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Plant-adapted Escherichia coli show increased lettuce colonizing ability, resistance to oxidative stress and chemotactic response.

Dublan Mde L, Ortiz-Marquez JC, Lett L, Curatti L - PLoS ONE (2014)

Bottom Line: E. coli are also frequently found in different environments and/or alternative secondary hosts, such as plant tissues.The lifestyle of E. coli in plants is poorly understood and has potential implications for food safety.However, acclimation to oxidative stress and/or minimal medium alone failed to prime E. coli cells for enhanced lettuce colonization efficiency.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Investigaciones en Biodiversidad y Biotecnología, Consejo Nacional de Investigaciones Científicas y Técnicas, Mar del Plata, Buenos Aires, Argentina; Fundación para Investigaciones Biológicas Aplicadas, Mar del Plata, Buenos Aires, Argentina; Laboratorio Integrado de Microbiología Agrícola y de Alimentos, Facultad de Agronomía, Universidad Nacional del Centro de la Provincia de Buenos Aires, Azul, Buenos Aires, Argentina.

ABSTRACT

Background: Escherichia coli is a widespread gut commensal and often a versatile pathogen of public health concern. E. coli are also frequently found in different environments and/or alternative secondary hosts, such as plant tissues. The lifestyle of E. coli in plants is poorly understood and has potential implications for food safety.

Methods/principal findings: This work shows that a human commensal strain of E. coli K12 readily colonizes lettuce seedlings and produces large microcolony-like cell aggregates in leaves, especially in young leaves, in proximity to the vascular tissue. Our observations strongly suggest that those cell aggregates arise from multiplication of single bacterial cells that reach those spots. We showed that E. coli isolated from colonized leaves progressively colonize lettuce seedlings to higher titers, suggesting a fast adaptation process. E. coli cells isolated from leaves presented a dramatic rise in tolerance to oxidative stress and became more chemotactic responsive towards lettuce leaf extracts. Mutant strains impaired in their chemotactic response were less efficient lettuce colonizers than the chemotactic isogenic strain. However, acclimation to oxidative stress and/or minimal medium alone failed to prime E. coli cells for enhanced lettuce colonization efficiency.

Conclusion/significance: These findings help to understand the physiological adaptation during the alternative lifestyle of E. coli in/on plant tissues.

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Related in: MedlinePlus

Chemotactic response of plant-adapted Escherichia coli.(A–B) Chemotactic response onto TB medium of (A) non-adapted or (B) plant-adapted bacteria. The bar in (A–B) represents 1 cm. (C–D) Chemotactic response towards (C) lettuce leaf blade or (D) lettuce-leaf main vein extracts. K12LB, non-adapted E. coli strain MG1655; K12, plant-adapted E. coli strain MG1655; RP437, non-adapted E. coli strain RP437 (genomic background of reference for chemotactic analysis); and RP9535, non-adapted E. coli strain RP9535 (ΔcheA1643 mutation in a RP437 genomic background). Strains RP437 and RP9535 were used as control of chemotactic and non-chemotactic E. coli K12 bacteria. Results in C–D are statistically different (P≤0.05).
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pone-0110416-g006: Chemotactic response of plant-adapted Escherichia coli.(A–B) Chemotactic response onto TB medium of (A) non-adapted or (B) plant-adapted bacteria. The bar in (A–B) represents 1 cm. (C–D) Chemotactic response towards (C) lettuce leaf blade or (D) lettuce-leaf main vein extracts. K12LB, non-adapted E. coli strain MG1655; K12, plant-adapted E. coli strain MG1655; RP437, non-adapted E. coli strain RP437 (genomic background of reference for chemotactic analysis); and RP9535, non-adapted E. coli strain RP9535 (ΔcheA1643 mutation in a RP437 genomic background). Strains RP437 and RP9535 were used as control of chemotactic and non-chemotactic E. coli K12 bacteria. Results in C–D are statistically different (P≤0.05).

Mentions: Plant-adapted E. coli cells presented a considerably more active chemotactic response as observed by migration onto TB plates (Fig. 6A–B). To confirm this result migration towards glass capillaries filled with leaf blade or vascular tissue cell-free extracts was scored as a ratio of migration towards sterile PBS buffer (control) from the same bacterial reservoir. Migration towards lettuce extracts was on average 4- to 5-fold more prominent for plant-adapted than non-adapted bacteria cultivated in LB medium. As a control we show that, conversely to its isogenic line (RP437), a mutant strain impaired in the chemotactic response (cheA- ΔcheA1643 strain RP9535) showed no preferential migration towards leaf-extracts (Fig. 6C–D).


