Salmonella persistence in soil depends on reciprocal interactions with indigenous microorganisms

Abstract

Summary Fresh fruits and vegetables have numerous benefits to human health. Unfortunately, their consumption is increasingly associated with food‐borne diseases, Salmonella enterica being their most frequent cause in Europe. Agricultural soils were postulated as reservoir of human pathogens, contributing to the contamination of crops during the growing period. Since the competition with the indigenous soil microbiota for colonization sites plays a major role in the success of invading species, we hypothesized that reduced diversity will enhance the chance of Salmonella to successfully establish in agricultural environments. We demonstrated that the abundance of Salmonella drastically decreased in soil with highly diverse indigenous prokaryotic community, while in soil with reduced prokaryotic diversity, Salmonella persisted for a long period. Furthermore, in communities with low diversity, Salmonella had an impact on the abundance of other taxa. The high physiological plasticity allows Salmonella to use agricultural soils as alternative habitat which might provide a route of animal/human infections. In addition, adjusted transcriptional profile with amino acid biosynthesis and the glyoxylate cycle most prominently regulated, suggests an adaptation to the soil environment. Our results underline the importance of the maintenance of diverse soil microbiome as a part of strategy aiming at reduced risk of food‐borne salmonellosis outbreaks.

Composted Sewage Sludge Influences the Microbiome and Persistence of Human Pathogens in Soil

“…The authors reported a significantly higher survival rate of Salmonella in soils with the organic amendment, reaching 91 dpi versus 35 dpi for control soils. Our study showed that the presence of Salmonella had no impact on the relative abundance of the soil microbiome on phylum level, which is in line with a previous study, which showed that Salmonella influenced the soil microbiome only when the prokaryotic diversity was very low [28].…”

“…In this scenario, we observe better Salmonella survival rates compared to control samples in which Salmonella was added to soil 28 days after fertilization. The results obtained in this study could be explained by the recent report by Schierstaedt et al [28], where it was demonstrated that the abundance of Salmonella enterica decreased faster in soils with a highly diverse prokaryotic community compared to soils with low diversity, underlying the importance of the native soil microbiome in suppressing pathogenic bacteria. Shah et al [58] investigated the persistence of S. Newport in soils with or without heat-treated chicken manure pellet amendment.…”

“…The ability to persist in soils seems to be governed by the diversity of the native soil microbial community. In the case of S. enterica , our previous study revealed a significantly lower persistence in soil with a natural diversity compared to soil with an experimentally reduced microbial diversity [ 28 ]. At the same time, it was shown that several biotic and abiotic factors, such as soil type and fertilizer applied, potentially influence the internalization of human pathogens in plant tissues [ 29 ].…”

Lessons learned from COVID-19 on potentially pathogenic soil microorganisms

“…Habitat is being degraded and homogenized, and nutrient runoff from fertilizers and pesticide use are problematic in industrial-scale agricultural settings (Foley et al, 2005;Stocker et al, 2013). Under these circumstances, changes in soil microbial diversity and structure directly affect the persistence of human pathogens in the soil, such as Salmonella is more durable in high-temperature sterilized soil (Schierstaedt et al, 2020). Furthermore, the global mean surface temperature is increasing, which may contribute to prolonged droughts and flooding, and increased the probability of exposure to frozen pathogens.…”

“…Meanwhile, global warming may facilitate the release of ancient pathogenic microorganisms and advance the population dynamics of viruses (Frenken et al, 2020;Labbé et al, 2020;Zhong et al, 2020), which can infect humans health through extreme weather or through the carriage of plants and animals. The soil pathogenic microbes, indigenous or exogenous pathogenic microbes in the soil that have the potential to cause disease to humans, are typically in balance with other microbes due to subtle interactions and soil properties, such as Salmonella, of which longevity in the soil depends on the interaction with indigenous microorganisms (Locatelli et al, 2013;Schierstaedt et al, 2020). However, this balance can be disrupted by the use of pesticides and fertilizers and by other types of industrial pollution, which may indirectly increase the competitive niche of pathogenic microbes and cause blooms, which increase the likelihood of outbreaks of disease in humans (Fig.…”