Medio ambiente y desarrollo sustentable

Artículo arbitrado

Actinomycetes as biological control agents

of phytopathogenic fungi

Los actinomicetos como agentes de control biológico

de hongos fitopatógenos

1,2

ANA CECILIA GONZÁLEZ-FRANCO Y LORETO ROBLES HERNÁNDEZ

Recibido: Febrero 23, 2009

Aceptado: Junio 3, 2009

Resumen

Abstract

Los actinomicetos son un reservorio enorme de antibióticos y

metabolitos bioactivos y muchos de ellos son excelentes agentes

de biocontrol para proteger a las plantas contra fitopatógenos.

Aunque miles de antibióticos y metabolitos bioactivos han sido

descritos, se cree que estos representan solo una fracción de

los compuestos bioactivos producidos por los actinomicetos. En

esta revisión se abordan las características generales y

propiedades de los actinomicetos como agentes de control

biológico, sus mecanismos a través de los cuales realizan el

biocontrol y el impacto de la composición química de la pared

celular de los hongos fitopatógenos en el proceso de control.

Actinomycetes are an enormous reservoir for antibiotics and

bioactive metabolites, and many are excellent biocontrol agents

for use in protecting plants against phytopathogens. Although

thousands of antibiotics and bioactive metabolites have been

described, these are thought to represent only a small fraction

of the bioactive compounds produced by actinomycetes. In

this review, we summarize the general characteristics and

properties of actinomycetes as biocontrol agents, the

mechanisms through which the biocontrol occurs, as well as

the impact of the phytopathogenic fungal cell wall composition

in the control process.

Palabras clave: Streptomyces, competencia, parasitismo,

antibiosis.

Keywords: Streptomyces, competition, parasitism, antibiosis.

Introduction

ctinomycetes are among the most widely distributed group of microorganisms in nature.

They are found abundantly in cultivated and uncultivated soils, in various regions throughout

the world (Goodfellow and Simpson, 1987; Goodfellow and Williams, 1983).

Actinomycetes, especially streptomycetes,

secondary metabolites of which some are

antibiotics that are predominant in therapeutic

and commercial importance (Alderson et al.,

1993). Over one thousand secondary

metabolites from actinomycetes were

discovered during the years 1988-1992, and

approximately 75% of these compounds were

can degrade a wide diversity recalcitrant

polymers occurring naturally in plant litter and

soil, including hemicelluloses, pectin, keratin,

and chitin (Gooday, 1990; Warren, 1996).

Actinomycetes also have the genetic capability

to synthesize several biologically active

________________________________

Profesor de la Facultad de Ciencias Agrotecnológicas, Universidad Autónoma de Chihuahua, Ciudad Universitaria S/N Campus 1,

Chihuahua, Chih., 31310, México.

Dirección electrónica del autor de correspondencia: conzalez@uach.mx

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ANA CECILIA GONZÁLEZ-FRANCO Y LORETO ROBLES HERNÁNDEZ: Actinomycetes as biological control agents of

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produced by strains of the genus

Streptomyces (Sanglier et al., 1993). The

compounds isolated during this period of time

belong to 46 chemical classes, demonstrating

the chemical diversity of the secondary

metabolites biosynthesized by actinomycetes.

Some examples of bioactive compounds

include anti-viral and anti-cancer compounds,

modulators of immune responses, various

enzyme inhibitors, as well as herbicides,

insecticides, anti-fungal, and anti-helmintic

compounds (Sanglier et al., 1993; Vining,

their DNA (> 55 mol%). The group

encompasses genera covering a wide range

of morphologies extending from the coccus

(Micrococcus) and rod-coccus cycle bacteria

(e.g. Arthrobacter), through fragmenting hyphal

forms (e.g. Nocardia), to genera with a

permanent and highly differentiated branched

mycelium (Micromonospora, Streptomyces

and others). Some, but not all, genera form

spores that range from motile zoospores to

specialized propagules that resist desiccation

and mild heat, but which do not have the

organization and marked resistance properties

of the bacterial endospore. The molecular

classification of actinomycetes has been

examined by Stackebrandt et al. (1997). All the

actinomycete families were divided into ten

suborders (Stackebrandt et al., 1997) (Table 1).

