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  • World J Microbiol Biotechnol (2009) 25:649–655DOI 10.1007/s11274-008-9933-x ORIGINAL PAPERActinomycetes isolated from medicinal plant rhizosphere soils:diversity and screening of antifungal compounds, indole-3-aceticacid and siderophore productionSutthinan Khamna Æ Akira Yokota ÆSaisamorn LumyongReceived: 24 July 2008 / Accepted: 27 November 2008 / Published online: 16 December 2008Ó Springer Science+Business Media B.V. 2008Abstract A total of 445 actinomycete isolates were industries. In agriculture, phytopathogenic fungi can causeobtained from 16 medicinal plant rhizosphere soils. Mor- plant diseases and much loss of crop yields. Pesticides arephological and chemotaxonomic studies indicated that 89% used to control plant diseases. However, agrochemicalof the isolates belonged to the genus Streptomyces, 11% treatment causes environmental pollution and decreasedwere non-Streptomycetes: Actinomadura sp., Microbispora diversity of non-target organisms. Microorganisms as bio-sp., Micromonospora sp., Nocardia sp, Nonomurea sp. and logical control agents have high potential to control plantthree isolates were unclassified. The highest number and pathogens and no effect on the environment or other non-diversity of actinomycetes were isolated from Curcuma target organisms. There are numerous reports on themangga rhizosphere soil. Twenty-three Streptomyces iso- potential use of biocontrol agents as replacements forlates showed activity against at least one of the five agrochemicals (Shimizu et al. 2000; Yang et al. 2007).phytopathogenic fungi: Alternaria brassicicola, Collecto- Actinomycetes are Gram-positive bacteria. They are thetrichum gloeosporioides, Fusarium oxysporum, Penicillium most widely distributed group of microorganisms in nature.digitatum and Sclerotium rolfsii. Thirty-six actinomycete They are also well known as saprophytic soil inhabitantsisolates showed abilities to produce indole-3-acetic acid (Takisawa et al. 1993). Most actinomycetes in soil belong to(IAA) and 75 isolates produced siderophores on chrome the genus Streptomyces (Goodfellow and Simpson 1987) andazurol S (CAS) agar. Streptomyces CMU-PA101 and 75% of biologically active compounds are produced by thisStreptomyces CMU-SK126 had high ability to produced genus. Actinomycetes occur in the plant rhizosphere soil andantifungal compounds, IAA and siderophores. produce active compounds (Suzuki et al. 2000). Attention has been paid to the possibility that actinomycetes can pro-Keywords Actinomycetes Á Antagonistic Á tect roots by inhibiting the development of potential fungalIndole-3-acetic acid Á Siderophores Á Biocontrol pathogens by producing enzymes which degrade the fungal cell wall or producing antifungal compounds (Goodfellow and Williams 1983). For example, Streptomyces sp. strainIntroduction 5406 has been used in China to protect cotton crops against soil-borne pathogens (Valois et al. 1996). Actinomycetes canMicroorganisms have been shown to be attractive sources promote plant growth by producing promoters such asof natural compounds for the pharmaceutical and other 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 secondaryS. Khamna Á S. Lumyong (&)Department of Biology, Faculty of Science, Chiang Mai metabolites has been decreasing, so the discovery of acti-University, Chiang Mai 50200, Thailand nomycetes in several sources increases the chance for thee-mail: koymicro@yahoo.com; scboi009@chiangmai.ac.th discovery of new secondary metabolites (Hayakawa et al. 2004). Active actinomycetes may be found in medicinalA. YokotaInstitute of Molecular and Cellular Biosciences, plant root rhizosphere soils and may have the ability toThe University of Tokyo, Tokyo, Japan produce new inhibitory compounds. 123
