Salmonella Establishment in Agricultural Soil and Colonization of Crop Plants Depend on Soil Type and Plant Species

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 thi...

Full description

Bibliographic Details
Main Authors: Sven Jechalke, Jasper Schierstaedt, Marlies Becker, Burkhardt Flemer, Rita Grosch, Kornelia Smalla, Adam Schikora
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.00967/full
id doaj-fde23f67aa504ae49cdf4cef19048589
record_format Article
spelling doaj-fde23f67aa504ae49cdf4cef190485892020-11-24T23:54:52ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-05-011010.3389/fmicb.2019.00967442699Salmonella Establishment in Agricultural Soil and Colonization of Crop Plants Depend on Soil Type and Plant SpeciesSven Jechalke0Jasper Schierstaedt1Marlies Becker2Burkhardt Flemer3Rita Grosch4Kornelia Smalla5Adam Schikora6Institute for Phytopathology, Justus Liebig University Giessen, Gießen, GermanyLeibniz Institute of Vegetable and Ornamental Crops, Plant-Microbe Systems, Großbeeren, GermanyFederal Research Centre for Cultivated Plants, Julius Kühn-Institut (JKI), Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, GermanyLeibniz Institute of Vegetable and Ornamental Crops, Plant-Microbe Systems, Großbeeren, GermanyLeibniz Institute of Vegetable and Ornamental Crops, Plant-Microbe Systems, Großbeeren, GermanyFederal Research Centre for Cultivated Plants, Julius Kühn-Institut (JKI), Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, GermanyFederal Research Centre for Cultivated Plants, Julius Kühn-Institut (JKI), Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, GermanyHuman 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 0.5–0.9% 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. On the one hand, transcriptome data from S. Typhimurium 14028s assessed in response to lettuce medium or lettuce root exudates showed 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 and 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.https://www.frontiersin.org/article/10.3389/fmicb.2019.00967/fullinternalizationplant defenseSalmonellapersistencesoilcrop plants
collection DOAJ
language English
format Article
sources DOAJ
author Sven Jechalke
Jasper Schierstaedt
Marlies Becker
Burkhardt Flemer
Rita Grosch
Kornelia Smalla
Adam Schikora
spellingShingle Sven Jechalke
Jasper Schierstaedt
Marlies Becker
Burkhardt Flemer
Rita Grosch
Kornelia Smalla
Adam Schikora
Salmonella Establishment in Agricultural Soil and Colonization of Crop Plants Depend on Soil Type and Plant Species
Frontiers in Microbiology
internalization
plant defense
Salmonella
persistence
soil
crop plants
author_facet Sven Jechalke
Jasper Schierstaedt
Marlies Becker
Burkhardt Flemer
Rita Grosch
Kornelia Smalla
Adam Schikora
author_sort Sven Jechalke
title Salmonella Establishment in Agricultural Soil and Colonization of Crop Plants Depend on Soil Type and Plant Species
title_short Salmonella Establishment in Agricultural Soil and Colonization of Crop Plants Depend on Soil Type and Plant Species
title_full Salmonella Establishment in Agricultural Soil and Colonization of Crop Plants Depend on Soil Type and Plant Species
title_fullStr Salmonella Establishment in Agricultural Soil and Colonization of Crop Plants Depend on Soil Type and Plant Species
title_full_unstemmed Salmonella Establishment in Agricultural Soil and Colonization of Crop Plants Depend on Soil Type and Plant Species
title_sort salmonella establishment in agricultural soil and colonization of crop plants depend on soil type and plant species
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-05-01
description 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 0.5–0.9% 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. On the one hand, transcriptome data from S. Typhimurium 14028s assessed in response to lettuce medium or lettuce root exudates showed 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 and 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.
topic internalization
plant defense
Salmonella
persistence
soil
crop plants
url https://www.frontiersin.org/article/10.3389/fmicb.2019.00967/full
work_keys_str_mv AT svenjechalke salmonellaestablishmentinagriculturalsoilandcolonizationofcropplantsdependonsoiltypeandplantspecies
AT jasperschierstaedt salmonellaestablishmentinagriculturalsoilandcolonizationofcropplantsdependonsoiltypeandplantspecies
AT marliesbecker salmonellaestablishmentinagriculturalsoilandcolonizationofcropplantsdependonsoiltypeandplantspecies
AT burkhardtflemer salmonellaestablishmentinagriculturalsoilandcolonizationofcropplantsdependonsoiltypeandplantspecies
AT ritagrosch salmonellaestablishmentinagriculturalsoilandcolonizationofcropplantsdependonsoiltypeandplantspecies
AT korneliasmalla salmonellaestablishmentinagriculturalsoilandcolonizationofcropplantsdependonsoiltypeandplantspecies
AT adamschikora salmonellaestablishmentinagriculturalsoilandcolonizationofcropplantsdependonsoiltypeandplantspecies
_version_ 1725464435760300032