Bacterial and plant produced lipids can exacerbate the Olive Quick Decline Syndrome caused by Xylella

Xylella fastidiosa is an insect vector-transmitted bacterial plant pathogen associated with severe diseases in a wide range of plants. In last decades, X. fastidiosa was detected in several European countries. Among X. fastidiosa subspecies, here we study X. fastidiosa subsp. pauca associated with the Olive Quick Decline Syndrome (OQDS) causing severe losses in Southern Italy. First, we collected Olea europaea L. (cv. Ogliarola salentina) samples in groves located in infected zones and uninfected zones. Secondly, the untargeted LC-TOF analysis of the lipid profiles of OQDS positive (+) and negative (-) plants showed a significant clustering of OQDS+ samples apart from OQDS-ones. Thirdly, using HPLC-MS/MS targeted methods and chemometric analysis, we identified a shortlist of 10 lipids significantly different in the infected versus healthy samples. Last, we observed a clear impact on X. fastidiosa subsp. pauca growth and biofilm formation in vitro liquid cultures supplemented with these compounds. Considering that growth and biofilm formation are primary ways by which X. fastidiosa causes disease, our results demonstrate that lipids produced as part of the plants immune response can exacerbate the disease. This is reminiscent of an allergic reaction in animal systems, offering the depression of plant immune response as a potential strategy for OQDS treatment. Author summaryGlobal trade and climate change are re-shaping the distribution map of pandemic pathogens. One major emerging concern is Xylella fastidiosa, a tropical bacterium recently introduced into Europe from America. Its impact has been dramatic: in the last 5-years only, Olive Quick Decline Syndrome (OQDS) has caused thousands of 200 years old olive trees to be felled in the southern Italy. Xylella fastidiosa through a tight coordination of the adherent biofilm and the planktonic states, invades the host systemically. The planktonic phase is correlated to low cell density and vessel colonization. Increase in cell density triggers a quorum sensing system based on cis 2-enoic fatty acids--diffusible signalling factors (DSF) that promote stickiness and biofilm. Xylem vessels are occluded by the combined effect of bacterial biofilm and plant defences (e.g. tyloses). This study provides novel insight on how X. fastidiosa subsp. pauca biology relates to the Olive Quick Decline Syndrome. We found that some class of lipids increase their amount in the infected olive tree. These lipid entities, provided to X. fastidiosa subsp. pauca behave as hormone-like molecules: modulating the dual phase, e.g. planktonic versus biofilm. Probably, part of these lipids represents a reaction of the plant to the bacterial contamination.