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Plant Microbiology

High Levels of CO2 Induce Spoilage by Leuconostoc mesenteroides by Upregulating Dextran Synthesis Genes

Barak Dror, Alon Savidor, Bolaji Babajide Salam, Noa Sela, Yael Lampert, Paula Teper-Bamnolker, Avinoam Daus, Shmuel Carmeli, Shlomo Sela (Saldinger), Dani Eshel
Isaac Cann, Editor
Barak Dror
aDepartment of Postharvest and Food Sciences, Agricultural Research Organization (ARO), The Volcani Center, Rishon LeZion, Israel
bDepartment of Food Quality and Safety, ARO, The Volcani Center, Rishon LeZion, Israel
cDepartment of Plant Pathology and Microbiology, The Robert H. Smith Faculty of Agriculture Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel
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Alon Savidor
dDe Button Institute for Protein Profiling, The Nancy and Stephen Grand Israel National Center for Personalized Medicine, Weizmann Institute of Science, Rehovot, Israel
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Bolaji Babajide Salam
aDepartment of Postharvest and Food Sciences, Agricultural Research Organization (ARO), The Volcani Center, Rishon LeZion, Israel
cDepartment of Plant Pathology and Microbiology, The Robert H. Smith Faculty of Agriculture Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel
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Noa Sela
eDepartment of Plant Pathology and Weed Science, ARO, The Volcani Center, Rishon LeZion, Israel
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Yael Lampert
aDepartment of Postharvest and Food Sciences, Agricultural Research Organization (ARO), The Volcani Center, Rishon LeZion, Israel
bDepartment of Food Quality and Safety, ARO, The Volcani Center, Rishon LeZion, Israel
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Paula Teper-Bamnolker
aDepartment of Postharvest and Food Sciences, Agricultural Research Organization (ARO), The Volcani Center, Rishon LeZion, Israel
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Avinoam Daus
aDepartment of Postharvest and Food Sciences, Agricultural Research Organization (ARO), The Volcani Center, Rishon LeZion, Israel
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Shmuel Carmeli
fRaymond and Beverly Sackler School of Chemistry and Faculty of Exact Sciences, Tel Aviv University, Tel Aviv, Israel
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Shlomo Sela (Saldinger)
bDepartment of Food Quality and Safety, ARO, The Volcani Center, Rishon LeZion, Israel
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Dani Eshel
aDepartment of Postharvest and Food Sciences, Agricultural Research Organization (ARO), The Volcani Center, Rishon LeZion, Israel
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Isaac Cann
University of Illinois at Urbana-Champaign
Roles: Editor
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DOI: 10.1128/AEM.00473-18
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ABSTRACT

During nonventilated storage of carrots, CO2 gradually accumulates to high levels and causes modifications in the carrot's microbiome toward dominance of Lactobacillales and Enterobacteriales. The lactic acid bacterium Leuconostoc mesenteroides secretes a slimy exudate over the surface of the carrots. The objective of this study was to characterize the slime components and the potential cause for its secretion under high CO2 levels. A proteomic analysis of the exudate revealed bacterial glucosyltransferases as the main proteins, specifically, dextransucrase. A chemical analysis of the exudate revealed high levels of dextran and several simple sugars. The exudate volume and dextran amount were significantly higher when L. mesenteroides was incubated under high CO2 levels than when incubated in an aerated environment. The treatment of carrot medium plates with commercial dextransucrase or exudate protein extract resulted in similar sugar profiles and dextran production. Transcriptome analysis demonstrated that dextran production is related to the upregulation of the L. mesenteroides dextransucrase-encoding genes dsrD and dsrT during the first 4 to 8 h of exposure to high CO2 levels compared to aerated conditions. A phylogenetic analysis of L. mesenteroides YL48 dsrD revealed a high similarity to other dsr genes harbored by different Leuconostoc species. The ecological benefit of dextran production under elevated CO2 requires further investigation. However, this study implies an overlooked role of CO2 in the physiology and fitness of L. mesenteroides in stored carrots, and perhaps in other food items, during storage under nonventilated conditions.

IMPORTANCE The bacterium Leuconostoc mesenteroides is known to cause spoilage of different types of foods by secreting a slimy fluid that damages the quality and appearance of the produce. Here, we identified a potential mechanism by which high levels of CO2 affect the spoilage caused by this bacterium by upregulating dextran synthesis genes. These results have broader implications for the study of the physiology, degradation ability, and potential biotechnological applications of Leuconostoc.

FOOTNOTES

    • Received 26 February 2018.
    • Accepted 10 October 2018.
    • Accepted manuscript posted online 26 October 2018.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.00473-18.

  • Copyright © 2018 American Society for Microbiology.

All Rights Reserved.

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High Levels of CO2 Induce Spoilage by Leuconostoc mesenteroides by Upregulating Dextran Synthesis Genes
Barak Dror, Alon Savidor, Bolaji Babajide Salam, Noa Sela, Yael Lampert, Paula Teper-Bamnolker, Avinoam Daus, Shmuel Carmeli, Shlomo Sela (Saldinger), Dani Eshel
Applied and Environmental Microbiology Dec 2018, 85 (1) e00473-18; DOI: 10.1128/AEM.00473-18

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High Levels of CO2 Induce Spoilage by Leuconostoc mesenteroides by Upregulating Dextran Synthesis Genes
Barak Dror, Alon Savidor, Bolaji Babajide Salam, Noa Sela, Yael Lampert, Paula Teper-Bamnolker, Avinoam Daus, Shmuel Carmeli, Shlomo Sela (Saldinger), Dani Eshel
Applied and Environmental Microbiology Dec 2018, 85 (1) e00473-18; DOI: 10.1128/AEM.00473-18
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KEYWORDS

Enterobacteriales
Lactobacillales
Leuconostoc mesenteroides
carrot
dextran
dextransucrase
microbiome

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