Salmonella enterica changes Macrosteles quadrilineatus feeding behaviors resulting in altered S. enterica distribution on leaves and increased populations

Abstract

Hemipteran insects are ubiquitous inhabitants of the phyllosphere. Changes in microbial phyllosphere communities have recently been demonstrated following infestation by Macrosteles quadrilineatus (Aster Leafhopper). Although epiphytic Salmonella enterica populations naturally decline in the phyllosphere of plants, M. quadrilineatus infestation facilitated the growth of the bacterial pathogen populations. Here, we demonstrate that cellular damage by insect stylet penetration results in a localized beneficial niche on the leaf surface, leading to enhanced S. enterica populations. We measured S. enterica populations and colonization patterns on plants infested with Hemipterans with distinct feeding behaviors. M. quadrilineatus infestation resulted in higher solute leakage and significantly greater bacterial populations than plants absent of insects. Following immigration via contaminated irrigation water, the highest populations of S. enterica are naturally found on the tips of tomato leaflets. We discovered M. quadrilineatus feeding preference altered the natural distribution of S. enterica populations, and that the presence of S. enterica altered the distribution of probing attempts. These findings elucidate how cellular damage resulting from insect feeding drives changes in bacterial colonization of the phyllosphere.