StreptomycesVolatile Compounds Influence Exploration and Microbial Community Dynamics by Altering Iron Availability

Abstract

Bacteria and fungi produce a wide array of volatile organic compounds (VOCs), and these can act as chemical cues or as competitive tools. Recent work has shown that the VOC trimethylamine (TMA) can promote a new form of Streptomyces growth, termed “exploration.” Here, we report that TMA also serves to alter nutrient availability in the area surrounding exploring cultures: TMA dramatically increases the environmental pH and, in doing so, reduces iron availability. This, in turn, compromises the growth of other soil bacteria and fungi. In response to this low-iron environment, Streptomyces venezuelae secretes a suite of differentially modified siderophores and upregulates genes associated with siderophore uptake. Further reducing iron levels by limiting siderophore uptake or growing cultures in the presence of iron chelators enhanced exploration. Exploration was also increased when S. venezuelae was grown in association with the related low-iron- and TMA-tolerant Amycolatopsis bacteria, due to competition for available iron. We are only beginning to appreciate the role of VOCs in natural communities. This work reveals a new role for VOCs in modulating iron levels in the environment and implies a critical role for VOCs in modulating the behavior of microbes and the makeup of their communities. It further adds a new dimension to our understanding of the interspecies interactions that influence Streptomyces exploration and highlights the importance of iron in exploration modulation. IMPORTANCE Microbial growth and community interactions are influenced by a multitude of factors. A new mode of Streptomyces growth—exploration—is promoted by interactions with the yeast Saccharomyces cerevisiae and requires the emission of trimethylamine (TMA), a pH-raising volatile compound. We show here that TMA emission also profoundly alters the environment around exploring cultures. It specifically reduces iron availability, and this in turn adversely affects the viability of surrounding microbes. Paradoxically, Streptomyces bacteria thrive in these iron-depleted niches, both rewiring their gene expression and metabolism to facilitate iron uptake and increasing their exploration rate. Growth in close proximity to other microbes adept at iron uptake also enhances exploration. Collectively, the data from this work reveal a new role for bacterial volatile compounds in modulating nutrient availability and microbial community behavior. The results further expand the repertoire of interspecies interactions and nutrient cues that impact Streptomyces exploration and provide new mechanistic insight into this unique mode of bacterial growth.

Pulcherrimin formation controls growth arrest of the Bacillus subtilis biofilm

“…In nature, the routes used for iron acquisition are highly diverse and competition between ecologically distant species is common. For instance, insect herbivores are able to hijack plant iron acquisition systems (51) and the soil bacterium Streptomyces venezuelae produces a volatile compound (trimethylamine) that enhances colonization by the bacterium through modulating iron availability (52, 53). Therefore, while there is no evidence that B. subtilis is able to use pulcherriminic acid as a siderophore, the intriguing question of how pulcherrimin is accessed and utilized in the complex soil environment remains open to multiple possibilities.…”

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.…”

Enhancement of disease resistance, growth potential, and photosynthesis in tomato (Solanum lycopersicum) by inoculation with an endophytic actinobacterium, Streptomyces thermocarboxydus strain BPSAC147

“…Among bacteria, Streptomyces alone account for more than 70% of the microbial natural products that have been documented and demonstrated to represent a potential source for the development of novel approaches for managing both biotic and abiotic stresses [19, 20, 21]. Among the bacteria, Streptomyces species are well known to produce a plethora of volatile organic compounds (VOCs) which may directly or indirectly influence the growth and gene expression of microorganism or plants [22, 23]. They are considered and recognized as ideal “infochemicals” as they can easily diffuse [24].…”