Impact of Tomato Varieties and Maturity State on Susceptibility of Tomatoes to Salmonella

From 1998 to 2007, fresh fruits, vegetables, spices, and nuts were commonly linked with outbreaks of human gastroenteritis (Batz, Hoffman, and Morris 2011). Non-typhoidal Salmonella has emerged as one of the problematic human pathogens associated with fresh produce, nuts, and complex foods containing them (Batz, Hoffman, and Morris 2011; DeWaal, Tian, and Plunkett 2009). This fact sheet was produced to provide up-to-date information about tomato production practices and their relationships with Salmonella. This information should be useful for county UF/IFAS Extension agents in their vegetable education programs.

Even though Salmonella has long been considered a zoonotic pathogen (i.e., communicable from animals to humans), it is clear that human salmonellosis is also likely to result from the consumption of plant-based (mostly raw) foods. Thus, it appears that Salmonella and pathogenic E. coli may persist on plants between encounters with their animal hosts as a part of their normal lifecycle. Recent research indicates that the outcomes of plant interactions with Salmonella and pathogenic E. coli to some extent depend on the plant host: colonization of plant tissues varied not only among plant species, but also among plant varieties (Jablasone, Warriner, and Griffiths 2005; Barak, Kramer, and Hao 2011; Klerks et al. 2007; Quilliam, Williams, and Jones 2012). This raises the intriguing possibility that cultivar selection could be used to identify crop varieties that may be less conducive to proliferation of human pathogens.

Several recent studies compared the extent to which tomato genotype affects the colonization of plant tissues by Salmonella (Barak, Kramer, and Hao 2011; Marvasi, Noel, et al. 2014). Overall, none of the tested tomato varieties were completely "resistant" to Salmonella, although there were hundred fold differences in the population sizes of the pathogen on tomatoes and within fruit tissues (Barak, Kramer, and Hao 2011; Marvasi, Noel, et al. 2014). In a limited survey of tomato varieties, there were no detectable patterns in susceptibility of heirloom or commercial varieties/hybrids to Salmonella. However, cherry tomatoes were generally less conducive to proliferation of Salmonella (Marvasi, Noel, et al. 2014). Tomatoes carrying ripening mutations (rin [ripening-inhibitor], nor [nonripening], Nr [never-ripe]) were significantly less conducive to Salmonella proliferation (Barak, Kramer, and Hao 2011; Marvasi, Noel, et al. 2014). However, the biochemical basis of why these mutants are less susceptible to Salmonella is not yet known.

Significant differences in the Salmonella colonization of tomatoes at different maturity stages have been observed (Marvasi, Cox, et al. 2013; Shi et al. 2007) and are consistent with the observation that ripe fruits are generally more susceptible to opportunistic pathogens. Differences in proliferation of Salmonella in mature and immature tomatoes did not seem to depend on the pigmentation of the ripe fruit (e.g., red, yellow, pink, brown, or green). How well do these differences observed in the greenhouse correlate to the susceptibility of field-grown tomatoes to Salmonella? When four tomato varieties—Bonny Best, Florida 47, Sebring, and Solar Fire—were tested in the field, their levels of susceptibility to Salmonella did not closely correlate to those observed in the greenhouse studies (Marvasi, Noel, et al. 2014). What is responsible for these observed differences is not yet clear; however, crop production practices and diversity of the microbial communities associated with fruits are known to affect the outcomes of interactions between human pathogens and crops (Marvasi, Cox, et al. 2013; Gutierrez-Rodriguez et al. 2012; Lopez-Velasco et al. 2012; Poza-Carrion, Suslow, and Lindow 2013; Williams et al. 2013).

Under the field conditions and in greenhouse tests, ripe tomatoes supported more rapid proliferation of Salmonella than immature green tomatoes (Shi et al. 2007; Marvasi, George, et al. 2014; Marvasi, Hochmuth, et al. 2013). Final cell numbers of Salmonella were, on average, tenfold higher in ripe tomatoes compared to the unripe tomatoes under the same conditions. In each season, there were samples in which Salmonella populations within red ripe tomatoes increased by at least 10⁵ from the initial dose of ~ 10² cells.