Volatile-mediated interactions between phylogenetically different soil bacteria

Abstract

There is increasing evidence that organic volatiles play an important role in interactions between micro-organisms in the porous soil matrix. Here we report that volatile compounds emitted by different soil bacteria can affect the growth, antibiotic production and gene expression of the soil bacterium Pseudomonas fluorescens Pf0–1. We applied a novel cultivation approach that mimics the natural nutritional heterogeneity in soil in which P. fluorescens grown on nutrient-limited agar was exposed to volatiles produced by 4 phylogenetically different bacterial isolates (Collimonas pratensis, Serratia plymuthica, Paenibacillus sp., and Pedobacter sp.) growing in sand containing artificial root exudates. Contrary to our expectation, the produced volatiles stimulated rather than inhibited the growth of P. fluorescens. A genome-wide, microarray-based analysis revealed that volatiles of all four bacterial strains affected gene expression of P. fluorescens, but with a different pattern of gene expression for each strain. Based on the annotation of the differently expressed genes, bacterial volatiles appear to induce a chemotactic motility response in P. fluorescens, but also an oxidative stress response. A more detailed study revealed that volatiles produced by C. pratensis triggered, antimicrobial secondary metabolite production in P. fluorescens. Our results indicate that bacterial volatiles can have an important role in communication, trophic - and antagonistic interactions within the soil bacterial community.

Volatile affairs in microbial interactions

“…Compared with diffusible compounds, volatile compounds can travel faster and over longer distances through both the liquid and gaseous phase of the soil (Insam and Seewald, 2010;Effmert et al, 2012), which facilitate the interactions between soil microorganisms. Therefore, volatiles have an important role in the communication and competitiveness between physically separated soil microorganisms (Kai et al, 2009;Effmert et al, 2012;Garbeva et al, 2014a). It is plausible that in soil, dormant microorganisms can sense changes in their environments via emitted volatiles and change their behaviour accordingly and in turn, influence the behaviour of other soil microorganisms (Garbeva et al, 2011).…”

“…Screenings of commonly produced volatiles with antimicrobial activity often did not reveal antibacterial activity (Schulz et al, 2010). Moreover, volatiles with strong antifungal activity (such as dimethyl disulphide, dimethyl trisulphide, S-methyl thioacetate and benzonitrile) did not exhibit antibacterial effects and even stimulated the growth of some bacteria (Garbeva et al, 2014a). However, some specific volatiles produced by only a few microorganisms have been indicated as potential antibacterial agents.…”

“…Among these common, differentially expressed genes was the Pfl_0064 catalase, an important enzyme that protects the cell against damage by reactive oxygen species (Lushchak, 2001). Furthermore, the volatiles produced by C. pratensis triggered the production of antimicrobial secondary metabolites (Garbeva et al, 2014a).…”

Intra- and inter-species interactions in microbial communities

“…Garbeva et al (2014) report the first experimental study indeed proving antibiotic production levels and gene expression changes in one bacterial species, Pseudomonas fluorescens Pf0-1, as a consequence of the exposure to volatiles produced by four different species. In these cases microbes are in direct contact, confined in a structured space, which they can alter to some degree, and to which they must adapt too.…”

Rapid mineralization of biogenic volatile organic compounds in temperate and Arctic soils

“…Production of BVOCs in soil (McNeal and Herbert, 2009;Ramirez et al, 2010) and by isolated soil microorganisms (Insam and Seewald, 2010;Garbeva et al, 2014) has been shown as well, though.…”