Protozoa are an integral part of most microbial consortia and are ubiquitous in nature, particularly in environments where water is present. Many species of protozoa feed on bacteria, which they ingest by phagocytosis and sequester within food vacuoles. Bacterivorous protozoa have been termed the "Trojan horses" of the microbial world as they may shield pathogenic bacteria that they internalize from the early defense responses of human hosts (2). Recent reviews report over 23 species and groups of pathogens found to associate with amoebae (16,27). Passage of intracellular pathogens such as Legionella pneumophila and Mycobacterium avium through Acanthamoeba castellanii results in these pathogens' greater infectivity (11, 12). Barker et al. The role of protozoa in the virulence of food-borne pathogens and their persistence in the environment has been relatively unexplored. Several pathogenic coliform species were found to be more resistant to chlorination while internalized within A. castellanii and Tetrahymena pyriformis (17). In addition, multiplication of Escherichia coli O157:H7 within Acanthamoeba polyphaga has been reported (4). However, the significance of bacterial entrapment within protozoa cysts or vesicles in the contamination cycle of food-borne pathogenic bacteria has not been addressed. The objective of our study was to determine whether Salmonella enterica could be released in a viable form in vesicles of Tetrahymena and whether this internalization affords a survival advantage over those bacteria that remain free in an aquatic environment. MATERIALS AND METHODSStrains and culture. S. enterica serovar Thompson strain RM1989 is a clinical isolate associated with an outbreak linked to cilantro in California (6, 9). Serovar Thompson strain STN pGT-Kan is a spontaneous nalidixic-acid-resistant mutant of strain RM1989 that is intrinsically labeled with the green fluorescent protein (GFP) by transformation with plasmid pGT-Kan. Plasmid pGT-Kan was constructed by fusion of the nptII promoter fragment from Tn5 to gfp on pPROBE-GT (22) and is stably maintained in serovar Thompson. Strain STN pGT-Kan was used throughout this study and cultured with agitation at 28°C in Luria-Bertani broth (without NaCl) containing gentamicin at 15 g ml Ϫ1 . Listeria monocytogenes strain RM2194 pNF8 is a clinical isolate labeled with GFP and was described previously (15). L. monocytogenes pNF8 was cultured at 28°C in Luria-Bertani broth (without NaCl) containing erythromycin and lincomycin at 1 and 25 g ml Ϫ1 , respectively. Tetrahymena was isolated from soil in California, and the isolate was named SSU. Enrichment for Tetrahymena SSU was performed by the addition of E. coli strain DH5-␣ cells to aqueous soil suspensions. An axenic culture of this isolate was then obtained by incubation of the suspension in Neff's culture medium supplemented with penicillin G and streptomycin sulfate at 250 g ml Ϫ1 each
Campylobacter jejuni has been isolated previously from market produce and has caused gastroenteritis outbreaks linked to produce. We have tested the ability of this human pathogen to utilize organic compounds that are present in leaf and root exudates and to survive in the plant environment under various conditions. Carbon utilization profiles revealed that C. jejuni can utilize many organic acids and amino acids available on leaves and roots. Despite the presence of suitable substrates in the phyllosphere and the rhizosphere, C. jejuni was unable to grow on lettuce and spinach leaves and on spinach and radish roots of plants incubated at 33°C, a temperature that is conducive to its growth in vitro. However, C. jejuni was cultured from radish roots and from the spinach rhizosphere for at least 23 and 28 days, respectively, at 10°C. This enteric pathogen also persisted in the rhizosphere of spinach for prolonged periods of time at 16°C, a temperature at which many cool-season crops are grown. The decline rate constants of C. jejuni populations in the spinach and radish rhizosphere were 10-and 6-fold lower, respectively, than on healthy spinach leaves at 10°C. The enhanced survival of C. jejuni in soil and in the rhizosphere may be a significant factor in its contamination cycle in the environment and may be associated with the sporadic C. jejuni incidence and campylobacteriosis outbreaks linked to produce.
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