Abstract
The release of zoospores from sporangia and motility of the released zoospores are critical in the disease cycle of the Peronosporomycetes that cause devastating diseases in plants, fishes, animals and humans. Disruption of any of these asexual life stages eliminates the possibility of pathogenesis. In the course of screening novel bioactive secondary metabolites, we found that extracts of some strains of marine Streptomyces spp. rapidly impaired motility and caused subsequent lysis of zoospores of the grapevine downy mildew pathogen Plasmopara viticola at 10 μg/ml. We tested a number of secondary metabolites previously isolated from these strains and found that macrotetrolide antibiotics such as nonactin, monactin, dinactin and trinactin, and nactic acids such as (+)-nonactic acid, (+)-homonactic acid, nonactic acid methyl ester, homonactic acid methyl ester, bonactin and feigrisolide C impaired motility and caused subsequent lysis of P. viticola zoospores in a dose- and time-dependent manners with dinactin being the most active compound (MIC 0.3 μg/ml). A cation channel-forming compound, gramicidin, and a carrier of monovalent cations, nigericin also showed similar biological activities. Among all 12 compounds tested, gramicidin most potently arrested the motility of zoospores at concentrations starting from 0.1 μg/ml. All macrotetrolide antibiotics also displayed similar motility impairing activities against P. viticola, Phytophthora capsici, and Aphanomyces cochlioides zoospores indicating non-specific biological effects of these compounds toward peronosporomyctes. Furthermore, macrotetrolide antibiotics and gramicidin also markedly suppressed the release of zoospores from sporangia of P. viticola in a dose-dependent manner. As macrotetrolide antibiotics and gramicidin are known as enhancers of mitochondrial ATPase activity, inhibition of zoosporogenesis and motility of zoospores by these compounds are likely linked with hydrolysis of ATP through enhanced ATPase activity in mitochondria. This is the first report on motility inhibitory and lytic activities of macrotetrolide antibiotics and nactic acids against the zoospores of peronosporomycete phytopathogens.
Highlights
The Peronosporomycete genera such as Plasmopara, Phytophthora, Pythium, and Aphanomyces are notorious pathogens of plants, fishes and vertebrates (Agrios, 1997)
The antibiotic activity of the crude extracts of strains Act 8970, B6167, B7857, Act7619, and Gt2005/2009 was due to the presence of macrotetrolide antibiotics as dinactin and nactic acids displayed identical motility inhibitory and lytic activities against the zoospores in a dose- and time-dependant manners
To see whether the inhibitory activities of macrotetrolides and nactic acids are specific to P. viticola or general to other economically important phytopathogenic peronosporomycetes, we included a damping-off pathogen of sugar beet and spinach, Aphanomyces cochlioides and a late blight pathogen of chili and several vegetables, Phytophthora capsici
Summary
The Peronosporomycete genera such as Plasmopara, Phytophthora, Pythium, and Aphanomyces are notorious pathogens of plants, fishes and vertebrates (Agrios, 1997). One of the unique features of the peronosporomycete pathogens is that in favorable environment they asexually produce motile zoospores from sporangia that develop at the tip of branched sporangiophores (Judelson and Blanco, 2005). The release of zoospores from sporangia (zoosporogenesis) involves cleavage of the sporangial cytoplasm by nucleus-enveloping membrane networks and an assembly of two flagellae per zoospore (Hardham and Hyde, 1997). Inhibition of enzymes that maintain ATP concentration, or shuttling of ATP from mitochondria to sites of high utilization such as flagellar kinetosomes of zoospores or depletion of ATP by enhancement of ATPase activity would result in impairment of motility of zoospores and suppression of zoosporogenesis (Judelson and Blanco, 2005)
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