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Understanding the physiology of Lactobacillus plantarum at zero growth.

Goffin P, van de Bunt B, Giovane M, Leveau JH, Höppener-Ogawa S, Teusink B, Hugenholtz J - Mol. Syst. Biol. (2010)

Bottom Line: Situations of extremely low substrate availability, resulting in slow growth, are common in natural environments.The combination of metabolic and transcriptomic analyses revealed behaviors involved in interactions with the environment, more particularly with plants: production of plant hormones or precursors thereof, and preparedness for the utilization of plant-derived substrates.Accordingly, the production of compounds interfering with plant root development was demonstrated in slow-growing L. plantarum.

View Article: PubMed Central - PubMed

Affiliation: Kluyver Centre for Genomics of Industrial Fermentations, Delft, The Netherlands.

ABSTRACT
Situations of extremely low substrate availability, resulting in slow growth, are common in natural environments. To mimic these conditions, Lactobacillus plantarum was grown in a carbon-limited retentostat with complete biomass retention. The physiology of extremely slow-growing L. plantarum--as studied by genome-scale modeling and transcriptomics--was fundamentally different from that of stationary-phase cells. Stress resistance mechanisms were not massively induced during transition to extremely slow growth. The energy-generating metabolism was remarkably stable and remained largely based on the conversion of glucose to lactate. The combination of metabolic and transcriptomic analyses revealed behaviors involved in interactions with the environment, more particularly with plants: production of plant hormones or precursors thereof, and preparedness for the utilization of plant-derived substrates. Accordingly, the production of compounds interfering with plant root development was demonstrated in slow-growing L. plantarum. Thus, conditions of slow growth and limited substrate availability seem to trigger a plant environment-like response, even in the absence of plant-derived material, suggesting that this might constitute an intrinsic behavior in L. plantarum.

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Inhibition of radish root development by supernatants of L. plantarum after 10 days under retentostat conditions. Radish root assays were performed according to Leveau and Lindow (2005). Samples were diluted 10,000 times. Error bars represent the s.d. values. **Highly significantly different from fresh medium (P<0.01 Tukey test).
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f4: Inhibition of radish root development by supernatants of L. plantarum after 10 days under retentostat conditions. Radish root assays were performed according to Leveau and Lindow (2005). Samples were diluted 10,000 times. Error bars represent the s.d. values. **Highly significantly different from fresh medium (P<0.01 Tukey test).

Mentions: Interestingly, a number of indole compounds derived from Trp, as well as phenylacetate derived from Phe or phenylacetaldehyde, are known to elicit auxin-like responses in plants (Woodward and Bartel, 2005). The compound, KMBA, has been previously identified as the precursor of the plant stress hormone ethylene in several microorganisms (Ince and Knowles, 1986). Thus, metabolic analysis pointed to a possible production of plant hormones—or precursors thereof—in slow-growing L. plantarum. To verify this hypothesis, supernatants from retentostat cultivation were assayed for their effect on radish root development. As shown in Figure 4, a significant reduction in length was observed when roots were treated with samples collected from retentostat after 10 days (μ=0.0021 h−1), corresponding to the highest measured concentration of indole compounds (Supplementary Figure S6a). The inhibition of radish root development by retentostat samples demonstrates that slow-growing L. plantarum produces compounds that interact with the plant physiology, as deduced from the in silico metabolic modeling approach, and in line with results from transcriptome analysis showing the upregulation of genes involved in the catabolism of plant-derived material.


Understanding the physiology of Lactobacillus plantarum at zero growth.

Goffin P, van de Bunt B, Giovane M, Leveau JH, Höppener-Ogawa S, Teusink B, Hugenholtz J - Mol. Syst. Biol. (2010)

Inhibition of radish root development by supernatants of L. plantarum after 10 days under retentostat conditions. Radish root assays were performed according to Leveau and Lindow (2005). Samples were diluted 10,000 times. Error bars represent the s.d. values. **Highly significantly different from fresh medium (P<0.01 Tukey test).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2964122&req=5

f4: Inhibition of radish root development by supernatants of L. plantarum after 10 days under retentostat conditions. Radish root assays were performed according to Leveau and Lindow (2005). Samples were diluted 10,000 times. Error bars represent the s.d. values. **Highly significantly different from fresh medium (P<0.01 Tukey test).
Mentions: Interestingly, a number of indole compounds derived from Trp, as well as phenylacetate derived from Phe or phenylacetaldehyde, are known to elicit auxin-like responses in plants (Woodward and Bartel, 2005). The compound, KMBA, has been previously identified as the precursor of the plant stress hormone ethylene in several microorganisms (Ince and Knowles, 1986). Thus, metabolic analysis pointed to a possible production of plant hormones—or precursors thereof—in slow-growing L. plantarum. To verify this hypothesis, supernatants from retentostat cultivation were assayed for their effect on radish root development. As shown in Figure 4, a significant reduction in length was observed when roots were treated with samples collected from retentostat after 10 days (μ=0.0021 h−1), corresponding to the highest measured concentration of indole compounds (Supplementary Figure S6a). The inhibition of radish root development by retentostat samples demonstrates that slow-growing L. plantarum produces compounds that interact with the plant physiology, as deduced from the in silico metabolic modeling approach, and in line with results from transcriptome analysis showing the upregulation of genes involved in the catabolism of plant-derived material.

Bottom Line: Situations of extremely low substrate availability, resulting in slow growth, are common in natural environments.The combination of metabolic and transcriptomic analyses revealed behaviors involved in interactions with the environment, more particularly with plants: production of plant hormones or precursors thereof, and preparedness for the utilization of plant-derived substrates.Accordingly, the production of compounds interfering with plant root development was demonstrated in slow-growing L. plantarum.

View Article: PubMed Central - PubMed

Affiliation: Kluyver Centre for Genomics of Industrial Fermentations, Delft, The Netherlands.

ABSTRACT
Situations of extremely low substrate availability, resulting in slow growth, are common in natural environments. To mimic these conditions, Lactobacillus plantarum was grown in a carbon-limited retentostat with complete biomass retention. The physiology of extremely slow-growing L. plantarum--as studied by genome-scale modeling and transcriptomics--was fundamentally different from that of stationary-phase cells. Stress resistance mechanisms were not massively induced during transition to extremely slow growth. The energy-generating metabolism was remarkably stable and remained largely based on the conversion of glucose to lactate. The combination of metabolic and transcriptomic analyses revealed behaviors involved in interactions with the environment, more particularly with plants: production of plant hormones or precursors thereof, and preparedness for the utilization of plant-derived substrates. Accordingly, the production of compounds interfering with plant root development was demonstrated in slow-growing L. plantarum. Thus, conditions of slow growth and limited substrate availability seem to trigger a plant environment-like response, even in the absence of plant-derived material, suggesting that this might constitute an intrinsic behavior in L. plantarum.

Show MeSH
Related in: MedlinePlus