|SONG, CHUNXU - WAGENINGEN UNIVERSITY|
|CHENG, XU - WAGENINGEN UNIVERSITY|
|OETJEN, JANINA - UNIVERSITY OF BREMEN|
|DORRESTEIN, PIETER - UNIVERSITY OF CALIFORNIA|
|WATROUS, JERAMIE - UNIVERSITY OF CALIFORNIA|
|VAN DER VOORT, MENNO - WAGENINGEN UNIVERSITY|
|RAAIJMAKERS, JOS - WAGENINGEN UNIVERSITY|
Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/10/2015
Publication Date: 8/6/2015
Citation: Song, C., Mazzola, M., Cheng, X., Oetjen, J., Dorrestein, P., Watrous, J., Van Der Voort, M., Raaijmakers, J.M. 2015. Molecular and chemical dialogues in bacteria-protozoa interactions. Scientific Reports. 5:12837.
Interpretive Summary: Environmental bacteria are exposed to a myriad of biotic interactions. The grazing activity of protozoan predators significantly impacts the dynamics, diversification and evolution of bacterial communities in soil ecosystems. To evade protozoan predation, bacteria employ various defense strategies. We have shown that certain soil bacteria can sense the presence of protozoan predators. When confronted with the protozoan predator Naegleria americana, these bacteria are triggered at the molecular level to produce specific detergent-like compounds, called lipopeptides, which protect them from being attacked and consumed. In this study we show that a broad range of changes in gene expression and corresponding production of metabolites is induced when bacteria of the genus Pseudomonas interact with protozoa that feed on these bacteria. These changes lead to, among other things, enhanced production of compounds that may protect the bacterium from protozoa feeding. These findings are among the first to demonstrate not only changes in gene expression induced in the bacterium, but also the real time production of the corresponding anti-protozoa compounds at the site where the protozoa are attempting to feed on the bacterium. These findings highlight the functional versatility of these natural detergents and document the extent of the molecular dialogue between bacteria and protozoan predators.
Technical Abstract: Soil-dwelling Pseudomonas fluorescens produce lipopeptide surfactants (LPs) with broad-spectrum antimicrobial activities. Recent studies suggested that LPs provide protection to P. fluorescens strain SS101 against grazing by the predatory protozoa Naegleria americana, both in vitro and in rhizosphere environments. These findings documented a new natural function of LPs and suggested that Pseudomonas-protozoa interactions activate an antipredator response in prey populations. Here, genome-wide transcriptome analysis revealed that upon protozoan grazing, 55 genes were up-regulated and 73 genes were down-regulated in P. fluorescens strain SS101. Among the up-regulated genes were the LP biosynthesis genes massABC, genes involved in alkane degradation and in putrescine catalysis. Subsequent assays revealed that putrescine induced trophozoite encystment and adversely affected cyst viability of N. americana. MALDI imaging mass spectrometry (IMS) and live colony NanoDESI mass spectrometry further showed, real time, site-specific LP production at the interface of Pseudomonas-protozoa interactions. In addition, identical transcriptional and metabolic responses were observed in the interaction of P. fluorescens strain SBW25 with N. americana, including the induction of LP and putrescine biosynthesis. Collectively, this multifaceted study provides new insights in common and also strain-specific transcriptional and metabolic responses in bacteria-protozoa interactions, including those responses that may contribute significantly to microbial survival in highly competitive environments such as the rhizosphere.