Rescue of morphological defects in Streptomyces venezuelae by the alkaline volatile compound trimethylamine

Abstract

ABSTRACT Microorganisms can produce a vast diversity of volatile organic compounds of different chemical classes that are capable of mediating intra- and inter-kingdom interactions. In this study, we showed that the soil-dwelling bacterium Streptomyces venezuelae can produce alkaline volatiles under multiple growth conditions, which we discovered through investigation of the S. venezuelae mutant strain MU-1. Strain MU-1 has a defective morphology and exhibits a bald phenotype due to the lack of aerial mycelia and spores, as confirmed by scanning electron microscopy. Using physical barriers to separate the strains on culture plates, we determined that volatile compounds produced by wild-type S. venezuelae could rescue the phenotype of strain MU-1, and pH analysis of the growth medium indicated that these volatile compounds were alkaline. Ultra-high-performance liquid chromatography, combined with mass spectrometry analysis, showed that wild-type S. venezuelae produced abundant levels of the alkaline volatile trimethylamine (TMA) and the oxide form TMAO; however, the levels of these compounds were much lower in strain MU-1. Notably, exposure to TMA alone could rescue the phenotype of this mutant strain, restoring the production of aerial mycelia and spores. We also showed that the rescue effect by alkaline volatiles is mostly species-specific, suggesting that the volatiles may aid particular mutants or other less-fit variants of closely related species to resume normal physiological status and to compete more effectively in complex communities such as soil. Our study reveals a new and intriguing role for bacterial volatiles, including volatiles that may have toxic effects on other species. IMPORTANCE Bacterial volatiles have a wide range of biological roles at intra- or inter-kingdom levels. The impact of volatiles has mainly been observed between producing bacteria and recipient bacteria, mostly of different species. In this study, we report that the wild-type, soil-dwelling bacterium Streptomyces venezuelae , which forms aerial hypha and spores as part of its normal developmental cycle, also produces the alkaline volatile compound trimethylamine (TMA) under multiple growth conditions. We showed that the environmental dispersion of TMA produced by S. venezuelae promotes the growth and differentiation of growth-deficient mutants of the same species or other slowly growing Streptomyces bacteria, and thus aids in their survival and their ability to compete in complex environmental communities such as soil. Our novel findings suggest a potentially profound biological role for volatile compounds in the growth and survival of communities of volatile-producing Streptomyces species.