  • 650 World J Microbiol Biotechnol (2009) 25:649–655 The present studies involved the isolation and identifi- show high ability to inhibit five pathogenic fungi, producedcation of actinomycetes from medicinal plant rhizosphere siderophores and IAA, were prepared according to asoils. The isolates were characterized regarding their bio- modification of the CTAB method (Murray and Thompsoncontrol activity and their in vitro production of active 1980). PCR amplification of 16S rDNA was carried outcompounds related to plant growth promotion. 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 submittedMaterials and methods to GenBank.Sampling In vitro antagonistic bioassaySoil samples were collected from 16 medicinal plant rhi- The actinomycete isolates were evaluated for their activityzospheres in Lumphun Province. The samples were air towards five pathogenic fungi: Alternaria brassicicola (rosedried at room temperature for 7 days. Soil pH was analyzed apple anthracnose), Colletotrichum gloeosporioides (potatoaccording to the method of Suzuki et al. (2000). dry rot), Fusarium oxysporum (Chinese cabbage leaf spot), Penicillium digitatum (orange green mold) and SclerotiumIsolation of actinomycetes rolfsii (damping-off of balsam) by dual-culture in vitro assay. These fungi were maintained on potato dextrose agarOne gram of each air-dried soil sample was treated in two (PDA) at room temperature and kept in a culture collectionways: pretreated with 6% yeast extract and 0.05% sodium at the Laboratory of Applied Microbiology, Department ofdodecylsulfate (SDS) (Hayakawa et al. 1988) or pretreated Biology, Faculty of Science, Chiang Mai University. Fun-with 1.5% phenol (Hayakawa et al. 2004). Humic acid gal discs (8 mm diam.), 5 days old on potato dextrose agarvitamin agar (HVA), oatmeal agar (OMA) and starch–casein (PDA) at 28°C were placed at the center of PDA plates.agar (SCA) pH 7.0 were used as selective media for isolation Two actinomycete discs (8 mm) 5 days old, grown on yeastof actinomycetes. All media were supplemented with 100 lg malt extract agar (YM) incubated at 28°C were placed onnystatin/ml, 100 lg cycloheximide/ml and 50 lg nalidixic opposite sides of the plates, 3 cm away from the fungal disc.acid/ml (Teachowisan et al. 2003). The plates were incu- Plates without the actinomycete disc served as controls. Allbated at 28°C for 4 weeks. Individual colonies were re- plates were incubated at 28°C for 14 days and colonygrown at 28°C on ISP-2 agar for purification. The isolated growth inhibition (%) was calculated by using the formula:colonies were subcultured onto Hickey–Trener (HT) slants C - T/C 9 100, where C is the colony growth of pathogenand kept in 20% glycerol at -20°C as stock culture. in control, and T is the colony growth of pathogen in dual- culture. All isolates were tested in triplicate.Characterization of actinomycete isolates Indole acetic acid (IAA) productionMorphological identification and chemotaxonomicanalyses The production of IAA by 200 actinomycete isolates was determined according to the method of Bano and MusarratPurified isolates were identified to genus level according to (2003). The actinomycete discs (8 mm), grown on yeast maltBergey’s Manual of Determinative Bacteriology (Holt et al. extract agar (YM) incubated at 28°C for 5 days, were inoc-1994) after direct microscopic observation at (400 and ulated into 5 ml YM broth containing 0.2% L-tryptophan and10009 magnification) of the vegetative and aerial myce- incubated at 28°C with shaking at 125 rev/min for 7 days.lium developed as growth on cover slips buried in ISP-2 Cultures were centrifuged at 11,000 rev/min for 15 min. Onemedium. Color of spore mass and diffusible pigment pro- milliliter of the supernatant was mixed with 2 ml of Sal-duction were visually estimated by using a color chart. Cell kowski reagent. Appearance of a pink color indicated IAAwall diaminopimelic acid (A2 pm) and sugar isomer were production. Optical density (OD) was read at 530 nm using aanalyzed as described by Hasegawa et al. (1983). spectrophotometer. The level of IAA produced was esti- mated by comparison with an IAA standard.DNA extraction, amplification and sequencing of the 16SrDNA of Streptomyces sp.CMU-PA101, Streptomyces Screening for siderophore productionCMU-SK126 and Streptomyces CMU-H009 The actinomycete discs (8 mm), grown on YM agar incu-Genomic DNA of Streptomyces CMU-PA101, Streptomy- bated at 28°C for 5 days were inoculated on CAS-substratesces CMU-SK126 and Streptomyces CMU-H009, which with modified Gaus No.1 medium (MGs) (You et al. 2004)123
