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African Crop Science Journal by African Crop Science Society Is Licensed Under a Creative Commons Attribution 3.0 Uganda License African Crop Science Journal, Vol. 28, No. 4, pp. 555 - 566 ISSN 1021-9730/2020 $4.00 Printed in Uganda. All rights reserved © 2020, African Crop Science Society African Crop Science Journal by African Crop Science Society is licensed under a Creative Commons Attribution 3.0 Uganda License. Based on a work at www.ajol.info/ and www.bioline.org.br/cs DOI: https://dx.doi.org/10.4314/acsj.v28i4.6 MORPHOLOGICAL AND MOLECULAR CHARACTERISATION OF Streptomyces spp. WHICH SUPPRESS PATHOGENIC FUNGI N. GOREDEMA, T. NDOWORA, R. SHOKO and E. NGADZE1 Chinhoyi University of Technology, Private Bag 7724, Chinhoyi, Zimbabwe 1University of Zimbabwe, P. O. Box MP 167 Mt. Pleasant, Harare, Zimbabwe Corresponding author: [email protected] (Received 26 September 2019; accepted 2 October 2020) ABSTRACT Streptomyces species are aerobes and chemoorganotrophic bacteria. These microorganisms produce a wide range of industrially significant compounds, specifically antibiotics and anti fungal substances. The objective of this study was to characterise soil-borne Streptomyces isolates using morphological and molecular traits in order to identify them to species level, and leverage from their potential to suppress the growth of Aspergillus flavus, Fusarium oxysporum and Penicillium italicum. Twenty- seven soil-borne putative Streptomyces, which elicited comprehensive antimicrobial activity against Aspergillus flavus, Fusarium oxysporum and Penicillium italicum, in a previous study, were evaluated. On the basis of morphology, the bacteria resembled the genus Streptomyces. Initially, colonies phenotypically appeared to have a relatively smooth surface but as growth progressed the bacteria developed a weft of aerial mycelium granular, powdery or velvety in appearance. Bacteria produced a wide variety of pigments which in turn were responsible for the colour of the vegetative and aerial mycelia, colour ranged from white to cream or buff shades and yellow to orange or brown. Microscopic analyses and morphological characteristics generated sub-groups of the isolates and clustered them according to their similarities. One bacterial strain was randomly selected from each cluster and investigated using molecular characteristics. Partial 16S rDNAs from the selected representative isolates from each subgroup, were sequenced and phylogenetic analysis performed. The 16S rDNA sequences of the isolates indicated that they were related to Streptomyces species: S. bungoensis, S. thermocarboxydus, S. corchorusii and S. lasaliensis, that are known secondary metabolite producers possessing antimicrobial activity against plant pathogens. Key Words: Antimicrobial activity, phylogenetic analysis, secondary metabolites RÉSUMÉ Les espèces de Streptomyces sont des bactéries aérobies et chimio-organotrophes. Ces micro- organismes produisent une large gamme de composés d’importance industrielle, en particulier des antibiotiques et des substances antifongiques. L’objectif de cette étude était de caractériser les isolats de Streptomyces transmis par le sol à l’aide de traits morphologiques et moléculaires afin de les 556 N. GOREDEMA et al. identifier au niveau de l’espèce, et de tirer parti de leur potentiel à supprimer la croissance d’Aspergillus flavus, Fusarium oxysporum et Penicillium italicum. Vingt-sept Streptomyces putatifs transmis par le sol, qui ont suscité une activité antimicrobienne complète contre Aspergillus flavus, Fusarium oxysporum et Penicillium italicum, dans une étude précédente, ont été évalués. Sur la base de la morphologie, les bactéries ressemblaient au genre Streptomyces. Au départ, les colonies semblaient phénotypiquement avoir une surface relativement lisse, mais au fur et à mesure que la croissance progressait, les bactéries développaient une trame de mycélium aérien d’aspect granuleux, poudreux ou velouté. Les bactéries produisaient une grande variété de pigments qui à leur tour étaient responsables de la couleur des mycéliums végétatifs et aériens, la couleur variait du blanc au crème ou au chamois et du jaune à l’orange ou au brun. Des analyses microscopiques et des caractéristiques morphologiques ont généré des sous-groupes d’isolats et les ont regroupés en fonction de leurs similitudes. Une souche bactérienne a été sélectionnée au hasard dans chaque groupe et étudiée en utilisant des caractéristiques moléculaires. Des ADNr 16S partiels provenant des isolats représentatifs sélectionnés de chaque sous-groupe ont été séquencés et une analyse phylogénétique a été effectuée. Les séquences d’ADNr 16S des isolats ont indiqué qu’ils étaient apparentés aux espèces de Streptomyces: S. bungoensis, S. thermocarboxydus, S. corchorusii et S. lasaliensis, qui sont des producteurs de