Paenibacillus Polymyxa: Antibiotics, Hydrolytic Enzymes and Hazard Assessment

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Paenibacillus Polymyxa: Antibiotics, Hydrolytic Enzymes and Hazard Assessment 002_OfferedReview_419 13-11-2008 14:35 Pagina 419 Journal of Plant Pathology (2008), 90 (3), 419-430 Edizioni ETS Pisa, 2008 419 OFFERED REVIEW PAENIBACILLUS POLYMYXA: ANTIBIOTICS, HYDROLYTIC ENZYMES AND HAZARD ASSESSMENT W. Raza, W. Yang and Q-R. Shen 1 College of Resource and Environmental Sciences, Nanjing Agriculture University, Nanjing, 210095, Jiangsu Province, P.R. China SUMMARY pressing several plant diseases and promoting plant growth (Benedict and Langlykke, 1947; Ryu and Park, Certain Paenibacillus polymyxa strains that associate 1997). These strains have been isolated from the rhizos- with many plant species have been used effectively in phere of a variety of crops like wheat (Triticum aes- the control of plant pathogenic fungi and bacteria. In tivum), barley (Hordeum gramineae) (Lindberg and this article we review the possible mechanism of action Granhall, 1984), white clover (Trifolium repens), peren- by which P. polymyxa promotes plant growth and sup- nial ryegrass (Lolium perenne), crested wheatgrass presses some plant diseases. Furthermore we present an (Agropyron cristatum) (Holl et al., 1988), lodgepole pine updated summary of antibiotics, autolysis, hydrolytic (Pinus contorta latifolia) (Holl and Chanway, 1992), and autolytic enzymes and levanase produced by this Douglas fir (Pseudotsuga menziesii) (Shishido et al., bacterium. Some hazards and mild pathogenic effects 1996), green bean (Phaseolus vulgaris) (Petersen et al., are also reported, but these appear to be strain-specific 1996) and garlic (Allium sativum ) (Kajimura and Kane- and negligible. The association between plants and P. da, 1996). P. polymyxa has been successfully used to con- polymyxa seems to be specific and to involve co-adapta- trol Botrytis cinerea, the causal agent of grey mould, in tion processes. There is every reason to believe that strawberries (Helbig, 2001), Fusarium oxysporum and gaining an improved understanding of these processes Pythium spp. causal agents of seedling blight, wilt and will enhance and facilitate efforts to wean off farmers root rot of cucumber and water melon (Yang et al., 2004; dependence on a wide range of agricultural chemicals. Dijksterhuis et al., 1999) sesame damping off (Ryu et al., 2006), and to control diseases of arabidopsis caused by Key words: rhizosphere, plant association, plant Phytophthora palmivora and Pythium aphanidermatum growth promotion, enzymes. (Timmusk and Wagner, 1999). P. polymyxa is known to produce two types of peptide antibiotics, one type is on- ly active against bacteria and the other is active against INTRODUCTION fungi, gram positive bacteria and actinomycetes (Beatty and Jensen, 2002). This species also synthesizes plant Among the myriads of bacteria thriving in the plant hormones auxin (Lebuhn et al., 1997) and cytokinin rhizosphere, some spore-forming plant-growth-promot- (Timmusk et al., 1999), solubilizes soil phosphorus ing rhizobacteria (PGPR), in particular gram-positive (Singh and Singh, 1993), enhances soil porosity (Gouzou bacilli and streptomycetes, attracted special attention et al., 1993) and has been used for flocculation and flota- due to their advantages over non-spore formers in prod- tion of various minerals (Deo and Natarajan, 1998). P. uct formulation and stable maintenance in soil (Emmert polymyxa spores cause sporangium deformation and and Handelsman, 1999). Among these, the genus Paeni- have thick walls with a star-shaped section. These can re- bacillus (species of a genus previously included in the main in a dormant state for long periods, being resistant genus Bacillus, Ash et al., 1993; Truper, 2005), compris- to heat, drying, radiation and toxic chemicals (Comas- es more than eighty-nine species up to the time of writ- Riu and Vives-Rego, 2002). This antagonistic potential is ing this article (February 2008). Paenibacillus species the base for effective applications of P. polymyxa strains are facultatively anaerobic, endospore-forming, low as an alternative to the chemical control against a wide G+C Gram-positive bacilli (http://www.bacterio.cict.fr/ set of fungal and bacterial plant pathogens. p/paenibacillus). Strains of Paenibacillus polymyxa (the The aim of this review is to evaluate and discuss the type species of genus), were found to be capable of sup- possible updated mechanisms that enable P. polymyxa strains to control a variety of pathogens that invade plants. This review also covers the effective use of these Corresponding author: Q-R. Shen Fax: +86-25-84431492 strains as biofertilizer and eventual hazards, if any, E-mail: [email protected] caused by P. polymyxa. 