  • World J Microbiol Biotechnol (2009) 25:649–655 651and incubated at 28°C for 10 days. The colonies with soils, a result reported by others (Atalan et al. 2000;orange zones were considered as siderophore-producing Jayasinghe and Parkinson 2007; Pandey and Palni 2007;isolates. The functional groups of the siderophores were Sembiring et al. 2000). The number and diversity of acti-determined. The active isolates (width of orange zone on nomycetes isolated from Curcuma mangga rhizosphereCAS plate [20 mm) were cultured on modified Gaus No.1 were higher than from other rhizosphere soils. Merckxbroth and incubated at 28°C with shaking at 125 rpm for et al. (1987) indicated that the rhizosphere represents a10 days. Catechol-type siderophores were estimated by unique biological niche that supports abundant and diverseArnow’s method (Arnow 1937) and hydroxamate sidero- saprophytic microorganisms because of a high input ofphores were estimated by the Csaky test (Csaky 1948). organic materials derived from the plant roots and root exudates. Previous studies have shown that diversity of actinomycetes in rhizosphere soils is positively correlatedResults and discussion to the level of organic matter and depended on the species of plant (Germida et al. 1998; Hayakawa et al. 1988; HenisActinomycete isolates from rhizosphere soils 1986). Tewtrakul and Subhadhirasakul (2007) found that the roots of Curcuma mangga produced an antimicrobialFrom 16 medicinal plant rhizosphere soils, 445 isolates of compound. It is possible that root exudates from this plantactinomycete were obtained (Table 1). About 89% of the might promote the growth of actinomycetes and antimi-isolates were presumed to be in genus Streptomyces and crobial compounds from the roots might decrease the11% were identified to the genera Acitinomadura, Micro- number of other soil bacteria and fungi so that the diversitybispora, Micromonospora, Nocardia and Nonomurea. of actinomycetes from this soil is higher than other soils.Three isolates were unidentified. Streptomyces were pres-ent in all rhizosphere soils, regardless of wild or Effect of the pretreatment approachagricultural plant species, suggesting their wide distribu-tion in association with plants in the natural environment. The number of actinomycetes isolated from soils pretreatedThe others actinomycetes were rare and could be isolated with 6% yeast extract and 0.05% SDS was higher thanfrom some rhizosphere soils. Streptomyces were the dom- from those pretreated with 1.5% phenol. Pretreatment withinant actinomycetes isolated from all 16 plant rhizosphere 6% yeast extract and 0.05% SDS increased efficiency whenTable 1 Occurrence and distribution of actinomycetes from rhizosphere soils of medicinal plantsPlant rhizosphere soil pH No. of No. of rare actinomycete isolates Streptomyces A B C D E FAcanthus ebrateatus Vahl. (sea holly) 7.30 21Achyranthes aspera L. (prickly chaff flower) 6.92 30 1 1Amaranthus gracilis Desf. (spinach) 6.93 23 1Bariena lunulina L. 6.98 17 2Boesenbergia pandurata Schl. (fingerroot) 5.80 19 1Curcuma mangga Val. and Zijp. 6.90 45 1 1 1 2 1 0Cymbopogon citratus Stapf. (lemongrass) 7.00 29 2Cymbopogon nardus Rendle. 7.00 13 3 1 (citronellagrass)Cyperus rotundus L. (cocograss) 6.38 10 1Imperata cylindrical Beauv. (cogongrass) 6.92 30 1Languas galanga L. (galangal) 6.89 22 2Ocimum sanctum L. (holy basil) 7.01 32 1 4 1Pandanus amaryllifolius Roxb. 6.87 42 1 4 (pandanus palm)Rhinacanthus nasutus Kurz. 7.09 21 1 3Stemona tuberosa Lour. (stemona) 6.93 18 1 1 4 1 2Zingiber officinale Rose. (ginger) 6.63 24 1 2Total 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 123