Plant-adapted Escherichia coli show increased lettuce colonizing ability, resistance to oxidative stress and chemotactic response.

Dublan Mde L, Ortiz-Marquez JC, Lett L, Curatti L - PLoS ONE (2014)

Chemotactic response of plant-adapted Escherichia coli.(A–B) Chemotactic response onto TB medium of (A) non-adapted or (B) plant-adapted bacteria. The bar in (A–B) represents 1 cm. (C–D) Chemotactic response towards (C) lettuce leaf blade or (D) lettuce-leaf main vein extracts. K12LB, non-adapted E. coli strain MG1655; K12, plant-adapted E. coli strain MG1655; RP437, non-adapted E. coli strain RP437 (genomic background of reference for chemotactic analysis); and RP9535, non-adapted E. coli strain RP9535 (ΔcheA1643 mutation in a RP437 genomic background). Strains RP437 and RP9535 were used as control of chemotactic and non-chemotactic E. coli K12 bacteria. Results in C–D are statistically different (P≤0.05).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4196987&req=5

pone-0110416-g006: Chemotactic response of plant-adapted Escherichia coli.(A–B) Chemotactic response onto TB medium of (A) non-adapted or (B) plant-adapted bacteria. The bar in (A–B) represents 1 cm. (C–D) Chemotactic response towards (C) lettuce leaf blade or (D) lettuce-leaf main vein extracts. K12LB, non-adapted E. coli strain MG1655; K12, plant-adapted E. coli strain MG1655; RP437, non-adapted E. coli strain RP437 (genomic background of reference for chemotactic analysis); and RP9535, non-adapted E. coli strain RP9535 (ΔcheA1643 mutation in a RP437 genomic background). Strains RP437 and RP9535 were used as control of chemotactic and non-chemotactic E. coli K12 bacteria. Results in C–D are statistically different (P≤0.05).
Mentions: Plant-adapted E. coli cells presented a considerably more active chemotactic response as observed by migration onto TB plates (Fig. 6A–B). To confirm this result migration towards glass capillaries filled with leaf blade or vascular tissue cell-free extracts was scored as a ratio of migration towards sterile PBS buffer (control) from the same bacterial reservoir. Migration towards lettuce extracts was on average 4- to 5-fold more prominent for plant-adapted than non-adapted bacteria cultivated in LB medium. As a control we show that, conversely to its isogenic line (RP437), a mutant strain impaired in the chemotactic response (cheA- ΔcheA1643 strain RP9535) showed no preferential migration towards leaf-extracts (Fig. 6C–D).

Bottom Line: E. coli are also frequently found in different environments and/or alternative secondary hosts, such as plant tissues.The lifestyle of E. coli in plants is poorly understood and has potential implications for food safety.However, acclimation to oxidative stress and/or minimal medium alone failed to prime E. coli cells for enhanced lettuce colonization efficiency.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Investigaciones en Biodiversidad y Biotecnología, Consejo Nacional de Investigaciones Científicas y Técnicas, Mar del Plata, Buenos Aires, Argentina; Fundación para Investigaciones Biológicas Aplicadas, Mar del Plata, Buenos Aires, Argentina; Laboratorio Integrado de Microbiología Agrícola y de Alimentos, Facultad de Agronomía, Universidad Nacional del Centro de la Provincia de Buenos Aires, Azul, Buenos Aires, Argentina.

ABSTRACT

Background: Escherichia coli is a widespread gut commensal and often a versatile pathogen of public health concern. E. coli are also frequently found in different environments and/or alternative secondary hosts, such as plant tissues. The lifestyle of E. coli in plants is poorly understood and has potential implications for food safety.

Methods/principal findings: This work shows that a human commensal strain of E. coli K12 readily colonizes lettuce seedlings and produces large microcolony-like cell aggregates in leaves, especially in young leaves, in proximity to the vascular tissue. Our observations strongly suggest that those cell aggregates arise from multiplication of single bacterial cells that reach those spots. We showed that E. coli isolated from colonized leaves progressively colonize lettuce seedlings to higher titers, suggesting a fast adaptation process. E. coli cells isolated from leaves presented a dramatic rise in tolerance to oxidative stress and became more chemotactic responsive towards lettuce leaf extracts. Mutant strains impaired in their chemotactic response were less efficient lettuce colonizers than the chemotactic isogenic strain. However, acclimation to oxidative stress and/or minimal medium alone failed to prime E. coli cells for enhanced lettuce colonization efficiency.

Conclusion/significance: These findings help to understand the physiological adaptation during the alternative lifestyle of E. coli in/on plant tissues.

Show MeSH
Related in: MedlinePlus