002_OfferedReview_419 13-11-2008 14:35 Pagina 420 420 Properties and hazard assessment of P. polymyxa Journal of Plant Pathology (2008), 90 (3), 419-430 Fig. 1. A. Scanning electron micrograph of cells of Paenibacillus polymyxa isolate B2 (Timmusk et al., 2003). Whole view (B) and cross- section C) of P. polymyxa spores (Dondero and Holbert, 1957). Bar = 2 µm. ANTIBIOTIC COMPOUNDS isms. The first member of the polymyxin family, polymyxin B, was discovered in 1947 (Ainsworth et al., The main type of peptide antibiotics produced by 1947; Stansly et al., 1947). Since then, at least 15 differ- some but not all strains of P. polymyxa is the polymyxin- ent polymyxins have been discovered in diverse bacteri- colistin-circulin family (Shoji et al., 1977a, 1977b, al species, but the genetic control of their biosynthesis 1977c; Umezawa et al., 1978). Other strains produce has been described only in part. The general structure different peptides, including polypeptins (Doi and Mc- of polymyxins includes a cyclic heptapeptide moiety at- Gloughlin, 1992), jolipeptin (Ito and Koyama, 1972a, tached to a tripeptide side chain with fatty acyl residues 1972b), gatavalin (Nakajima et al., 1972), gavaserin on the N-terminal amino group (Fig. 2). Polymyxins can (Pichard et al., 1995), saltavidin (Pichard et al., 1995), be distinguished from each other by differences in fusaricidins (Kajimura and Kaneda, 1996, 1997) and amino acid or fatty acid composition (Orwa et al., polyxin (Piuri et al., 1998). In addition, P. polymyxa 2002). Polymyxin B and polymyxin E (colistin) have NRRL-B-30509 secreted bacteriocin which reduced been extensively characterized and are being used as both levels and frequency of chick colonization by sulfate, sulfomethylated or colistimethate forms of med- Campylobacter jejuni (Stern et al., 2005; Svetoch et al., 2005). P. polymyxa also produced some antimicrobial and antifungal compounds whose nature remained until now undefined (Rosado and Seldin, 1993; Oedjijono et al., 1993; Liang et al., 1996; Dijksterhuis et al., 1999). Pathogen (mainly fungi) suppression takes place by means of an interaction process, in which the presence of living bacteria is a prerequisite for continuous sup- pression. It was found that anti-fungal compounds pro- duced by the bacteria were counteracted by magnesium ions (Dijksterhuis et al., 1999). Polymyxin-Colistin-Circulin Family Polymyxins have a bactericidal effect on Gram-nega- tive bacilli, especially Pseudomonas and coliform organ- Fig. 2. General structure of polymyxins. 002_OfferedReview_419 13-11-2008 14:35 Pagina 421 Journal of Plant Pathology (2008), 90 (3), 419-430 Raza et al. 421 icines especially for infections caused by Gram-negative 219 protoplasts is immediately initiated by the addition bacteria. The major types of polymyxin B are polymyxin of jolipeptin, but not by colistin, even at higher concen- B1- B6 (Thomas et al., 1980; Orwa et al., 2001). Anoth- trations, which, however, lyses spheroplasts of Gram- er minor type described so far, is isoleucine-polymyxin negative bacteria. Colistin is inactivated by Nagarse and B1 (Elverdam et al., 1981). Polymyxin E is effective colistinase, which have no effect on jolipeptin (Ito and against Gram-negative bacilli, except Proteus. The ma- Koyama, 1972a, 1972b). jor types of polymyxin E are polymyxin E1 and E2. Mi- Polyxin is a proteinaceous factor with a bacteriolytic nor types include polymyxins E3, E4 and E7 (Thomas effect on Gram-positive bacteria, and bacteriostatic ef- et al., 1980; Orwa et al., 2001), norvalinepolymyxin E1, fect on actively growing Gram-negative cells (Piuri et valine-polymyxin E2 (Elverdam et al., 1981), valine- al., 1998). These differences in reaction of polyxin be- polymyxin E1, isoleucine-polymyxin E1, isoleucine- tween the two classes of organisms might depend on polymyxin E2 (Ikai et al., 1998) and isoleucine- differences in cell wall structure. polymyxin E8 (Orwa et al., 2001). Polymyxins alter cytoplasmic membrane permeability Polymyxin A, B, C and D have differences of little sig- by binding to a negatively charged site in the nificance in the molecular weights but at high surface lipopolysaccharide layer that has an electrostatic attrac- concentration. The characteristics of their unimolecular tion for the positively charged amino groups in the films when spread at the air-water interface on concen- cyclic peptide portion. The polymyxin fatty acid moiety trated salt solution, can classify polymyxins according to dissolves in the hydrophobic region of the membranes the compressibility, collapse pressures and electrical and disrupts their integrity. This causes leakage of cellu- properties. In these respects, polymyxins A and D have lar molecules, inhibition of cellular respiration and identical force-area curve values whilst films of polymyx- binding and inactivation of endotoxin (Teuber and Bad- in B only appear to be slightly more closely packed
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