1990).

Morphology and taxonomy of

actinomycetes

Actinomycetes are Gram-positive bacteria

with a high guanine plus cytosine content in

Table 1. Hierarchic classification of the actinomycetes based on the phylogenetic

analyses of the 16S rDNA sequence data (Stackebrandt et al., 1997).

Class: Actinobacteria; Subclass: Actinobacteridae; Order: Actinomycetales

Family

Suborder

Micrococcaceae, Brevibacteriaceae, Cellulomonadaceae,

Micrococcineae

Dermabacteriaceae, Dermatophilaceae, Intrasporangiaceae, Jonesiaceae,

Microbacteriaceae, Promicromonosporaceae

Actinomycineae

Frankineae

Actinomycetaceae

Frankiaceae, Acidothermaceae, Geodermatophilaceae,

Microsphaeraceae, Sporichthyaceae

Propionibacterineae

Streptomycineae

Propionibacteriaceae, Nocardioidaceae

Streptomycetaceae

Corynebacteriaceae, Dietziaceae, Gordoniaceae, Mycobacteriaceae,

Nocardiaceae, Tsukamurellaceae

Corynebacterineae

Micromonosporineae

Streptosporangineae

Pseudonocardineae

Glycomycineae

Micromonosporaceae

Streptosporangiaceae, Nocardiopsaceae, Thermomonosporaceae

Pseudonocardiaceae

Glycomycetaceae

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By far, streptomycetes are the most

abundant culturable actinomycete (Lee and

Hwang, 2002). The genus Streptomyces

belongs to the family Streptomycetaceae, a

unique family of the suborder Streptomycineae.

Streptomycetes grow as mycelial filaments in

soil; their mature colonies may contain two

types of mycelia, the substrate (vegetative)

mycelium, and the aerial mycelium. Each has

a different biological role (Hopwood, 1999).

Vegetative mycelia absorb nutrients, and are

composed of a dense and complex network of

hyphae usually embedded in the soil or

immobilize substrate. Once the cell culture

becomes nutrient-limited, an aerial mycelium

develops from the surface of the vegetative

mycelium. The role of this type of mycelium is

mainly reproductive; indeed, the aerial

mycelium develops into spore chains as the

mature stage in their life cycle (Hopwood,

we must understand how they colonize the

rhizosphere environment, and how they utilize

the different mechanisms of biocontrol once

they are established there. The rhizosphere is

a special environment where the plant is the

provider of nutrition to many life forms that are

competing for life space. Information on the

microflora present in the rhizosphere has been

obtained primarily through isolation and

cultivation of microorganisms from

rhizosphere soils on laboratory media.

However, more detailed descriptions of the

microbial populations associated with roots are

now possible with the use of molecular ecology

methods such as repetitive elements-PCR

(repPCR) (Schneider and De Brujin, 1996),

denaturing gradient gel electrophoresis

(DGGE) (Muyzer and Smalla, 1998;

Williamson et al., 2000), and green fluorescent

protein (GFP) (Gage et al., 1996). These

methods examine unculturable as well as

culturable organisms.

1999). Both, reproductive and aerial mycelium

along with clearly sporulation of some

mesophilic Streptomyces strains are shown in

Figure 1.

