Meet me in the middle: Leafhopper feeding preference alters the natural distribution of Salmonella enterica on tomato leaflets

In the last decade, cases of salmonellosis derived from the consumption of contaminated fresh produce has steadily increased. Despite Salmonella enterica populations naturally declining on the phyllosphere of healthy plants, continued reports of produce-associated S. enterica outbreaks indicate that ubiquitous environmental factors, such as insects, contribute to enhanced survival or growth. Previously, infestations by Macrosteles quadrilineatus (Aster leafhopper) were found to significantly promote S. enterica population persistence over time on tomato leaves, whereas other phytophagous insects such as the Myzus persicae (green peach aphid) provided no apparent benefit. We hypothesize that cellular damage by M. quadrilineatus’ intracellular stylet penetration results in a localized beneficial niche on the leaf surface, thereby manipulating the plant phyllosphere to the benefit of S. enterica. Our study demonstrated that M. quadrilineatus infestation resulted in significantly greater cellular damage and simultaneously larger S. enterica populations than plants absent of insects, whereas M. persicae infestation had no impact on cellular integrity or bacterial populations. Although S. enterica populations are observed to be highest at the tip of unaffected tomato leaflets, M. quadrilineatus’ feeding re-distributed bacterial populations evenly across tip and middle portions of leaflets shown through salivary sheath distribution and bacterial population assessments. When observed over a 72-hours on partially contaminated leaflets, M. quadrilineatus initially preferred water inoculated regions, but avoided S. enterica contaminated leaflets by the end of the experiment. These biological assessments have improved our understanding of how phytophagous insects influence human bacterial pathogens on plants which can result in human health consequences.