  • 652 World J Microbiol Biotechnol (2009) 25:649–655 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 theFig. 1 Number of actinomycete isolates using two pretreatment rhizosphere microbiota and attract more or less bacterialmethods and three media antagonists responsible for natural soil suppression. Plantisolating general actinomycetes (Hayakawa et al. 1988). root exudates stimulate growth of rhizosphere actinomy-Phenol is a biocide and toxic to actinomycetes, so treat- cetes that are strongly antagonistic to fungal pathogens,ment with 1.5% phenol reduced the number of while the actinomycetes utilize root exudates for growthactinomycetes which were sensitive to this biocide and synthesis of antimicrobial substances (Crawford et al.(Hayakawa et al. 2004). Humic acid vitamin agar was the 1993; Yuan and Crawford 1995). It is possible thatTable 2 Antifungal activities of Streptomyces isolatesStreptomyces % inhibitionaisolates Alternaria Colletotrichum Fusarium Penicillium Sclerotium brassicicola gloeosporioides oxysporum digitatum rolfsiiCMU C14-12 0 0 55.4 ± 1.2 0 0CMU Gin001 0 0 0 58.4 ± 0.8 0CMU Gin003 26.5 ± 0.7 84.6 ± 0.6 68.7 ± 0.4 62.2 ± 0.5 0CMU Gin005 0 0 0 62.3 ± 0.4 0CMU G7-2 0 0 0 69.8 ± 0.2 0CMU H001 0 0 0 58.7 ± 0.3 0CMU PA001 0 0 25 ± 0.3 0 0CMU PA101 97.5 ± 0.6 85.0 ± 0.4 74.2 ± 0.3 98.5 ± 0.8 77.5 ± 0.7CMU PA510 0 0 25 ± 0.5 45.5 ± 0.8 0CMU PA511 46.0 ± 0.4 42.9 ± 0.8 0 40 ± 0.9 0CMU PA517 40.0 ± 0.6 57.1 ± 0.8 43.7 ± 0.9 0 0CMU PA521 0 20.6 ± 0.6 0 63.9 ± 0.3 0CMU PA528 0 0 0 42.5 ± 1.1 0CMU PA531 0 0 0 44.0 ± 0.5 0CMU PA529 0 28.6 ± 0.5 0 0 0CMU PA537 49.0 ± 0.5 0 0 0 0CMU PA533 0 42.9 ± 1.1 0 0 0CMU PA539 0 42.9 ± 0.7 0 0 0CMU SK126 69.9 ± 0.9 70.0 ± 0.5 77.5 ± 0.4 55.0 ± 0.2 68.8 ± 1.0CMU SK132 0 0 0 39.9 ± 0.8 0CMU UK102 0 0 25.0 ± 0.4 0 0CMU W110 0 0 37.5 ± 0.3 0 0CMU X209 0 0 25.0 ± 0.4 0 0a Average ± standard error from triplicate samples123
  • World J Microbiol Biotechnol (2009) 25:649–655 653excretions from the roots of pandanus palm might induce et al. (2007) isolated Streptomyces from medicinal plantactinomycetes that show anti-fungal activity. Two isolates, rhizosphere soils and 8 isolates had antipathogenic activity.Streptomyces CMU-PA101 (accession number FJ025786) Crawford et al. (1993) found that 12 actinomycete strainsfrom P. amaryllifolius rhizosphere and Streptomyces isolated from Taraxicum officinale rhizosphere were activeCMU-SK126 (accession number FJ217218) from against Pythium ultimum. Although 89.5% of the Strepto-C. mangga rhizosphere, strongly inhibited all of the path- myces isolates in this study did not show any antifungalogenic fungi (Fig. 2). The 16SrRNA gene sequences of activity towards the test organisms, they might produceStreptomyces CMU-PA101 and Streptomyces CMU-SK126 other useful compounds.were similar to Streptomyces spectabilis (99% identity) andStreptomyces cinnamoneus (99% identity). Similar studieshave been carried out by other workers. Ouhdouch andBarakate (2001) found 10 isolates of actinomycetes from Table 3 IAA production by actinomycete isolates after 7 daysmedicinal plant rhizosphere soils, most of which were incubationStreptomyces spp. After testing for antifungal activity Genus Isolates IAA production (lg/ml)aagainst Candida albicans and C. tropicalis, they found thatall Streptomyces had antifungal activity. Thangapandian 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 CMU-Gin003 53.79 ± 0.5 Streptomyces CMU-Gin004 16.85 ± 0.9 Streptomyces CMU-Gin006 36.61 ± 0.2 Streptomyces CMUG-I 13.64 ± 0.5 Streptomyces CMU-H009 143.95 ± 0.2 Streptomyces CMU-H011 26.80 ± 1.8 Streptomyces CMU-K101 13.23 ± 0.2 Streptomyces CMU-K101 13.19 ± 0.3 Streptomyces CMU-K201 12.32 ± 1.8 Streptomyces CMU-K202 18.06 ± 0.3 Streptomyces CMU-K204 11.65 ± 0.7 Streptomyces CMU-L105 14.60 ± 0.5 Streptomyces CMU-PA101 28.86 ± 0.3 Streptomyces CMU-PA203 31.88 ± 0.2 Streptomyces CMU-PA301 19.09 ± 0.8 Streptomyces CMU-PA524 20.39 ± 0.7 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 ± 0.3Fig. 2 Zones of growth inhibition caused by metabolites from Streptomyces CMU-VAN301 29.34 ± 0.4Streptomyces CMU PA101, grown on potato dextrose agar for Streptomyces CMU-VAN307 16.01 ± 0.314 days, against a Fusarium oxysporum b Sclerotium sp. c Collet- Streptomyces CMU-X208 11.03 ± 0.2otrichum gloeosporioides. Left, control; right, in the presence of aStreptomyces CMU PA101 Average ± standard error from triplicate samples 123
