In situ evaluation of Paenibacillus alvei in reducing carriage of Salmonella enterica serovar newport on whole tomato plants

Authors: ALLARD, SARAH - Us Food & Drug Administration (FDA); ENURAH, ALEXANDER - Us Food & Drug Administration (FDA); STRAIN, ERROL - Us Food & Drug Administration (FDA); Millner, Patricia; RIDEOUT, STEVEN - Virginia Tech; BROWN, ERIC - Us Food & Drug Administration (FDA); ZHENG, JIE - Us Food & Drug Administration (FDA)

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/11/2015
Publication Date: 6/30/2015
Citation: Allard, S., Enurah, A., Strain, E., Millner, P.D., Rideout, S., Brown, E., Zheng, J. 2015. In situ evaluation of Paenibacillus alvei in reducing carriage of Salmonella enterica serovar newport on whole tomato plants. Applied and Environmental Microbiology. 80:3842-3849.

Interpretive Summary: Production of fresh and processed tomatoes in the USA accounts for more than $2 billion in annual farm cash receipts (http://www.ers.usda.gov/topics/crops/vegetables-pulses/tomatoes.aspx). While fresh field-grown tomato production has consistently increased over the past several decades, an increasing number of foodborne illness outbreaks caused by various serovars of Salmonella enterica have been associated with consumption of fresh and fresh-cut tomatoes. Salmonella can contaminate the fruit at the primary production stage through soil, irrigation water, and blossoms allowing the pathogen to colonize the exterior and interior of developing fruit. In the absence of cultivar resistance to colonization or a processing “kill-step” to eliminate Salmonella from contamination of tomatoes, the only available control to reduce risk of tomato contamination is following good agricultural practices (GAPs). This study was conducted to isolate potential bacterial antagonists against Salmonella, to examine their modes of action, and to test their effectiveness in reducing carriage of Salmonella on whole tomato plants in a high tunnel setting. In these studies, two strains, A6-6i and TS-15, identified as Paenibacillus alvei, were isolated from plants native to the Virginia Eastern Shore tomato growing region. Both strains were screened for antimicrobial activity against Salmonella and other major foodborne pathogens and major bacterial phytopathogens of tomato. In challenge tests between TS-15 and Salmonella Newport inoculated onto fruits, leaves, and blossoms of tomato plants, in an insect-screened high tunnel, S. Newport declined significantly (p=0.05) compared with controls. Less than 10% of the plants had detectable levels of Salmonella by day 5 for blossoms. Results of the in situ tomato plant trials further showed that P. alvei strain TS-15 is highly effective in reducing the carriage of S. Newport on tomato plants, indicating its potential use as a novel biocontrol agent to mitigate Salmonella contamination at the preharvest level. This report will be of interest to scientists, plant pathologists, tomato growers, and food safety specialists.

Technical Abstract: Recently, tomatoes have been implicated as a primary vehicle in foodborne outbreaks of Salmonella Newport and other Salmonella serovars. Long-term intervention measures to reduce Salmonella prevalence on tomatoes remain elusive for growing and post-harvest environments. A naturally-occurring bacterium identified by 16S rDNA sequencing as Paenibacillus alvei was isolated epiphytically from plants native to the Virginia Eastern Shore tomato growing region. After initial antimicrobial activity screening against Salmonella and 10 other bacterial pathogens associated with the human food supply, strain TS-15 was further used to challenge an attenuated strain of S. Newport on inoculated fruits, leaves, and blossoms of tomato plants in an insect-screened high tunnel with a split-plot design. Survival of Salmonella after inoculation was measured for groups with and without the antagonist at days 0, 1, 2, 3, and 5 for blossoms and 6 for fruits and leaves, respectively. Strain TS-15 exhibited broad range antimicrobial activity against both major foodborne pathogens and major bacterial phytopathogens of tomato. After P. alvei strain TS-15 was applied onto the fruits, leaves, and blossoms of tomato plants, the concentration of S. Newport declined significantly (p=0.05) compared with controls. More than 90% of the plants had no detectable levels of Salmonella by day 5 for blossoms. The naturally-occurring antagonist strain TS-15 is highly effective in reducing carriage of Salmonella Newport on whole tomato plants. The application of P. alvei strain TS-15 is a promising approach for reducing the risk of Salmonella contamination during tomato production.