Interactions Between Myxobacteria, Plant Pathogenic Fungi, and Biocontrol Agents

Myxobacteria are gram-negative, unicellular bacteria with rod-shaped vegetative cells. They are unique among prokaryotes for using intercellular communication to engage in cooperative morphogenesis from which they produce fruiting bodies bearing resistant myxospores (5). Thick-walled myxospores are responsible for the survival of myxobacteria under unfavorable conditions such as desiccation, high temperature, and UV irradiation (17). Myxobacteria have been found worldwide in many different types of soil (5). They inhabit the topsoil, and population estimates range from 2,000 to 450,000 cells per gram of soil (5). However, only a few authors reported their presence in agricultural soils (5,24,29). Myxobacteria specialize in the biodegradation of biomacromolecules and are considered micropredators because antibiotics and/or enzymes produced by myxobacteria kill microorganisms and lyse cells from which biomacromolecules are then scavenged (5). Lytic metabolites include antibiotics, cell wall degrading enzymes, lipases, nucleases, polysaccharidases, and proteases (20). Some of these enzymes and antibiotics appear to be involved in the lysis of prey microbes as well as in autolysis or programmed cell death, which is simultaneous with myxospore development (20,21). Myxobacteria represent a rich source of bioactive secondary metabolites. Antibiotic compounds have been isolated from 55 and 95% of bacteriolytic and cellulolytic myxobacteria, respectively (18). More than 80 different basic structures and 350 structural variants have been identified from myxobacteria, placing myxobacteria in league with pseudomonads as abundant antibiotic producers (19). In contrast to pseudomonads and Bacillus spp., myxobacteria produce many different classes of antibiotics, including some that are rarely found as microbial secondary metabolites. Although many novel compounds have been isolated and are being evaluated for their clinical potential, the majority of compounds are macrocyclic lactone and lactam rings and linear cyclic peptides (18,19). One familiar antibiotic of agricultural importance, pyrrolnitrin, has been isolated from the myxobacterial species Myxococcus fulvus, Corallococcus exiguous, and Cystobacter ferrugineus (6,20). Although pyrrolnitrin production by Pseudomonas fluorescens strain BL915 is required for control of damping-off of cotton caused by Rhizoctonia solani Kühn (7), the role of its production by myxobacteria in plant disease control has not been evaluated. Although studies evaluating the role of secondary metabolites in predation of microorganisms by myxobacteria have been conducted, few studies have evaluated interactions between myxobacteria and plant pathogens. The genus Polyangium perforated and lysed the hyphae of R. solani and conidia of Cochliobolus miyabeanus Ito & Kuribay (9). Hocking and Cook (8) found that the genus Sorangium could reduce damping-off of conifer seedlings and also lyse several fungi in culture. Additionally, Fusarium roseum was inhibited by fatty acids from Myxococcus xanthus (14). Despite their ability to produce a wide range of antibiotics and to prey on an array of microorganisms, the role of myxobacteria in plant health remains relatively unexplored. The objectives of this research were to: (i) evaluate the presence of myxobacteria in agricultural soils of coastal California and on strawberry (Fragaria × ananassa Duchesne) roots; (ii) determine if fumigation with methyl bromide and chloropicrin influences myxobacterial populations; (iii) determine if myxobacteria influence the growth of important soilborne fungal plant pathogens and fungal biocontrol agents; and (iv) determine the role of secondary metabolite production and phenazine antibiotics in the protection of biological control agents from lysis by Myxococcus spp. Preliminary results of this research have been reported (4,23).