30 - Medicinal Plants

ORIGINAL PAPER

Actinomycetes isolated from medicinal plant rhizosphere soils:diversity and screening of antifungal compounds, indole-3-aceticacid and siderophore production

Sutthinan Khamna Æ Akira Yokota ÆSaisamorn Lumyong

Received: 24 July 2008 / Accepted: 27 November 2008 / Published online: 16 December 2008

� Springer Science+Business Media B.V. 2008

Abstract A total of 445 actinomycete isolates were

obtained from 16 medicinal plant rhizosphere soils. Mor-

phological and chemotaxonomic studies indicated that 89%

of the isolates belonged to the genus Streptomyces, 11%

were non-Streptomycetes: Actinomadura sp., Microbispora

sp., Micromonospora sp., Nocardia sp, Nonomurea sp. and

three isolates were unclassified. The highest number and

diversity of actinomycetes were isolated from Curcuma

mangga rhizosphere soil. Twenty-three Streptomyces iso-

lates showed activity against at least one of the five

phytopathogenic fungi: Alternaria brassicicola, Collecto-

trichum gloeosporioides, Fusarium oxysporum, Penicillium

digitatum and Sclerotium rolfsii. Thirty-six actinomycete

isolates showed abilities to produce indole-3-acetic acid

(IAA) and 75 isolates produced siderophores on chrome

azurol S (CAS) agar. Streptomyces CMU-PA101 and

Streptomyces CMU-SK126 had high ability to produced

antifungal compounds, IAA and siderophores.

Keywords Actinomycetes � Antagonistic �Indole-3-acetic acid � Siderophores � Biocontrol

Introduction

Microorganisms have been shown to be attractive sources

of natural compounds for the pharmaceutical and other

industries. In agriculture, phytopathogenic fungi can cause

plant diseases and much loss of crop yields. Pesticides are

used to control plant diseases. However, agrochemical

treatment causes environmental pollution and decreased

diversity of non-target organisms. Microorganisms as bio-

logical control agents have high potential to control plant

pathogens and no effect on the environment or other non-

target organisms. There are numerous reports on the

potential use of biocontrol agents as replacements for

agrochemicals (Shimizu et al. 2000; Yang et al. 2007).

Actinomycetes are Gram-positive bacteria. They are the

most widely distributed group of microorganisms in nature.

They are also well known as saprophytic soil inhabitants

(Takisawa et al. 1993). Most actinomycetes in soil belong to

the genus Streptomyces (Goodfellow and Simpson 1987) and

75% of biologically active compounds are produced by this

genus. Actinomycetes occur in the plant rhizosphere soil and

produce active compounds (Suzuki et al. 2000). Attention

has been paid to the possibility that actinomycetes can pro-

tect roots by inhibiting the development of potential fungal

pathogens by producing enzymes which degrade the fungal

cell wall or producing antifungal compounds (Goodfellow

and Williams 1983). For example, Streptomyces sp. strain

5406 has been used in China to protect cotton crops against

soil-borne pathogens (Valois et al. 1996). Actinomycetes can

promote plant growth by producing promoters such as

indole-3-acetic acid (IAA) to help growth of roots or produce

siderophores to improve nutrient uptake (Merckx et al.

1987). However, the rate of discovery of new secondary

metabolites has been decreasing, so the discovery of acti-

nomycetes in several sources increases the chance for the

discovery of new secondary metabolites (Hayakawa et al.

2004). Active actinomycetes may be found in medicinal

plant root rhizosphere soils and may have the ability to

produce new inhibitory compounds.

S. Khamna � S. Lumyong (&)

Department of Biology, Faculty of Science, Chiang Mai

University, Chiang Mai 50200, Thailand

e-mail: [email protected]; [email protected]

A. Yokota

Institute of Molecular and Cellular Biosciences,

The University of Tokyo, Tokyo, Japan

123

World J Microbiol Biotechnol (2009) 25:649–655

DOI 10.1007/s11274-008-9933-x

The present studies involved the isolation and identifi-

cation of actinomycetes from medicinal plant rhizosphere

soils. The isolates were characterized regarding their bio-

control activity and their in vitro production of active

compounds related to plant growth promotion.

Materials and methods

Sampling

Soil samples were collected from 16 medicinal plant rhi-

zospheres in Lumphun Province. The samples were air

dried at room temperature for 7 days. Soil pH was analyzed

according to the method of Suzuki et al. (2000).

