Production of ammonia as a low-cost and long-distance antibiotic strategy by Streptomyces species

Abstract

Soil-inhabiting streptomycetes are nature’s medicine makers, producing over half of all known antibiotics and many other bioactive natural products. However, these bacteria also produce many volatiles, molecules that disperse through the soil matrix and may impact other (micro)organisms from a distance. Here, we show that soil- and surface-grown streptomycetes have the ability to kill bacteria over long distances via air-borne antibiosis. Our research shows that streptomycetes do so by producing surprisingly high amounts of the low-cost volatile ammonia, dispersing over long distances to inhibit the growth of Gram-positive and Gram-negative bacteria. Glycine is required as precursor to produce ammonia, and inactivation of the glycine cleavage system nullified ammonia biosynthesis and concomitantly air-borne antibiosis. Reduced expression of the porin master regulator OmpR and its cognate kinase EnvZ is used as a resistance strategy by E. coli cells to survive ammonia-mediated antibiosis. Finally, ammonia was shown to enhance the activity of canonical antibiotics, suggesting that streptomycetes adopt a low-cost strategy to sensitize competitors for antibiosis from a distance.

Scent of a Killer: Microbial Volatilome and Its Role in the Biological Control of Plant Pathogens

“…Inorganic volatile molecules such as CO, CO 2 , H 2 , N 2, O 2 , NH 3 , H 2 S, NO 2 -, SO 2 , SO 3 , and HCN are the most relevant and are involved in a wide variety of biological functions ranging from electron acceptors/ donor to acting as defense compound (Effmert et al, 2012). Moreover, a role in the interspecies communication (e.g., quorum sensing/quenching) and antibiotic resistance has been recently proved (Schmidt et al, 2015;Avalos et al, 2019). By acknowledging the important role of inorganic volatile metabolites under diverse biological and ecological aspects, the current review deals mainly with volatile organic compounds of microbial origin and their role in biological control of plant pathogens.…”

Fungal volatiles mediate cheese rind microbiome assembly

“…Therefore, the ecological relevance of VOCs in driving pairwise microbial interactions and microbial community assembly is still unresolved. It is possible that VOCs could promote the growth of poor competitors or inhibit the growth of a dominant species allowing subdominant species to thrive (Jones et al ., 2019; Avalos et al ., 2020), but we are unaware of examples where VOCs have been demonstrated to control the assembly of multispecies communities.…”

The Streptomyces coelicolor Small ORF trpM Stimulates Growth and Morphological Development and Exerts Opposite Effects on Actinorhodin and Calcium-Dependent Antibiotic Production

“…Indeed, glutamate/glutamine and arginine play a key role in nitrogen assimilation (Lu, 2006;Lewis et al, 2011) and their down-representation could account for an increased amount of free ammonium causing medium alkalinization. In addition, it has been recently reported that different Streptomyces species, including S. coelicolor, are able to produce ammonia in presence of higher levels of glycine, exerting (i) an antimicrobial activity and (ii) reinforcing the efficiency of other antibiotics through perturbation of membrane permeability in target cells (Avalos et al, 2019). At this regard, it would be interesting to clarify the role of GlyA, which converts serine in glycine, and its putative interplay with TrpM.…”