Salmonella enterica Suppresses Pectobacterium carotovorum subsp. carotovorum Population and Soft Rot Progression by Acidifying the Microaerophilic Environment
ABSTRACTAlthough enteric human pathogens are usually studied in the context of their animal hosts, a significant portion of their life cycle occurs on plants. Plant disease alters the phyllosphere, leading to enhanced growth of human pathogens; however, the impact of human pathogens on phytopathogen biology and plant health is largely unknown. To characterize the interaction between human pathogens and phytobacterial pathogens in the phyllosphere, we examined the interactions betweenPectobacterium carotovorumsubsp.carotovorumandSalmonella entericaorEscherichia coliO157:H7 with regard to bacterial populations, soft rot progression, and changes in local pH. The presence ofP. carotovorumsubsp.carotovorumenhanced the growth of bothS. entericaandE. coliO157:H7 on leaves. However, in a microaerophilic environment,S. entericareducedP. carotovorumsubsp.carotovorumpopulations and soft rot progression by moderating local environmental pH. Reduced soft rot was not due toS. entericaproteolytic activity. Limitations onP. carotovorumsubsp.carotovorumgrowth, disease progression, and pH elevation were not observed on leaves coinoculated withE. coliO157:H7 or when leaves were coinoculated withS. entericain an aerobic environment.S. entericaalso severely undermined the relationship between the phytobacterial population and disease progression of aP. carotovorumsubsp.carotovorum budBmutant defective in the 2,3-butanediol pathway for acid neutralization. Our results show thatS. entericaandE. coliO157:H7 interact differently with the enteric phytobacterial pathogenP. carotovorumsubsp.carotovorum.S. entericainhibition of soft rot progression may conceal a rapidly growing human pathogen population. Whereas soft rotted produce can alert consumers to the possibility of food-borne pathogens, healthy-looking produce may entice consumption of contaminated vegetables.IMPORTANCESalmonella entericaandEscherichia coliO157:H7 may use plants to move between animal and human hosts. Their populations are higher on plants cocolonized with the common bacterial soft rot pathogenPectobacterium carotovorumsubsp.carotovorum, turning edible plants into a risk factor for human disease. We inoculated leaves withP. carotovorumsubsp.carotovorumandS. entericaorE. coliO157:H7 to study the interactions between these bacteria. WhileP. carotovorumsubsp.carotovorumenhanced the growth of bothS. entericaandE. coliO157:H7, these human pathogens affectedP. carotovorumsubsp.carotovorumfundamentally differently.S. entericareducedP. carotovorumsubsp.carotovorumgrowth and acidified the environment, leading to less soft rot on leaves;E. coliO157:H7 had no such effects. As soft rot signals a food safety risk, the reduction of soft rot symptoms in the presence ofS. entericamay lead consumers to eat healthy-looking butS. enterica-contaminated produce.