Within the rhizosphere, plant roots have a

direct effect on the composition and density of

the soil microbial populations. Root exudates

selectively influence the growth of bacterial and

fungal populations by altering the presence of

substrates in soil in the vicinity of roots

Actinomycetes as biological

control agents

Besides the enormous numbers of

agroactive metabolites produced by

actinomycetes (Tanaka and Omura, 1993), they

also play an important role in agriculture as

biocontrol agents. Antagonism against an

extensive variety of plant pathogens has been

reported (Bressan, 2003; Chamberlain and

Crawford, 1999; Doumbou et al., 2002;

Tahvonen and Avikainen, 1987; Trejo-Estrada

et al., 1998a; Yuan and Crawford, 1995). A

microorganism that colonizes roots is ideal for

use as a biocontrol agent against soil-borne

diseases (Weller, 1988). Actinomycetes,

especially Streptomyces, are qualitatively and

quantitatively important in the rhizosphere

where they actively colonize plant root systems

(

Grayston et al., 1996; Yang and Crowley,

000). Plant root exudates contain sugars,

amino acids, organic acids, fatty acids, sterols,

vitamins, nucleotides, and other compounds

(

Jaeger et al., 1999; Smucker, 1993). The

specific varieties of organic compounds

released by different plants have been

postulated to be a key factor influencing the

diversity of microorganisms in the rhizosphere

of different plant species (Buyer et al., 2002;

Doumbou et al., 2002; Grayston et al., 1996;

Grayston et al., 1998). There is also evidence

that production of root exudates can be up

regulated in the presence of certain nutrients.

For example, citrate, malate, and related

organic acids are over excreted by wheat and

(Crawford et al., 1993; Doumbou et al., 2001;

maize in response to high Al concentrations

Ma et al., 2001). The microflora present on

Tokala et al., 2002). To better understand how

these bacteria may act as biocontrol agents,

(

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Figure 1. Microscopic morphological structures of S.hygroscopicus strainsAZ529 (A-C),AZ541

(D-F), AZ560 (G) and S. lydicus WYEC108 (H).All the strains showed the spore chain

morphology (s) in compact long spirals, except for S. lydicus WYCED-108, which

showed flexuous chains of spores. Substrate mycelia is also showed (m).

Photographs by Ana C. Gonzalez-Franco

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the roots can also influence the amount of root

exudates produced. Rhizosphere-colonizing

bacteria referred to as plant growth-promoting

rhizobacteria (PGPR) can also influence the

nutritional status of the rhizosphere in several

ways. For example, many PGPR are able to

produce plant growth hormones such as

auxins (Brandl et al., 2001). Thus, the

rhizosphere is a dynamic habitat rich in

microorganisms and in plant microbe

interactions, some of which are beneficial to

the microbes and plants, and some of which

are detrimental to one and/or the other. For

example, root exudates from peas susceptible

to Fusarium oxysporum stimulated the fungus

in pure culture, but also caused many

rhizosphere isolates to antagonize the

pathogen (Rovira, 1965).

synthesis of particular extracellular enzymes,

and the degradation of phytotoxins (Lewis and

Starkey, 1969; Tokala et al., 2002; Trejo-Estrada

et al., 1998a). There are three mechanisms

known to be involved in this disease-suppression

phenomenon.

Antibiosis. Antibiosis occurs when the

antagonist (biocontrol agent) colonizes the

rhizosphere and produces one or more

substances that inhibits or kills the pathogen.

Antibiosis by root-colonizing actinomycetes has

been studied in several systems (Chamberlain

and Crawford, 1999; Crawford et al., 1993;

Rothrock and Gottlieb, 1984; Trejo-Estrada et

al., 1998a). There is evidence that antibiotics

are indeed produced in soil, and they have been

implicated in the biocontrol of pathogens in situ.

Rhothrock and Gottlieb (1984) tested

Streptomyces hygroscopicus var. geldanus, a

producer of geldanamycin, in soil pots for its

ability to control Rhizoctonia root rot of pea. Soil

antibiotic extraction was quantified and the

presence of antibiotic was correlated with

pathogen control. Amended soils with

geldanamycin in amounts equivalent to that

produced in vivo by the streptomycete also

controlled the disease (Rothrock and Gottlieb,

Mechanisms for biological

control of plant pathogens

Interest in biocontrol of plant pathogens

has increased considerably over the past

years, partly as a response to public concern

about the use of hazardous chemical

fungicides and pesticides such as methyl

bromide, but also because it may provide

control of diseases that cannot, or can only

partially, be managed by other control

strategies (Cook, 1993). Many studies on the

biocontrol of phytopathogens focus on the

suppressive effects of single biocontrol strains

on specific fungal pathogens.

