Biotic and abiotic soil properties influence survival of Listeria monocytogenes in soil

Listeria monocytogenes is a food-borne pathogen responsible for the potentially fatal disease listeriosis and terrestrial ecosystems have been hypothesized to be its natural reservoir. Therefore, identifying the key edaphic factors that influence its survival in soil is critical. We measured the sur...

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Published inPloS one Vol. 8; no. 10; p. e75969
Main Authors Locatelli, Aude, Spor, Aymé, Jolivet, Claudy, Piveteau, Pascal, Hartmann, Alain
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 07.10.2013
Public Library of Science (PLoS)
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Abstract Listeria monocytogenes is a food-borne pathogen responsible for the potentially fatal disease listeriosis and terrestrial ecosystems have been hypothesized to be its natural reservoir. Therefore, identifying the key edaphic factors that influence its survival in soil is critical. We measured the survival of L. monocytogenes in a set of 100 soil samples belonging to the French Soil Quality Monitoring Network. This soil collection is meant to be representative of the pedology and land use of the whole French territory. The population of L. monocytogenes in inoculated microcosms was enumerated by plate count after 7, 14 and 84 days of incubation. Analysis of survival profiles showed that L. monocytogenes was able to survive up to 84 days in 71% of the soils tested, in the other soils (29%) only a short-term survival (up to 7 to 14 days) was observed. Using variance partitioning techniques, we showed that about 65% of the short-term survival ratio of L. monocytogenes in soils was explained by the soil chemical properties, amongst which the basic cation saturation ratio seems to be the main driver. On the other hand, while explaining a lower amount of survival ratio variance (11%), soil texture and especially clay content was the main driver of long-term survival of L. monocytogenes in soils. In order to assess the effect of the endogenous soils microbiota on L. monocytogenes survival, sterilized versus non-sterilized soils microcosms were compared in a subset of 9 soils. We found that the endogenous soil microbiota could limit L. monocytogenes survival especially when soil pH was greater than 7, whereas in acidic soils, survival ratios in sterilized and unsterilized microcosms were not statistically different. These results point out the critical role played by both the endogenous microbiota and the soil physic-chemical properties in determining the survival of L. monocytogenes in soils.
AbstractList Listeria monocytogenes is a food-borne pathogen responsible for the potentially fatal disease listeriosis and terrestrial ecosystems have been hypothesized to be its natural reservoir. Therefore, identifying the key edaphic factors that influence its survival in soil is critical. We measured the survival of L. monocytogenes in a set of 100 soil samples belonging to the French Soil Quality Monitoring Network. This soil collection is meant to be representative of the pedology and land use of the whole French territory. The population of L. monocytogenes in inoculated microcosms was enumerated by plate count after 7, 14 and 84 days of incubation. Analysis of survival profiles showed that L. monocytogenes was able to survive up to 84 days in 71% of the soils tested, in the other soils (29%) only a short-term survival (up to 7 to 14 days) was observed. Using variance partitioning techniques, we showed that about 65% of the short-term survival ratio of L. monocytogenes in soils was explained by the soil chemical properties, amongst which the basic cation saturation ratio seems to be the main driver. On the other hand, while explaining a lower amount of survival ratio variance (11%), soil texture and especially clay content was the main driver of long-term survival of L. monocytogenes in soils. In order to assess the effect of the endogenous soils microbiota on L. monocytogenes survival, sterilized versus non-sterilized soils microcosms were compared in a subset of 9 soils. We found that the endogenous soil microbiota could limit L. monocytogenes survival especially when soil pH was greater than 7, whereas in acidic soils, survival ratios in sterilized and unsterilized microcosms were not statistically different. These results point out the critical role played by both the endogenous microbiota and the soil physic-chemical properties in determining the survival of L. monocytogenes in soils.
Listeria monocytogenes is a food-borne pathogen responsible for the potentially fatal disease listeriosis and terrestrial ecosystems have been hypothesized to be its natural reservoir. Therefore, identifying the key edaphic factors that influence its survival in soil is critical. We measured the survival of L. monocytogenes in a set of 100 soil samples belonging to the French Soil Quality Monitoring Network. This soil collection is meant to be representative of the pedology and land use of the whole French territory. The population of L. monocytogenes in inoculated microcosms was enumerated by plate count after 7, 14 and 84 days of incubation. Analysis of survival profiles showed that L. monocytogenes was able to survive up to 84 days in 71% of the soils tested, in the other soils (29%) only a short-term survival (up to 7 to 14 days) was observed. Using variance partitioning techniques, we showed that about 65% of the short-term survival ratio of L. monocytogenes in soils was explained by the soil chemical properties, amongst which the basic cation saturation ratio seems to be the main driver. On the other hand, while explaining a lower amount of survival ratio variance (11%), soil texture and especially clay content was the main driver of long-term survival of L. monocytogenes in soils. In order to assess the effect of the endogenous soils microbiota on L. monocytogenes survival, sterilized versus non-sterilized soils microcosms were compared in a subset of 9 soils. We found that the endogenous soil microbiota could limit L. monocytogenes survival especially when soil pH was greater than 7, whereas in acidic soils, survival ratios in sterilized and unsterilized microcosms were not statistically different. These results point out the critical role played by both the endogenous microbiota and the soil physic-chemical properties in determining the survival of L. monocytogenes in soils.
