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Effects of stressful physico-chemical factors on the fitness of the plant pathogenic bacterium Dickeya solani

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Abstract

Dickeya solani is a pectinolytic bacterium that causes significant losses of potato crops. Interaction between bacteria and plant during infection and transmission within the host tissue are associated with a variety of challenges, including exposure to physico-chemical factors that induce osmotic, acidic, oxidative or thermal stresses. In this work, we tested the effects of various potentially adverse conditions on growth and fitness of the D. solani IPO2222 type strain. We found the bacteria were able to withstand a great variety of stressful conditions. Treatment with high concentrations of osmolytes (up to 1.6 Osm), low pH (5.0), or elevated temperature (up to 40 °C) was still tolerated. Short term exposure to these conditions did not impair the ability of bacteria to macerate potato tuber tissue. However, D. solani was sensitive to a relatively low content (above 0.5 mM) of the oxidant H2O2 and treatment with this oxidant caused a loss of culturability. All used stressful conditions are known to affect the stability, and structure of proteins and induction of the folding stress-related genes, dnaK, dnaJ and groEL, was observed in most cases. The only exception was oxidative stress for which the chaperone genes were slightly down-regulated. This observation is in line with a low tolerance of D. solani to H2O2.

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Acknowledgements

The research was supported by the grant NCN OPUS-7 UMO-2014/13/B/ NZ9/02021 of National Science Centre, Poland.

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Authors and Affiliations

  1. Department of General and Medical Biochemistry, Faculty of Biology, University of Gdansk, Gdansk, Poland

    Tomasz Przepiora, Donata Figaj, Marta Radzinska, Malgorzata Apanowicz (Bukrejewska), Malgorzata Sieradzka, Patrycja Ambroziak & Joanna Skorko-Glonek

  2. Microbiologie Adaptation et Pathogénie, Université Lyon, CNRS, INSA Lyon, Université Claude Bernard Lyon 1, Villeurbanne, France

    Nicole Hugouvieux-Cotte-Pattat

  3. Department of Plant Protection and Biotechnology, Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, Gdansk, Poland

    Ewa Lojkowska

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  1. Tomasz Przepiora
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Contributions

Joanna Skorko-Glonek, Tomasz Przepiora and Donata Figaj contributed to the study conception and design.

Material preparation, data collection and analysis were performed by Tomasz Przepiora, Donata Figaj, Malgorzata Apanowicz, Malgorzata Sieradzka, Patrycja Ambroziak, Marta Radzinska and Joanna Skorko-Glonek.

The first draft of the manuscript was written by Joanna Skorko-Glonek, Tomasz Przepiora, and Donata Figaj.

Nicole Hugouvieux-Cotte-Pattat and Ewa Lojkowska commented on first draft of the manuscript.

All authors read and approved the final manuscript.

Conceptualization: Joanna Skorko-Glonek;

Methodology: Tomasz Przepiora, Donata Figaj;

Formal analysis and investigation: Joanna Skorko-Glonek, Tomasz Przepiora, Donata Figaj;

Writing - original draft preparation: Joanna Skorko-Glonek, Tomasz Przepiora, Donata Figaj;

Writing - review and editing: Joanna Skorko-Glonek, Nicole Hugouvieux-Cotte-Pattat, Ewa Lojkowska, Tomasz Przepiora, Malgorzata Apanowicz, Malgorzata Sieradzka, Donata Figaj;

Funding acquisition: Joanna-Skorko-Glonek;

Supervision: Joanna Skorko-Glonek.

Corresponding author

Correspondence to Joanna Skorko-Glonek.

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Electronic supplementary material

Supplementary Table 1

Stress conditions used in the experiments. (DOCX 16 kb)

Supplementary Table 2

Growth conditions of the D. solani IPO2222 cultures used for the potato tuber maceration tests. (DOCX 12 kb)

Supplementary Figure 1

Cultivability and viability ofD. solaniIPO2222 under sucrose hyperosmotic stress. Bacteria were grown in minimal medium M63Y under microaerobic conditions to the stationary (a-d) or exponential growth phase (e-h) and subsequently exposed to the osmolyte. To measure colony formation, aliquots of cultures grown in the presence of 0.32 M sucrose at 30 °C (a and e) or 37 °C (b and f) were withdrawn 1 h and 4 h after addition of sucrose. The CFU ml−1 was determined by plating serial dilutions of bacteria. A content of living cells (%) was estimated by fluorescent staining. Panels c and g represent samples incubated at 30 °C, panels d and h at 37 °C. Controls represent untreated samples. Values shown are means of at least three independent experiments and the standard deviations (SD) are represented by error bars. (PDF 425 kb)

Supplementary Figure 2

Ability ofD. solanito withstand oxidative or/and acid stress. Bacteria were grown at 30 °C in minimal medium M63Y under micro-aerobic conditions to the exponential growth phase and subsequently exposed to stressful conditions (H2O2 and/or pH = 5.0) for 1 h or 4 h, at 30 °C (a) or 37 °C (b). Controls represent not treated samples. Values shown are means of at least three independent experiments and the standard deviations (SD) are represented by error bars, * denote statistically significant differences between control and treated samples. The content of living cells (%) was estimated by fluorescent staining. Pictures c and d show examples of fluorescent staining: (c) bacteria incubated for four hours at 37 °C; (d) 37 °C, pH 5.0 and 0.25 mM H2O2. (PDF 277 kb)

Supplementary Figure 3

Effects of oxidative stress on cultivability of the exponential growth phaseD. solanicells IPO2222, IFB0223, IFB0099, IFB0158 and IFB0484. Bacteria were grown in minimal medium M63Y under micro-aerobic conditions to the exponential growth phase and subsequently exposed to stressful conditions. Following 1 h (panels a-c and g-i) or 4 h of exposure to the oxidant (panels d-f and j-l), serial dilutions of bacterial cells were spotted onto the M63Y agar plates and incubated at 30 °C (a-f) or 37 °C (g-l). Panels a, d, g and j show the control (untreated) cell counts. H2O2 was used at a concentration of 0.1 mM (b, e, h, k) or 0.25 mM (c, f, i, l). The roman numbers at the top of the panels indicate the bacterial strain (I – IPO2222, II – IFB0223, III – IFB0099, IV – IFB0158, V – IFB0484). The figure shows representative examples of at least three independent experiments. (PDF 687 kb)

Supplementary Figure 4

Effects of oxidative stress on cultivability of the stationary growth phaseD. solanicells IPO2222, IFB0223, IFB0099, IFB0158 and IFB0484. Bacteria were grown in minimal medium M63Y under micro-aerobic conditions to the stationary growth phase and subsequently treaded as described before supplemental Fig. 3. The roman numbers at the top of the panels indicate the bacterial strain (I – IPO2222, II – IFB0223, III – IFB0099, IV – IFB0158, V – IFB0484). The figure shows representative examples of at least three independent experiments. (PDF 706 kb)

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Przepiora, T., Figaj, D., Radzinska, M. et al. Effects of stressful physico-chemical factors on the fitness of the plant pathogenic bacterium Dickeya solani. Eur J Plant Pathol 156, 519–535 (2020). https://doi.org/10.1007/s10658-019-01902-z

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