984). Similarly, Trejo-Estrada (1998) tested

Streptomyces violaceusniger YCED9,

producer of nigericin, geldanamicin and a

complex of macrocyclic lactone antibiotics, in

greenhouse experiments to control Rhizoctonia

solani and Sclerotinia homeocarpa (causative

agents of grass seedling and crown-foliar

disease, respectively). Partial control of the

pathogen was associated with production of

antibiotics, one of which (nigericin) could be

extracted from the soil (Trejo-Estrada et al.,

Biocontrol of plant diseases, especially of

fungal origin, has been achieved using

microorganisms such as Trichoderma sp.,

Pseudomonas sp., Bacillus sp., and

Streptomyces sp. (Elad et al., 1980; Ligon et

al., 2000; Raaijmakers et al., 2002; Trejo-

Estrada et al., 1998a). Streptomycetes, along

with other bacterial strains belonging to the

Actinomycetales, have several properties that

give them the ability to act as effective

biocontrol agents in the rhizosphere, including

the ability to colonize plant root surfaces,

antibiosis against plant root pathogens, the

998b). Another study in the same

Streptomyces species showed that a mutant

of the strain defective in the production of

geldanamycin lost the ability to control the

disease (Beausejour et al., 2001).

Competition for nutrition and space. There

are cases where mutants of biocontrol strains

that are deficient in the production of

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antimicrobial substances are almost as efficient

in biocontrol as the wild type strains (Kempf

and Wolf, 1989). This mechanism of biocontrol

is related to the colonization ability and other

competitive traits of the biocontrol agent. The

ability to use a specific compound as an energy

source that not all microorganisms are able to

use, for example, can provide a competitive

advantage to the biocontrol agent. Also, the

ability to use and out compete pathogens for

inorganic compounds is another important

aspect, which would determine whether a

potential biocontrol agent will be successful or

not in suppressing a pathogen. Iron is one of

the resources that can limit growth of plant

pathogens and one well-known source for

nutrient competition in the rhizosphere (Douling

and O’Gara, 1994). By sequestering iron away

from invading pathogens, the root-colonizing

biocontrol strain prevents it from invading and

colonizing the plant roots.

2002; Valois et al., 1996) by a biocontrol agent.

These hydrolases initiate the process of

physical destruction of the fungal cell walls

(FCW) (Adams, 1990).As was mention above,

actinomycetes have the ability to produce a

wide variety of extracellular enzymes that

allows them to degrade various biopolymers

in soil. Numerous correlations between fungal

antagonism and bacterial production of

chitinases or glucanases have been noted

(Gonzalez-Franco et al., 2003). Also, mature

composts amended with chitin residues

acquire suppressive properties against fungal

plant pathogens. The microbial population of

one such suppressive compost was

characterized, and mainly Gram-positive

bacteria belonging to the actinomycetes were

found (Labrie et al., 2001). To have more

insight in the correlation of fungal

mycoparasitism and bacterial production of

lytic enzymes, knowledge of the composition

of the FCW is required, and enzymes from

known antifungal biocontrol agents need to be

isolated and characterized for the mycolytic

activities.

Streptomycetes, along with other bacterial

strains belonging to the Actinomycetales have

the ability to colonize plant root surfaces

(Kortemaa et al., 1994; Tokala et al., 2002).