Isolation of actinomycetes

One gram of each air-dried soil sample was treated in two

ways: pretreated with 6% yeast extract and 0.05% sodium

dodecylsulfate (SDS) (Hayakawa et al. 1988) or pretreated

with 1.5% phenol (Hayakawa et al. 2004). Humic acid

vitamin agar (HVA), oatmeal agar (OMA) and starch–casein

agar (SCA) pH 7.0 were used as selective media for isolation

of actinomycetes. All media were supplemented with 100 lg

nystatin/ml, 100 lg cycloheximide/ml and 50 lg nalidixic

acid/ml (Teachowisan et al. 2003). The plates were incu-

bated at 28�C for 4 weeks. Individual colonies were re-

grown at 28�C on ISP-2 agar for purification. The isolated

colonies were subcultured onto Hickey–Trener (HT) slants

and kept in 20% glycerol at -20�C as stock culture.

Characterization of actinomycete isolates

Morphological identification and chemotaxonomic

analyses

Purified isolates were identified to genus level according to

Bergey’s Manual of Determinative Bacteriology (Holt et al.

1994) after direct microscopic observation at (400 and

10009 magnification) of the vegetative and aerial myce-

lium developed as growth on cover slips buried in ISP-2

medium. Color of spore mass and diffusible pigment pro-

duction were visually estimated by using a color chart. Cell

wall diaminopimelic acid (A2 pm) and sugar isomer were

analyzed as described by Hasegawa et al. (1983).

DNA extraction, amplification and sequencing of the 16S

rDNA of Streptomyces sp.CMU-PA101, Streptomyces

CMU-SK126 and Streptomyces CMU-H009

Genomic DNA of Streptomyces CMU-PA101, Streptomy-

ces CMU-SK126 and Streptomyces CMU-H009, which

show high ability to inhibit five pathogenic fungi, produced

siderophores and IAA, were prepared according to a

modification of the CTAB method (Murray and Thompson

1980). PCR amplification of 16S rDNA was carried out

with a set of universal primers 27f and 1525r. The nucle-

otide sequences of the 16S rDNA obtained were subjected

to BLAST analysis with the NCBI database and submitted

to GenBank.

In vitro antagonistic bioassay

The actinomycete isolates were evaluated for their activity

towards five pathogenic fungi: Alternaria brassicicola (rose

apple anthracnose), Colletotrichum gloeosporioides (potato

dry rot), Fusarium oxysporum (Chinese cabbage leaf spot),

Penicillium digitatum (orange green mold) and Sclerotium

rolfsii (damping-off of balsam) by dual-culture in vitro

assay. These fungi were maintained on potato dextrose agar

(PDA) at room temperature and kept in a culture collection

at the Laboratory of Applied Microbiology, Department of

Biology, Faculty of Science, Chiang Mai University. Fun-

gal discs (8 mm diam.), 5 days old on potato dextrose agar

(PDA) at 28�C were placed at the center of PDA plates.

Two actinomycete discs (8 mm) 5 days old, grown on yeast

malt extract agar (YM) incubated at 28�C were placed on

opposite sides of the plates, 3 cm away from the fungal disc.

Plates without the actinomycete disc served as controls. All

plates were incubated at 28�C for 14 days and colony

growth inhibition (%) was calculated by using the formula:

C - T/C 9 100, where C is the colony growth of pathogen

in control, and T is the colony growth of pathogen in dual-

culture. All isolates were tested in triplicate.

Indole acetic acid (IAA) production

The production of IAA by 200 actinomycete isolates was

determined according to the method of Bano and Musarrat

(2003). The actinomycete discs (8 mm), grown on yeast malt

extract agar (YM) incubated at 28�C for 5 days, were inoc-

ulated into 5 ml YM broth containing 0.2% L-tryptophan and

incubated at 28�C with shaking at 125 rev/min for 7 days.

Cultures were centrifuged at 11,000 rev/min for 15 min. One

milliliter of the supernatant was mixed with 2 ml of Sal-

kowski reagent. Appearance of a pink color indicated IAA

production. Optical density (OD) was read at 530 nm using a

spectrophotometer. The level of IAA produced was esti-

mated by comparison with an IAA standard.

Screening for siderophore production

The actinomycete discs (8 mm), grown on YM agar incu-

bated at 28�C for 5 days were inoculated on CAS-substrates

with modified Gaus No.1 medium (MGs) (You et al. 2004)

650 World J Microbiol Biotechnol (2009) 25:649–655

123

and incubated at 28�C for 10 days. The colonies with

orange zones were considered as siderophore-producing

isolates. The functional groups of the siderophores were

determined. The active isolates (width of orange zone on

CAS plate[20 mm) were cultured on modified Gaus No.1

broth and incubated at 28�C with shaking at 125 rpm for

10 days. Catechol-type siderophores were estimated by

Arnow’s method (Arnow 1937) and hydroxamate sidero-

phores were estimated by the Csaky test (Csaky 1948).

