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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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Growth of L. plantarum WCFS1 under retentostat conditions. Data from retentostat cultivation 1 and 2 are represented as black diamonds and gray circles, respectively. (A) Measured biomass concentration (gDW l−1). The biomass calculated from the fitted van Verseveld equation for fermentation 1 (black plain line) and 2 (gray plain line) are shown, as well as the corresponding calculated specific growth rates (black and gray dotted lines for fermentation 1 and 2, respectively). (B) RNA (dotted lines) and protein (plain lines) content of the biomass. (C) Major end products of metabolism during retentostat cultivation of L. plantarum (fermentation 1). Concentrations are expressed as the difference between the measured concentration in the medium feed and the measured concentration in the filter line samples. Closed squares, lactate; closed triangles, acetate; closed circles, formate; open diamonds, ethanol; open triangles, succinate. Source data is available for this figure at www.nature.com/msb.
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f1: Growth of L. plantarum WCFS1 under retentostat conditions. Data from retentostat cultivation 1 and 2 are represented as black diamonds and gray circles, respectively. (A) Measured biomass concentration (gDW l−1). The biomass calculated from the fitted van Verseveld equation for fermentation 1 (black plain line) and 2 (gray plain line) are shown, as well as the corresponding calculated specific growth rates (black and gray dotted lines for fermentation 1 and 2, respectively). (B) RNA (dotted lines) and protein (plain lines) content of the biomass. (C) Major end products of metabolism during retentostat cultivation of L. plantarum (fermentation 1). Concentrations are expressed as the difference between the measured concentration in the medium feed and the measured concentration in the filter line samples. Closed squares, lactate; closed triangles, acetate; closed circles, formate; open diamonds, ethanol; open triangles, succinate. Source data is available for this figure at www.nature.com/msb.

Mentions: L. plantarum WCFS1 was grown under anaerobic retentostat conditions in a chemically defined medium containing glucose and citrate as carbon sources. Two independent cultivations were carried out, which were run for 45 and 31 days (fermentation 1 and 2, respectively). Biomass accumulation followed a negative exponential pattern (Figure 1A), as predicted from the van Verseveld equation (van Verseveld et al, 1986). The biomass accumulation profile did not show different modes of growth, as reported for other microorganisms (Chesbro et al, 1979; van Verseveld et al, 1984; Müller and Babel, 1996). The specific growth rate μ was calculated from the fitted van Verseveld equation (section II.2 of Supplementary information): in the longest-lasting fermentation, the final μ was 0.00006 h−1, corresponding to a calculated doubling time of 1.3 years.


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)

Growth of L. plantarum WCFS1 under retentostat conditions. Data from retentostat cultivation 1 and 2 are represented as black diamonds and gray circles, respectively. (A) Measured biomass concentration (gDW l−1). The biomass calculated from the fitted van Verseveld equation for fermentation 1 (black plain line) and 2 (gray plain line) are shown, as well as the corresponding calculated specific growth rates (black and gray dotted lines for fermentation 1 and 2, respectively). (B) RNA (dotted lines) and protein (plain lines) content of the biomass. (C) Major end products of metabolism during retentostat cultivation of L. plantarum (fermentation 1). Concentrations are expressed as the difference between the measured concentration in the medium feed and the measured concentration in the filter line samples. Closed squares, lactate; closed triangles, acetate; closed circles, formate; open diamonds, ethanol; open triangles, succinate. Source data is available for this figure at www.nature.com/msb.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f1: Growth of L. plantarum WCFS1 under retentostat conditions. Data from retentostat cultivation 1 and 2 are represented as black diamonds and gray circles, respectively. (A) Measured biomass concentration (gDW l−1). The biomass calculated from the fitted van Verseveld equation for fermentation 1 (black plain line) and 2 (gray plain line) are shown, as well as the corresponding calculated specific growth rates (black and gray dotted lines for fermentation 1 and 2, respectively). (B) RNA (dotted lines) and protein (plain lines) content of the biomass. (C) Major end products of metabolism during retentostat cultivation of L. plantarum (fermentation 1). Concentrations are expressed as the difference between the measured concentration in the medium feed and the measured concentration in the filter line samples. Closed squares, lactate; closed triangles, acetate; closed circles, formate; open diamonds, ethanol; open triangles, succinate. Source data is available for this figure at www.nature.com/msb.
Mentions: L. plantarum WCFS1 was grown under anaerobic retentostat conditions in a chemically defined medium containing glucose and citrate as carbon sources. Two independent cultivations were carried out, which were run for 45 and 31 days (fermentation 1 and 2, respectively). Biomass accumulation followed a negative exponential pattern (Figure 1A), as predicted from the van Verseveld equation (van Verseveld et al, 1986). The biomass accumulation profile did not show different modes of growth, as reported for other microorganisms (Chesbro et al, 1979; van Verseveld et al, 1984; Müller and Babel, 1996). The specific growth rate μ was calculated from the fitted van Verseveld equation (section II.2 of Supplementary information): in the longest-lasting fermentation, the final μ was 0.00006 h−1, corresponding to a calculated doubling time of 1.3 years.

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