Also, they have the capacity to synthesize

extracellular enzymes that allow them to use

recalcitrant organic compounds as energy

sources and to degrade phytotoxin compounds

Components of fungal cell walls

Fungal cell walls are made of fibrillar

polysaccharides (structural components)

including chitin, cellulose or other β-glucans,

embedded in a matrix of amorphous

components (cementing components) that

include polysaccharides, lipids, and proteins

that maintain the organization of the whole

structure (Ruiz-Herrera, 1992). Some of these

components are chemically associated via

covalent bonds, although hydrogen bonding

and hydrophobic associations are also

important in the configuration of the resulting

structure (Garret and Grisham, 1998; Gooday,

(

Goodfellow and Williams, 1983; Lewis and

Starkey, 1969; McCarthy and Williams, 1992).

Streptomycetes have the ability to produce iron-

chelating compounds, siderophores, that

starve pathogens for iron (Tokala et al., 2002).

The ability to produce siderophores as a

mechanism gives the biocontrol agent a

competitive advantage in environments, such

as rhizospheres, where soluble iron is scarce

(Mullen, 2004).

Parasitism. Parasitism is the third

1990; Ruiz-Herrera, 1992).

mechanism of phytopathogen biocontrol.

Mycoparasitism of fungal pathogens can

sometimes be attributed to the production of

extracellular lytic enzymes such as chitinases

Fungal cell walls are made mostly of

polysaccharides, which comprise typically

about 80-90% of their dry weight (Bartnicki-

Garcia, 1968). Proteins, lipids, pigments (e.g.

melanins), and inorganic salts are present in

smaller amounts (Ruiz-Herrera, 1992).

(Berg et al., 2002; Chernin et al., 1995; Lorito

et al., 1996) and β-1,3 glucanases (Berg et al.,

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Bartnicki-Garcia found that cell walls from fungi

could be grouped into eight different

chemotypes according to their polysaccharide

composition (Bartnicki-Garcia, 1968). This

author suggested an evolutionary pathway to

explain the divergence of the wall chemotypes

form, whereas in others, the opposite occurs.

In the case of Candida albicans, there is higher

amount of chitin present in the cell walls of the

mycelial (invasive) form of the fungus that is

associated to animal pathogenesis, since data

suggest that adhesive properties of invasive

mycelial cells are dependent, at least in part,

on the chitin present in the cell wall (Lehrer,

1986). The yeast form of C. albicans is included

in group VI of Bartnicki-Garcia (Table 2), which

comprises the yeast forms of the Ascomycetes

and Deuteromycetes. Glucans comprise

cellulose made of β-1,4 bonded glucose units,

and noncellulosic glucans containing variable

proportions of β-1,3 and β-1,6 linkages, and á-

1,3 glucans. The noncellulosic glucan type is

the most abundant form in fungal cell wall

chemotypes (Table 2). Some polysaccharides

are characteristic of specific fungal groups, for

example chitosan. This deacetylated analog of

chitin has been found to be a characteristic

component of the cell walls from Zygomycetes

(Table 2). Biocontrol agents that have the ability

to mycoparasitize fungal pathogens generally

produce a variety of hydrolytic enzymes active

against multiple cell wall components.

(

Table 2). By far, the most numerous category

including most of the pathogens of plants) is

the group V (chitin-glucan), harboring all

mycelial forms of the Ascomycetes,

Basidiomycetes, and Deuteromycetes. The

Chytridiomycetes, are also included (Table 2).

Chitin is the most characteristic polysaccharide

of the fungal cell walls. It is an unbranched

polysaccharide made of N-acetylglucosamine

(GlcNAc) joined through β-1,4 bonds. Chitin

was once thought to be absent in Oomycetes;

however, traces of chitin are actually present

in the cell walls of members of this fungal

group, including pathogens such as

Phytophthora, and Pythium species (Dietrich,

973). Differences in the content of chitin

between both morphologies of dimorphic fungi

have been noticed. However, these differences

appear unrelated to either morphology. Some

species contain more chitin in the mycelial

Table 2. Chemotypes of fungal cell walls (Bartnicki-Garcia, 1968).