Results and discussion

Actinomycete isolates from rhizosphere soils

From 16 medicinal plant rhizosphere soils, 445 isolates of

actinomycete were obtained (Table 1). About 89% of the

isolates were presumed to be in genus Streptomyces and

11% were identified to the genera Acitinomadura, Micro-

bispora, Micromonospora, Nocardia and Nonomurea.

Three isolates were unidentified. Streptomyces were pres-

ent in all rhizosphere soils, regardless of wild or

agricultural plant species, suggesting their wide distribu-

tion in association with plants in the natural environment.

The others actinomycetes were rare and could be isolated

from some rhizosphere soils. Streptomyces were the dom-

inant actinomycetes isolated from all 16 plant rhizosphere

soils, a result reported by others (Atalan et al. 2000;

Jayasinghe and Parkinson 2007; Pandey and Palni 2007;

Sembiring et al. 2000). The number and diversity of acti-

nomycetes isolated from Curcuma mangga rhizosphere

were higher than from other rhizosphere soils. Merckx

et al. (1987) indicated that the rhizosphere represents a

unique biological niche that supports abundant and diverse

saprophytic microorganisms because of a high input of

organic materials derived from the plant roots and root

exudates. Previous studies have shown that diversity of

actinomycetes in rhizosphere soils is positively correlated

to the level of organic matter and depended on the species

of plant (Germida et al. 1998; Hayakawa et al. 1988; Henis

1986). Tewtrakul and Subhadhirasakul (2007) found that

the roots of Curcuma mangga produced an antimicrobial

compound. It is possible that root exudates from this plant

might promote the growth of actinomycetes and antimi-

crobial compounds from the roots might decrease the

number of other soil bacteria and fungi so that the diversity

of actinomycetes from this soil is higher than other soils.

Effect of the pretreatment approach

The number of actinomycetes isolated from soils pretreated

with 6% yeast extract and 0.05% SDS was higher than

from those pretreated with 1.5% phenol. Pretreatment with

6% yeast extract and 0.05% SDS increased efficiency when

Table 1 Occurrence and distribution of actinomycetes from rhizosphere soils of medicinal plants

Plant rhizosphere soil pH No. of

StreptomycesNo. of rare actinomycete isolates

A B C D E F

Acanthus ebrateatus Vahl. (sea holly) 7.30 21

Achyranthes aspera L. (prickly chaff flower) 6.92 30 1 1

Amaranthus gracilis Desf. (spinach) 6.93 23 1

Bariena lunulina L. 6.98 17 2

Boesenbergia pandurata Schl. (fingerroot) 5.80 19 1

Curcuma mangga Val. and Zijp. 6.90 45 1 1 1 2 1 0

Cymbopogon citratus Stapf. (lemongrass) 7.00 29 2

Cymbopogon nardus Rendle.(citronellagrass)

7.00 13 3 1

Cyperus rotundus L. (cocograss) 6.38 10 1

Imperata cylindrical Beauv. (cogongrass) 6.92 30 1

Languas galanga L. (galangal) 6.89 22 2

Ocimum sanctum L. (holy basil) 7.01 32 1 4 1

Pandanus amaryllifolius Roxb.

(pandanus palm)

6.87 42 1 4

Rhinacanthus nasutus Kurz. 7.09 21 1 3

Stemona tuberosa Lour. (stemona) 6.93 18 1 1 4 1 2

Zingiber officinale Rose. (ginger) 6.63 24 1 2

Total 396 (89.0%) 4 (0.90%) 2 (0.50%) 6 (1.40%) 31 (7.0%) 3 (0.70%) 3 (0.70%)

A, Actinomadura; B, Microbispora; C, Micromonospora sp.; D, Nocardia sp.; E, Nonomurea sp.; F, unidentified

World J Microbiol Biotechnol (2009) 25:649–655 651

123

isolating general actinomycetes (Hayakawa et al. 1988).

Phenol is a biocide and toxic to actinomycetes, so treat-

ment with 1.5% phenol reduced the number of

actinomycetes which were sensitive to this biocide

(Hayakawa et al. 2004). Humic acid vitamin agar was the

best medium for isolating actinomycetes from both pre-

treatments because this medium contained soil humic acid

as sole carbon and nitrogen sources which were suitable for

recovery of actinomycetes from soil samples (Fig. 1).

Antimicrobial activities

Twenty-three (5.2%) of actinomycete isolates were active

against at least one of the five pathogenic fungi. All the

active isolates were identified as Streptomyces sp.

