Exploring bacterial interspecific interactions for discovery of novel antimicrobial compounds

Abstract

SummaryRecent studies indicated that the production of secondary metabolites by soil bacteria can be triggered by interspecific interactions. However, little is known to date about interspecific interactions between Gram‐positive and Gram‐negative bacteria. In this study, we aimed to understand how the interspecific interaction between the Gram‐positive Paenibacillus sp. AD87 and the Gram‐negative Burkholderia sp. AD24 affects the fitness, gene expression and the production of soluble and volatile secondary metabolites of both bacteria. To obtain better insight into this interaction, transcriptome and metabolome analyses were performed. Our results revealed that the interaction between the two bacteria affected their fitness, gene expression and the production of secondary metabolites. During interaction, the growth of Paenibacillus was not affected, whereas the growth of Burkholderia was inhibited at 48 and 72 h. Transcriptome analysis revealed that the interaction between Burkholderia and Paenibacillus caused significant transcriptional changes in both bacteria as compared to the monocultures. The metabolomic analysis revealed that the interaction increased the production of specific volatile and soluble antimicrobial compounds such as 2,5‐bis(1‐methylethyl)‐pyrazine and an unknown Pederin‐like compound. The pyrazine volatile compound produced by Paenibacillus was subjected to bioassays and showed strong inhibitory activity against Burkholderia and a range of plant and human pathogens. Moreover, strong additive antimicrobial effects were observed when soluble extracts from the interacting bacteria were combined with the pure 2,5‐bis(1‐methylethyl)‐pyrazine. The results obtained in this study highlight the importance to explore bacterial interspecific interactions to discover novel secondary metabolites and to perform simultaneously metabolomics of both, soluble and volatile compounds.

Airborne medicine: bacterial volatiles and their influence on plant health

“…In particular, one specific volatile compound (i.e. 2,5‐bis(1‐methylethy)‐pyrazine) that significantly inhibited the plant pathogens R. solani and Fusarium culmorum (Tyc et al , ) was only found in the presence of this Paenibacillus strain (Schulz‐Bohm et al , ). This finding is in line with the observation that the loss of soil bacterial diversity can lead to a decline in the production of antifungal volatiles.…”

The ecological role of volatile mediated interactions belowground

“…AD21, are presented in Table S6.2. The annotation of final contigs for all bacteria were performed with a modified version of PROKKA V1.11 (Seemann 2014) and COG annotations were obtained as described by Tyc et al (2017a) and manually adapted according to available descriptions of gene functions. Annotation of the F. culmorum genome was available from a previous study (Schmidt 2017 Xia et al 2015).…”

“…Weikl et al 2016), an important biotic factor affecting the blend of bioactive VOCs released in soil is the direct interplay between soil shown that the fungal terpene 3-carene stimulated bacterial motility at low concentrations while high concentrations inhibited motility (Schmidt et al 2016). On the other hand, the biological activity of VOCs can be enhanced by synergistic effects between different volatile compounds (De Vrieze et al 2015;Mookherjee et al 2017) or volatile and non-volatile compounds (Tyc et al 2017a;Tyc et al 2017b). …”

“…Several recent studies reported that the production of certain mVOCs can be induced or suppressed during inter-specific microbial interactions (Garbeva et al 2014a;Tyc et al 2015;Piechulla et al 2017).mVOCs were often considered to be by-products of primary metabolism, but recent findings revealed that many mVOCs demonstrate biological activity (Schmidt et al 2015;Tyc et al 2017a). Furthermore, in bacteria, the production of certain mVOCs is dependent on the GacS/GacA two-component regulatory system (Cheng et al 2016;Ossowicki et al 2017).…”

“…However, bacteria showing antifungal activity under lab conditions might not be competitive under natural conditions (Hol et al 2013, Velivelli et al 2014. It was demonstrated that interspecific interactions between non-antagonistic bacteria can trigger or suppress the production of bioactive compounds (Garbeva & De Boer 2009, Traxler et al 2013Garbeva et al 2014a, Tyc et al 2014, Tyc et al 2017a. Furthermore, culture conditions including the supplied nutrient source can have a profound effect on the composition of produced secondary metabolite (Weise et al 2012, Garbeva et al 2014b) and, subsequently, on the performance of the bacteria.…”