métabolites secondaires connus possédant une activité antimicrobienne contre les phytopathogènes. Mots Clés: activité antimicrobienne, analyse phylogénétique, métabolites secondaires INTRODUCTION small filaments and spores, which usually have a diameter of 1 µm or less (Willemse et al., Streptomyces, previously termed Actinomyces, 2011). Streptomyces colonies are slow-growing was discovered by Waksman and Henrici and in most cases, they release a soil-like odour (1943). These were later extensively studied attributed to the production of geosmin a and found to be spore-forming, Gram-positive volatile metabolite (Jüttner and Watson, 2007). bacteria with a filamentous form (Compant et Initially, Streptomyces colonies phenotypically al., 2005). Streptomyces is a genus of over appear to have a relatively smooth surface, but 500 species of Gram-positive bacteria in the as growth progresses, they develop a weft of phylum Actinobacteria, order Streptomycetales aerial mycelium visually different, and may be and family Streptomycetaceae. Phylum granular, powdery or velvety in appearance Actinobacteria to which Streptomyces belong (Ambarwati et al., 2012). is one of the largest taxonomic units among Streptomyces are ubiquitous in soil habitats all the 18 major lineages of studied bacteria and aquatic sediments (Gontang et al., 2007). (Ludwig, 2012). Over time, the taxonomy of They are widely distributed and abundant in Actinobacteria has evolved significantly as soil, predominantly in composts and decaying more bacteria are being studied. The order in vegetation. which Streptomyces belong, Actinomycetales, Streptomycetes are also capable of was established in 1917 by Buchanan. degrading cellulose, lignocellulose, chitin and Streptomyces species are aerobes and many other organic compounds in chemoorganotrophic bacteria. These biogeochemical cycles (Lewin et al., 2012). microorganisms produce a wide range of Streptomyces degrade adenine, casein, esculin, industrially significant compounds, specifically gelatin, hypoxanthine, starch, and ltyrosine antibiotics and anti-fungal substances (Berdy, (Smaoui et al., 2011). They also are catalase 2012; Compant et al., 2016). Their genomes positive and have the ability to reduce nitrates have a high GC content of about 70-78% to nitrites (Smaoui, et al., 2011). Within the (Kavitha et al., 2010). Streptomyces have very temperature range of 25 – 35 °C and a pH in Morphological and molecular characterisation of Streptomyces spp. 557 the neutral range 6.5 - 8 Streptomyces grow category was given a number from 0-5 best. They occur in the same habitats as fungi depending on the number of sub categories (Ikeda et al., 2003). within a specific group. The growth rates of Streptomyces produce a variety of pigments, Streptomyces isolates were determined by which in turn are responsible for the colour measuring their radii on the agar plate, relative of the vegetative and aerial mycelial to each other. There were three Streptomyces appearance (Flärdh et al., 2009). Their colour isolates with growth rate categories with the ranges from white to cream or buff shades; largest diameters which were ranked as fast yellow to orange or brown; pink to cinnamon, growers; while those with the least growth red or pinkish tan to lavender; and green to were ranked as slow growers. Growth rate grey or blue. categories were assigned number from 0-2 A wide range of organic compounds are from the slowest growers to the fastest available as carbon sources for Streptomyces growers. energy and growth. Mycelia colour of Streptomyces isolates Developing zero-chemical master-plans for growing on Oatmeal Agar (OA), was assessed the control of plant pathogens is one of the visually and the four colour categories were major issues that have caught global attention yellow to orange, brown, greenish to grey, and in recent years. white to cream, with each colour category Unfortunately, only a few attempts have assigned a number from 0-3, respectively. been done so far on morphological and Mycelia texture was also visually assessed molecular characterisation of Streptomyces. and classified into three categories, which were The objective of this study was to characterise mucoid, viscid or buttery. Streptomyces spp. soil-borne Streptomyces spp. isolates, pigmentation was grouped into four categories morphological and molecular, to identify them which were colourless, white, brown and and to leverage from their potential to suppress yellow. Opacity (visible light impenetrability) the growth of Aspergillus flavus, Fusarium was categorised as opaque or translucent. oxysporum and Penicillium italicum. (Davelos et al., 2004). Surface appearance of the Streptomyces METHODOLOGY isolates was classified into three categories, namely smooth, rough or glistering. Spore Streptomyces strains. Twenty-seven
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