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Front. Microbiol. | doi: 10.3389/fmicb.2019.00967

Salmonella establishment in agricultural soil and colonization of crop plants depend on soil type and plant species

 Sven Jechalke1, 2,  Jasper Schierstaedt3, Marlies Becker2, 4, Burkhardt Flemer3,  Rita Grosch3, Kornelia Smalla2 and  Adam Schikora2*
  • 1Institute for Phytopathology, University of Giessen, Germany
  • 2Institute for Epidemiology and Pathogen Diagnostics, Julius Kühn-Institut - Braunschweig, Germany
  • 3Plant-Microbe Systems, Leibniz-Institut für Gemüse- und Zierpflanzenbau (IGZ), Germany
  • 4Department of Biotechnology, Technische Universitat Braunschweig, Germany

Human pathogenic bacteria, such as Salmonella enterica, are able to colonize crop plants. So far, not much is known about biotic and abiotic factors influencing this colonization in field soil. This understanding, however, is imperative for the provision of safe fresh produce to the consumer. In this study, we investigated the effects of soil type, organic fertilization, plant species and the way of Salmonella entry into the plant production system, on the survival of S. enterica in soil as well as the colonization of plants. The selected S. enterica serovar Typhimurium strain 14028s, S. Typhimurium strain LT2 and S. Senftenberg were able to persist in soil for several weeks. Salmonella’s persistence in soil was prolonged in loamy, if compared to sandy soil, and when applied together with organic fertilizer. The leaves of lettuce and corn salad were colonized by S. enterica providing evidence for internalization from the soil via the root. Colonization rates were affected by soil type, plant species and S. enterica strain. Overall, S. enterica was detected in leaves of 0.5% to 0.9% of the plants, while lettuce was more frequently colonized than corn salad. Plants grown in sandy soil were more often colonized than plants grown in loamy soil. After spray-inoculation, S. enterica could be detected on and in leaves for several weeks by cultivation depending methods, confirmed by confocal microscopy using GFP-labeled S. Typhimurium 14028s. Transcriptome data from S. Typhimurium 14028s assessed in response to lettuce medium or lettuce root exudates showed on one hand, an upregulation of genes associated with biofilm formation and virulence. On the other hand, lettuce inoculated with S. Typhimurium 14028s showed a strong upregulation of genes associated with plant immune response and genes related to stress response. In summary, these results showed that organic fertilizers can increase the persistence of Salmonella in soil and that soil type, together with the plant species, play a crucial role in the interactions between human pathogens and crop plants. This understanding is therefore a starting point for new strategies to provide safe food for the consumer.

Keywords: internalization, plant defence, Salmonella, Persistence, Soil, crop plants

Received: 13 Dec 2018; Accepted: 16 Apr 2019.

Edited by:

Camille E. Granada, University of Taquari Valley, Brazil

Reviewed by:

Oswaldo Valdes-Lopez, National Autonomous University of Mexico, Mexico
Anna Gałązka, Institute of Soil Science and Plant Cultivation, Poland  

Copyright: © 2019 Jechalke, Schierstaedt, Becker, Flemer, Grosch, Smalla and Schikora. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Adam Schikora, Julius Kühn-Institut - Braunschweig, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, 38104, Berlin, Germany,