Interaction of Phytophagous Insects with Salmonella enterica on Plants and Enhanced Persistence of the Pathogen with Macrosteles quadrilineatus Infestation or Frankliniella occidentalis Feeding

2014

Appl Environ Microbiol

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Several pest insects of human and livestock habitations are known as vectors of Salmonella enterica; however, the role of plantfeeding insects as vectors of S. enterica to agricultural crops remains unexamined. Using a hemipteran insect pest-lettuce system, we investigated the potential for transmission and retention of S. enterica. Specifically, Macrosteles quadrilineatus and Myzus persicae insects were fed S. enterica-inoculated lettuce leaf discs or artificial liquid diets confined in Parafilm sachets to allow physical contact or exclusively oral ingestion of the pathogen, respectively. After a 24-h acquisition access period, insects were moved onto two consecutive noninoculated leaf discs or liquid diets and allowed a 24-h inoculation access period on each of the two discs or sachets. Similar proportions of individuals from both species ingested S. enterica after a 24-h acquisition access period from inoculated leaf discs, but a significantly higher proportion of M. quadrilineatus retained the pathogen internally after a 48-h inoculation access period. S. enterica was also recovered from the honeydew of both species. After a 48-h inoculation access period, bacteria were recovered from a significantly higher proportion of honeydew samples from M. quadrilineatus than from M. persicae insects. The recovery of S. enterica from leaf discs and liquid diets postfeeding demonstrated that both species of insects were capable of transmitting the bacteria in ways that are not limited to mechanical transmission. Overall, these results suggest that phytophagous insects may serve as potential vectors of S. enterica in association with plants.

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Transmission and Retention of Salmonella enterica by Phytophagous Hemipteran Insects

Soto-Arias

Groves

2014

Appl Environ Microbiol

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“…Nevertheless, the aggregation behavior and short-distance dispersal on lettuce (32) indicate that S. enterica-contaminated leafhoppers could contaminate multiple leaves and adjacent plants even in a short period. Additionally, the fact that infestation with M. quadrilineatus enhanced the epiphytic survival of S. enterica on lettuce leaves (8) and that its honeydew can serve as a growth medium for the bacterium (J. P. Soto-Arias, R. L. Groves, and J. D. Barak, presented at the Food Research Institute annual meeting, Madison, WI, 21 to 22 May 2014) increases the chances of insect contamination, and therefore further dispersal of the pathogen on and among plants. Thus, this study further confirms that the most likely mode of transmission of ingested S. enterica by M. quadrilineatus implicates survival of the pathogen during passage through the alimentary canal and release in the environment in contaminated honeydew.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies demonstrated that M. quadrilineatus can become contaminated with S. enterica after feeding on contaminated plant material, and plant infestation with these insects enhanced the persistence of the pathogen on lettuce (8). M. quadrilineatus can also transmit externally attached and ingested bacteria to noninoculated leaves or artificial diets, thereby serving as vectors of S. enterica (6).…”

mentioning

confidence: 99%

Influence of prgH on the Persistence of Ingested Salmonella enterica in the Leafhopper Macrosteles quadrilineatus

Dundore‐Arias

Groves

2015

Appl Environ Microbiol

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Phytophagous insects can encounter Salmonella enterica on contaminated plant surfaces and transmit externally adhered and internalized bacteria on and among leaves. Excretion of ingested S. enterica by the leafhopper Macrosteles quadrilineatus has been previously reported; however, the sites of persistence of ingested bacteria remain undetermined. Fluorescence microscopy revealed the presence and persistence of S. enterica in various organs of M. quadrilineatus fed an inoculated diet for 12 h and then moved to two consecutive noninoculated diets for a total of 48 h. Ingested S. enterica was predominantly observed in the filter chamber, midgut, and Malpighian tubules of M. quadrilineatus dissected immediately after acquisition and at 24-and 48-h post-acquisition access periods (post-AAPs). Additionally, we examined the potential roles of the Salmonella pathogenicity island 1 (SPI-1) and SPI-2 type III secretion systems (T3SSs) in the persistence and excretion of ingested S. enterica. In competition assays, a prgH mutant lacking a functional SPI-1 T3SS was recovered at significantly lower levels than the WT in insect homogenates at 24 h post-AAP, and complementation with prgH restored S. enterica persistence in M. quadrilineatus. Moreover, expression of prgH inside M. quadrilineatus was observed up to 48 post-AAP. No differences were observed between the WT and an ssaK mutant lacking a functional SPI-2 T3SS in insect homogenates or between the WT and either mutant in insect excretions. This study provides novel insight into the presence and persistence of S. enterica inside M. quadrilineatus and demonstrates that the SPI-1 T3SS influences the persistence of the pathogen in the gut of a potential vector. Salmonella enterica is the leading cause of bacterial foodborne illness in the United States (1). In the last few decades, salmonellosis outbreaks attributed to S. enterica-contaminated fresh produce have increased, and produce is now considered the most likely vehicle of disease transmission (2). Plant contamination with S. enterica is thought to primarily occur in the field before harvest, and the pathogen has the ability to adhere, colonize, and persist in and on plant surfaces, in some cases for extended periods (3, 4). Domestic and wild animals represent one of the main entry routes for S. enterica to produce fields, where they can directly introduce the bacterial pathogens to plants or agricultural water through excretion of contaminated waste (3). Additionally, synanthropic and coprophagic insects can introduce human bacterial pathogens to produce fields by dispersing bacteria associated with their exoskeletons onto plant surfaces (5). These events increase the chances that phytophagous insects could encounter a human enteric pathogen as a result of feeding or wandering on contaminated plant surfaces. The abundance and distribution of phytophagous insects within agricultural fields suggest that their contamination could influence the dispersal of enteric pathogens in the field (6).The aster leafhopper, Macro...

Xanthomonas hortorum pv. gardneri TAL effector AvrHah1 is necessary and sufficient for increased persistence of Salmonella enterica on tomato leaves

Cowles

Block

2022

Sci Rep

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Salmonella enterica is ubiquitous in the plant environment, persisting in the face of UV stress, plant defense responses, desiccation, and nutrient limitation. These fluctuating conditions of the leaf surface result in S. enterica population decline. Biomultipliers, such as the phytopathogenic bacterium Xanthomonas hortorum pv. gardneri (Xhg), alter the phyllosphere to the benefit of S. enterica. Specific Xhg-dependent changes to this niche that promote S. enterica persistence remain unclear, and this work focuses on identifying factors that lead to increased S. enterica survival on leaves. Here, we show that the Xhg transcription activator-like effector AvrHah1 is both necessary and sufficient for increased survival of S. enterica on tomato leaves. An Xhg avrHah1 mutant fails to influence S. enterica survival while addition of avrHah1 to X. vesicatoria provides a gain of function. Our results indicate that although Xhg stimulates a robust immune response from the plant, AvrHah1 is not required for these effects. In addition, we demonstrate that cellular leakage that occurs during disease is independent of AvrHah1. Investigation of the interaction between S. enterica, Xhg, and the plant host provides information regarding how an inhospitable environment changes during infection and can be transformed into a habitable niche.