Taxonomic group

Chemotype

Cellulose-glycogen

Acrasiales

II Cellulose-glucan

III Cellulose-chitin

IV Chitosan-chitin

Oomycetesa

Hyphochytridiomycetes

Zygomycetes

Chitin-glucan

Chytridiomycetes, Euascomycetes, Homobasidiomycetes and Deuteromycetes

VI Mannan-glucanb

VII Mannan-chitin

Hemiascomycetes

Heterobasidiomycetes

VIII Polygalactosamine-galactan Trichomycetes

Incompletely characterized; probably β-1,3- and β-1,6-linked.

Chitin is present in low amounts

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Conclusion remarks

BRANDL, M. T., Quinones, B. and Lindow, S. (2001).

Heterogeneous transcription of an indoleacetic acid

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The control of plant diseases is an urgent

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application of agrochemicals for this purpose,

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ability to colonize plant root surfaces protecting

the plant for pressure of plant pathogens.

These biological control agents compete for

nutrients and space with plant pathogens; they

also synthesize extracellular enzymes that

attack the phytopathogenic fungal cell walls and

they have the ability to produce descant-

resistant spores to survive under water

deficiency. All the properties exhibited by

actinomycetes, especially those that belong to

the genus Streptomyces as biological control

agents of fungal phytopathogens, not only give

us a better understanding in their environmental

and ecological benefits, but also in their impact

as an attractive alternative for use in

agriculture.

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• Vol. III, No. 2 • Mayo-Agosto 2009 •

ANA CECILIA GONZÁLEZ-FRANCO Y LORETO ROBLES HERNÁNDEZ: Actinomycetes as biological control agents of

phytopathogenic fungi

Este artículo es citado así:

González-Franco A. C. y L. Robles-Hernández. 2009: Actinomycetes as biological control agents of

phytopathogenic fungi. TECNOCIENCIA Chihuahua 3(2): 64-73.

Resúmenes curriculares de autor y coautores

ANA CECILIA GONZÁLEZ-FRANCO. Es profesora-investigadora de la Facultad de Ciencias Agrotecnológicas de la UniversidadAutónoma de

Chihuahua (UACH). Obtuvo su licenciatura en la Facultad de Ciencias Químicas, su maestría en la Facultad de Ciencias

Agrotecnológicas de la Universidad Autónoma de Chihuahua y su doctorado en Microbiología, Biología Molecular y Bioquímica lo

obtuvo en la Universidad de Idaho, USA. Su área de investigación se centra en el control biológico de enfermedades y en la

interacción-microorganismo-planta. Imparte las cátedras de Interacción Microorganismo Planta, Bioquímica, Química y Biotecnología.

Asesora estudiantes de licenciatura y posgrado. Es responsable del área de microbiología aplicada y biología molecular en el

Laboratorio de Microbiología Aplicada, Fitopatología y Fisiología Post-cosecha de la Facultad de Ciencias Agrotecnológicas,

UACH.

LORETO ROBLES-HERNÁNDEZ. Es profesor-investigador de la Facultad de Ciencias Agrotecnológicas de la Universidad Autónoma de

Chihuahua. Obtuvo su licenciatura en 1992, su maestría en 1994 en la misma institución y su doctorado en la Universidad de Idaho,

USA en 2004. Su investigación se centra en la epidemiología de enfermedades de plantas, con énfasis en aquellas causadas por

virus y por bacterias fitopatógenas. Imparte los cursos de Fitopatología, Microbiología, Control Biológico y Fisiología Post-cosecha.

Asesora estudiantes de licenciatura y maestría. Está a cargo del área de fitopatología y fisiología post-cosecha en el laboratorio

de Microbiología Aplicada, Fitopatología y Fisiología de Post-cosecha de la Facultad de Ciencias Agrotecnológicas, UACH.

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Vol. III, No. 2 • Mayo-Agosto 2009 •