(Table 2). Most of the active strains were isolated from

pandanus palm (Pandanus amaryllifolius) rhizosphere.

Lemanceau et al. (1995) and Wiehe et al. (1996) indicated

that differences in the quantitative and qualitative compo-

sition of root excretions provide different impact on the

rhizosphere microbiota and attract more or less bacterial

antagonists responsible for natural soil suppression. Plant

root exudates stimulate growth of rhizosphere actinomy-

cetes that are strongly antagonistic to fungal pathogens,

while the actinomycetes utilize root exudates for growth

and synthesis of antimicrobial substances (Crawford et al.

1993; Yuan and Crawford 1995). It is possible that

Fig. 1 Number of actinomycete isolates using two pretreatment

methods and three media

Table 2 Antifungal activities of Streptomyces isolates

Streptomycesisolates

% inhibitiona

Alternariabrassicicola

Colletotrichumgloeosporioides

Fusariumoxysporum

Penicilliumdigitatum

Sclerotiumrolfsii

CMU C14-12 0 0 55.4 ± 1.2 0 0

CMU Gin001 0 0 0 58.4 ± 0.8 0

CMU Gin003 26.5 ± 0.7 84.6 ± 0.6 68.7 ± 0.4 62.2 ± 0.5 0

CMU Gin005 0 0 0 62.3 ± 0.4 0

CMU G7-2 0 0 0 69.8 ± 0.2 0

CMU H001 0 0 0 58.7 ± 0.3 0

CMU PA001 0 0 25 ± 0.3 0 0

CMU PA101 97.5 ± 0.6 85.0 ± 0.4 74.2 ± 0.3 98.5 ± 0.8 77.5 ± 0.7

CMU PA510 0 0 25 ± 0.5 45.5 ± 0.8 0

CMU PA511 46.0 ± 0.4 42.9 ± 0.8 0 40 ± 0.9 0

CMU PA517 40.0 ± 0.6 57.1 ± 0.8 43.7 ± 0.9 0 0

CMU PA521 0 20.6 ± 0.6 0 63.9 ± 0.3 0

CMU PA528 0 0 0 42.5 ± 1.1 0

CMU PA531 0 0 0 44.0 ± 0.5 0

CMU PA529 0 28.6 ± 0.5 0 0 0

CMU PA537 49.0 ± 0.5 0 0 0 0

CMU PA533 0 42.9 ± 1.1 0 0 0

CMU PA539 0 42.9 ± 0.7 0 0 0

CMU SK126 69.9 ± 0.9 70.0 ± 0.5 77.5 ± 0.4 55.0 ± 0.2 68.8 ± 1.0

CMU SK132 0 0 0 39.9 ± 0.8 0

CMU UK102 0 0 25.0 ± 0.4 0 0

CMU W110 0 0 37.5 ± 0.3 0 0

CMU X209 0 0 25.0 ± 0.4 0 0

a Average ± standard error from triplicate samples


123

excretions from the roots of pandanus palm might induce

actinomycetes that show anti-fungal activity. Two isolates,

Streptomyces CMU-PA101 (accession number FJ025786)

from P. amaryllifolius rhizosphere and Streptomyces

CMU-SK126 (accession number FJ217218) from

C. mangga rhizosphere, strongly inhibited all of the path-

ogenic fungi (Fig. 2). The 16SrRNA gene sequences of

Streptomyces CMU-PA101 and Streptomyces CMU-SK126

were similar to Streptomyces spectabilis (99% identity) and

Streptomyces cinnamoneus (99% identity). Similar studies

have been carried out by other workers. Ouhdouch and

Barakate (2001) found 10 isolates of actinomycetes from

medicinal plant rhizosphere soils, most of which were

Streptomyces spp. After testing for antifungal activity

against Candida albicans and C. tropicalis, they found that

all Streptomyces had antifungal activity. Thangapandian

et al. (2007) isolated Streptomyces from medicinal plant

rhizosphere soils and 8 isolates had antipathogenic activity.

Crawford et al. (1993) found that 12 actinomycete strains

isolated from Taraxicum officinale rhizosphere were active

against Pythium ultimum. Although 89.5% of the Strepto-

myces isolates in this study did not show any antifungal

activity towards the test organisms, they might produce

other useful compounds.