  • 654 World J Microbiol Biotechnol (2009) 25:649–655Table 4 Siderophore- CAS-positive Genusproducing actinimycete isolates Halo diameter Streptomyces Actinomadura Microbispora Nocardia ???? 6(3%) 0(0%) 0(0%) 0(0%) ??? 4(2%) 1(0.5%) 0(0%) 0(0%) ?? 8(4%) 0(0%) 1(0.5%) 3(1.5%) ? 20(10%) 2(1.0%) 0(0%) 1(0.5%)?, 10 mm; ??, 10–20 mm; Not active 136(68%) 1(0.5%) 1(0.5%) 16(8.0%)???, 21–30 mm; ????, Total 174(87%) 4(2%) 2(1%) 20(10%)[30 mmIndole acetic acid (IAA) and siderophore production Table 5 Siderophore production by active actinomycete isolates after 10 daysThirty-six (8.1%) of actinomycete isolates produced IAA, Actinomycetes Catechols Hydroxamateand 30 of these were Streptomyces sp. (Table 3). The (lg/ml)a (lg/ml)arange of IAA production was 5.5–144 lg/ml. Streptomy- Actinomadura CMU-Y218 3.94 ± 0.9 20.0 ± 0.2ces CMU-H009 (accession number FJ185171) isolated Streptomyces CMU-A104 52.42 ± 0.3from lemongrass (Cymbopogon citrates) showed highability to produce IAA. The 16SrRNA gene sequence was Streptomycete CMU-AT204 6.97 ± 0.6found to be 99% identical, to Streptomyces viridis. El- Streptomyces CMU-GIN004 7.84 ± 0.1 10.00 ± 0.5Tarabilya and Sivasithamparamb (2006) and Tsavkelova Streptomyces CMU-H009 32.73 ± 0.9et al. (2006) found that Streptomyces from many crop Streptomyces CMU-K203 12.42 ± 0.7rhizosphere soils have the ability to produce IAA and Streptomyces CMU-L206 26.97 ± 1.0promoted plant growth. In the rhizosphere soils, root Streptomyces CMU-PA101 21.82 ± 0.4exudates are the natural source of tryptophan for rhizo- Streptomyces CMU-SK107 25.76 ± 0.3sphere micro-organisms, which may enhance auxin Streptomyces CMU-SK126 16.19 ± 0.5 54.85 ± 1.2biosynthesis in the rhizosphere. It is possible that high Streptomyces CMU-VAN301 14.85 ± 0.7tryptophan will be present in root exudates of lemongrass a Average ± standard error from triplicate samplesand enhance IAA biosynthesis in Streptomyces CMU-H009. Siderophore production were found in 45 (27.5%)of all actinomycete isolates. The active isolates grew on From the present study, it could be demonstrated thatCAS agar and an orange halo formed around the colonies. rhizosphere soil from Curcuma mangga provided a richMost of them were Streptomyces (Table 4). Streptomyces source of diversity of actinomycetes. Streptomyces CMU-CMU-SK126 isolated from C. mangga rhizosphere soil PA101, Streptomyces CMU-SK126 and Streptomycesshowed high ability to produce siderophores. This isolate CMU-H009 had the ability to produce high antifungalproduced catechols 16.19 lg/ml and hydroxamate compounds, siderophore and IAA. However, more detailed54.9 lg/ml on modified Gaus No.1 broth (Table 5). investigation is required to demonstrate the potential ofUsually, siderophores are produced by various soil these organisms for the biocontrol of pathogenic fungi andmicrobes to bind Fe3? from the environment, transport it in plant growth promotion which may be useful in phar-back to the microbial cell and make it available for macological and agricultural fields in the future.growth (Leong 1996; Neilands and Leong 1986). Micro-bial siderophores may also be utilized by plants as an iron Acknowledgments This work was supported by The Royal Golden Jubilee Ph.D. Program (PHD/0153/2546). We are grateful to Dr. Ericsource (Bar-Ness et al. 1991; Wang et al. 1993). Rhizo- H. C McKenzie (Landcare Research, Private Bag 92170, Auckland,sphere soil actinomycetes have to compete with other New Zealand) for improving the English text.rhizosphere bacteria and fungi for iron supply andtherefore siderophore production may be very importantfor their growth. Competition for iron is also a possible Referencesmechanism to control the phytopathogens. Soil Strepto-myces have been reported to produce hydroxamate-type Arnow LE (1937) Colorimetric estimation of the components of 3,4-siderophores that could inhibit the growth of phytopath- dihydroxy phenylalanine tyrosine mixtures. J Biol Chemogens by competition for iron in plant rhizosphere soils 118:531–535(Muller et al. 1984; Muller and Raymond 1984; Tokala Atalan E, Manfio GP, Ward AC, Kroppenstedt RM, Goodfellow M (2000) Biosystematic studies on novel Streptomycetes from soil.et al. 2002). Antonie Van Leeuwenhoek 77:337–353123
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