Audience Academic
Author Spor, Aymé
Jolivet, Claudy
Piveteau, Pascal
Locatelli, Aude
Hartmann, Alain
AuthorAffiliation 2 INRA, US-1106 InfoSol, BP20619, Orléans, France
University of Illinois at Chicago College of Medicine, United States of America
3 Université de Bourgogne, UMR1347 Agroécologie, Dijon, France
1 INRA, UMR1347 Agroécologie, Dijon, France
AuthorAffiliation_xml – name: 1 INRA, UMR1347 Agroécologie, Dijon, France
– name: 3 Université de Bourgogne, UMR1347 Agroécologie, Dijon, France
– name: 2 INRA, US-1106 InfoSol, BP20619, Orléans, France
– name: University of Illinois at Chicago College of Medicine, United States of America
Author_xml – sequence: 1
  givenname: Aude
  surname: Locatelli
  fullname: Locatelli, Aude
  organization: INRA, UMR1347 Agroécologie, Dijon, France
– sequence: 2
  givenname: Aymé
  surname: Spor
  fullname: Spor, Aymé
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  givenname: Claudy
  surname: Jolivet
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  givenname: Pascal
  surname: Piveteau
  fullname: Piveteau, Pascal
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  givenname: Alain
  surname: Hartmann
  fullname: Hartmann, Alain
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24116083$$D View this record in MEDLINE/PubMed
https://hal.inrae.fr/hal-02650765$$DView record in HAL
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ContentType Journal Article
Copyright COPYRIGHT 2013 Public Library of Science
2013 Locatelli et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Distributed under a Creative Commons Attribution 4.0 International License
2013 Locatelli et al 2013 Locatelli et al
Copyright_xml – notice: COPYRIGHT 2013 Public Library of Science
– notice: 2013 Locatelli et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: Distributed under a Creative Commons Attribution 4.0 International License
– notice: 2013 Locatelli et al 2013 Locatelli et al
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IsDoiOpenAccess true
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Issue 10
Keywords endogenous microbiota
pH
Listeria monocytogenes
french soil monitoring network
basic cation saturation ratio
survival
Language English
License Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
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content type line 23
Competing Interests: The authors have declared that no competing interests exist.
Conceived and designed the experiments: AL AS CJ PP AH. Performed the experiments: AL AS CJ PP AH. Analyzed the data: AL AS CJ PP AH. Contributed reagents/materials/analysis tools: AL AS CJ PP AH. Wrote the paper: AL AS CJ PP AH.
ORCID 0000-0002-4707-9559
0000-0002-1210-251X
0000-0001-5871-6413
0000-0001-6034-5068
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3792134/
PMID 24116083
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Snippet Listeria monocytogenes is a food-borne pathogen responsible for the potentially fatal disease listeriosis and terrestrial ecosystems have been hypothesized to...
Listeria monocytogenes is a food-borne pathogen responsible for the potentially fatal disease listeriosis and terrestrial ecosystems have been hypothesized to...
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StartPage e75969
SubjectTerms Acidic soils
Analysis
Animals
Bacteria
Biota
Chemical properties
Clay soils
E coli
Environmental monitoring
Environmental Sciences
Food contamination & poisoning
Incubation
Irrigation
Land use
Life Sciences
Listeria
Listeria monocytogenes
Listeria monocytogenes - physiology
Listeriosis
Livestock
Loam soils
Manures
Microbiology
Microbiota
Microbiota (Symbiotic organisms)
Microcosms
Pathogens
Pedology
Quality control
Seeds
Soil - chemistry
Soil acidity
Soil Microbiology
Soil pH
Soil properties
Soil quality
Soil testing
Soil texture
Statistical analysis
Statistical methods
Survival
Terrestrial ecosystems
Terrestrial environments
Territory
Texture
Variance
Vegetables
Vegetal Biology
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Title Biotic and abiotic soil properties influence survival of Listeria monocytogenes in soil
URI https://www.ncbi.nlm.nih.gov/pubmed/24116083
https://www.proquest.com/docview/1440075691
https://search.proquest.com/docview/1443428377
https://hal.inrae.fr/hal-02650765
https://pubmed.ncbi.nlm.nih.gov/PMC3792134
https://doaj.org/article/ab128f0f045e479cb157be0a70d21cb3
http://dx.doi.org/10.1371/journal.pone.0075969
Volume 8
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