fungal or bacteria) could be potentially each other with the capability of eliminate pathogens
used in plants of agricultural interest by developing mixed (Oliveira et al., 2009; Muñoz-Rojas et al., 2013; Baez-Rogelio
bio-inoculants or using their inhibitory substances per se et al., 2017; Molina-Romero et al., 2017b; Pérez-Santos
148 - Acta biol. Colomb.,25(1):140-154, Enero - Abril 2020Antimicrobial compounds of beneficial bacteria for biocontrol
et al., 2017a; b) and some of these formulations contain diverse kind of pathogens, is still in development. Having
desiccation-tolerant bacteria, making them more efficient them available will contribute to sustainable agriculture
in environments with low water availability (Molina-Romero by reducing the use of toxic compounds without affecting
et al., 2017b; Pérez-Santos et al., 2017a; Pazos-Rojas et al., agricultural productivity.
2018).
Some bacterial inoculants are commercially available
for promoting growth in crops and are also useful for ACKNOWLEDGEMENTS
biocontrol; however, some of them inhibit pathogens due We are grateful to CONACYT for the fellowship to Catherine
to the presence of fungicides (Crovo and Clemente, 2015) Cesa-Luna (Scholarship number: 538125/294272). The
such as metalaxyl, fludioxonil or benomyl which may cause work was supported by the following: PRODEP (CA-262),
health damages. and VIEP-BUAP-2018.
Recently, in the Laboratory of Ecology and Survival
of Microorganisms from the Center of Research in
Microbiological Sciences (Sciences Institute, University of CONFLICT OF INTEREST
Puebla, Puebla, Mexico) multispecies inoculants have been The authors declare that there is no conflict of interest.
developed, fulfilling the challenge of containing strains
capable of coexisting without antagonizing each other and
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