Fig. 2 Zones of growth inhibition caused by metabolites from

Streptomyces CMU PA101, grown on potato dextrose agar for

14 days, against a Fusarium oxysporum b Sclerotium sp. c Collet-otrichum gloeosporioides. Left, control; right, in the presence of

Streptomyces CMU PA101

Table 3 IAA production by actinomycete isolates after 7 days

incubation

Genus Isolates IAA production (lg/ml)a

Actinomadura CMU-AW310 17.44 ± 0.1

Actinomadura CMU-li5 5.47 ± 0.7

Actinomadura CMU-Li7 29.20 ± 0.4

Nocardia CMU-li6 44.73 ± 0.9

Nocardia CMU-O107 54.44 ± 0.2

Nonomurea CMU-AW311 31.71 ± 0.1

Streptomyces CMU-Aa104 57.46 ± 0.9

Streptomyces CMU-At204 29.22 ± 0.2

Streptomyces CMU-Aw312 30.66 ± 0.3

Streptomyces CMU-Bc014 16.93 ± 0.2

Streptomyces CMU-CL401 24.31 ± 0.3

Streptomyces CMU-Gin001 33.83 ± 06

Streptomyces CMU-Gin002 13.93 ± 0.4




Streptomyces CMUG-I 13.64 ± 0.5

Streptomyces CMU-H009 143.95 ± 0.2


Streptomyces CMU-K101 13.23 ± 0.2





Streptomyces CMU-L105 14.60 ± 0.5

Streptomyces CMU-PA101 28.86 ± 0.3




Streptomyces CMU-PE401 28.52 ± 0.6

Streptomyces CMU-SK126 13.79 ± 0.3

Streptomyces CMU-T101 11.31 ± 1.6

Streptomyces CMU-T301 25.79 ± 0.3

Streptomyces CMU-VAN301 29.34 ± 0.4


Streptomyces CMU-X208 11.03 ± 0.2



123

Indole acetic acid (IAA) and siderophore production

Thirty-six (8.1%) of actinomycete isolates produced IAA,

and 30 of these were Streptomyces sp. (Table 3). The

range of IAA production was 5.5–144 lg/ml. Streptomy-

ces CMU-H009 (accession number FJ185171) isolated

from lemongrass (Cymbopogon citrates) showed high

ability to produce IAA. The 16SrRNA gene sequence was

found to be 99% identical, to Streptomyces viridis. El-

Tarabilya and Sivasithamparamb (2006) and Tsavkelova

et al. (2006) found that Streptomyces from many crop

rhizosphere soils have the ability to produce IAA and

promoted plant growth. In the rhizosphere soils, root

exudates are the natural source of tryptophan for rhizo-

sphere micro-organisms, which may enhance auxin

biosynthesis in the rhizosphere. It is possible that high

tryptophan will be present in root exudates of lemongrass

and enhance IAA biosynthesis in Streptomyces CMU-

H009. Siderophore production were found in 45 (27.5%)

of all actinomycete isolates. The active isolates grew on

CAS agar and an orange halo formed around the colonies.

Most of them were Streptomyces (Table 4). Streptomyces

CMU-SK126 isolated from C. mangga rhizosphere soil

showed high ability to produce siderophores. This isolate

produced catechols 16.19 lg/ml and hydroxamate

54.9 lg/ml on modified Gaus No.1 broth (Table 5).

Usually, siderophores are produced by various soil

microbes to bind Fe3? from the environment, transport it

back to the microbial cell and make it available for

growth (Leong 1996; Neilands and Leong 1986). Micro-

bial siderophores may also be utilized by plants as an iron

source (Bar-Ness et al. 1991; Wang et al. 1993). Rhizo-

sphere soil actinomycetes have to compete with other

rhizosphere bacteria and fungi for iron supply and

therefore siderophore production may be very important

for their growth. Competition for iron is also a possible

mechanism to control the phytopathogens. Soil Strepto-

myces have been reported to produce hydroxamate-type

siderophores that could inhibit the growth of phytopath-

ogens by competition for iron in plant rhizosphere soils

(Muller et al. 1984; Muller and Raymond 1984; Tokala

et al. 2002).

From the present study, it could be demonstrated that

rhizosphere soil from Curcuma mangga provided a rich

source of diversity of actinomycetes. Streptomyces CMU-

PA101, Streptomyces CMU-SK126 and Streptomyces

CMU-H009 had the ability to produce high antifungal

compounds, siderophore and IAA. However, more detailed

investigation is required to demonstrate the potential of

these organisms for the biocontrol of pathogenic fungi and

in plant growth promotion which may be useful in phar-

macological and agricultural fields in the future.

Acknowledgments This work was supported by The Royal Golden

Jubilee Ph.D. Program (PHD/0153/2546). We are grateful to Dr. Eric

H. C McKenzie (Landcare Research, Private Bag 92170, Auckland,

New Zealand) for improving the English text.

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Table 4 Siderophore-

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?, \10 mm; ??, 10–20 mm;

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