Intracellular pH Effects in Lactic Acid Bacteria

Nannen, Nancy L.; Hutkins, Robert W.

doi:10.3168/jds.s0022-0302(91)78219-2

Cited by 66 publications

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“…The growth-inhibiting eect seen at low pH was coupled to the production of lactic acid. Lactococci have been found to withstand extracellular pH values down to 5.7 (Kashket 1987) or 5.0 (Nannen and Hutkins 1991). Under these conditions, both the intracellular accumulation of the lactate anion (Russel 1992) and the uncoupling of ATP synthesis (Kashket 1987) have been claimed to inhibit growth.…”

Section: Resultsmentioning

confidence: 99%

“…It has been reported that the by-product formation is pHdependent such that more by-products, i.e. more acid equivalents, are produced at higher pH (de Ley 1962;Nannen and Hutkins 1991;Yoo et al 1996). Pyruvate formate-lyase is inactivated at low pH, resulting in reduced formic acid and acetyl-CoA and increased lactic acid production (Takahashi et al 1982).…”

Section: Resultsmentioning

confidence: 99%

“…The optimal pH for growth and product formation has been established to be around 6 for both lactococci and lactobacilli (Parente et al 1994;Wijtzes et al 1995;Yoo et al 1996;A Ê kerberg et al 1998). By-product formation decreases with decreasing pH (de Ley 1962;Snoep et al 1990;Nannen and Hutkins 1991;Yoo et al 1996) and was lowest at pH 5 and 30°C for L. lactis 19435 (A Ê kerberg et al 1998).…”

Section: Introductionmentioning

confidence: 99%

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Effect of temperature and pH on growth and product formation of Lactococcus lactis ssp. lactis ATCC 19435 growing on maltose

Hofvendahl

Niel

Hahn‐Hägerdal

1999

Applied Microbiology and Biotechnology

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Link to publicationCitation for published version (APA): Hofvendahl, K., van Niel, E., & Hahn-Hägerdal, B. (1999). Effect of temperature and pH on growth and product formation of Lactococcus lactis ssp. lactis ATCC 19435 growing on maltose. Applied Microbiology and Biotechnology, 51(5), 669-672. https://doi.org/10.1007/s002530051449General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights.• Users may download and print one copy of any publication from the public portal for the purpose of private study or research.• You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Abstract Lactococcus lactis ssp. lactis ATCC 19435 is known to produce mixed acids when grown on maltose. A change in fermentation conditions only, elevated temperatures (up to 37°C) and reduced pH values (down to 5.0) resulted in a shift towards homolactic product formation. This was accompanied by decreased growth rate and cell yield. The results are discussed in terms of redox balance and maintenance, and the regulation of lactate dehydrogenase and pyruvate formate-lyase.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Effect of temperature and pH on growth and product formation of Lactococcus lactis ssp. lactis ATCC 19435 growing on maltose

Hofvendahl

Niel

Hahn‐Hägerdal

1999

Applied Microbiology and Biotechnology

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“…This group consists of certain ruminal bacteria (Russell, 1991b) and various species of lactic acid bacteria (Kashket, 1987). A common feature is the ability to decrease their pH, with pH,, during growth (Russell & Hino, 1985;Nannen & Hutkins, 1991a;Cook & Russell, 1994), and therefore this group of bacteria does not comply with the conventional classification of pH homeostasis. The pronounced organic acid production of these bacteria creates an environment unfavourable for most other organisms (Russell, 1992), which is the basis of many methods of food preservation by fermentation.…”

Section: Introductionmentioning

confidence: 99%

Use of fluorescence ratio imaging for intracellular pH determination of individual bacterial cells in mixed cultures

Siegumfeldt¹,

Rechinger²,

Jakobsen³

1999

Microbiology

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The development of a rapid method for measuring intracellular pH (pH,) in single bacterial cells is described. Lactobacillus delbrueckii subsp. bulgaricus and Listeria innocua were used as test organisms. The method is based upon fluorescence microscopy and ratio imaging of cells stained with carboxyfluorescein succinimidyl ester. After staining, the bacteria were immobilized on a membrane filter and transferred to a closed perfusion chamber, allowing control of the cell environment during analysis. The set-up was optimized with regard to the use of neutral-density filters and background subtraction, for determining the excitation ratio 490 nm/435 nm (R49,,,435) independent of the excitation light intensity, and to reduce photobleaching. This allowed for time-lapse studies with multiple exposures.To study the pH, of Lb. delbrueckii subsp. bulgaricus and L. innocua in response to different extracellular pH (pH,,) values, an in vivo calibration curve was constructed in the pH, range 5-0-8-5. Distinct differences between the two cultures were observed. L. innocua maintained a near-neutral pH, almost independently of pH, (5-&8-0), whereas the pH, of Lb. delbmeckii subsp.bulgaricus decreased with decreasing pH, ,. In pure and mixed cultures a t pH, 5-0, the pH, values of Lb. delbmeckii subsp. bulgaricus and L. innocua were 6120.2 and 7.5202, respectively. This difference in pH, may explain how Lb. delbrueckii subsp. bulgaricus obtains a competitive advantage over L. innocua at low pH, , .Keywords : intracellular pH, ratio imaging, single cells, Lactobacillus delbrueckii subsp. bulgaricus, Listeria innocua INTRODUCTIONMost bacteria maintain an intracellular pH (pH,) close to neutral within fairly narrow limits (Padan et al., 19Sl), because this enables metabolic reactions to occur even under unfavoura ble extracellular pH (pH,,) conditions. Bacteria can be divided into three groups with regard to pH homeostasis : neutrophiles, acidophiles and alkalophiles. These groups differ in requirement for pH,,, but all groups maintain a pH, between 6.5 and 9-5 (White, 1995). Acidophiles maintain a large gradient between pH, and pH,, (ApH), but are restricted to growth in very acidic environments due to an inverted membrane potential (White, 1995 group of acid-tolerant fermentative bacteria grows at pH values ranging from neutral to pH 3-5 (Kashket, 1987;McDonald et al., 1990; Russell, 1991a). This group consists of certain ruminal bacteria (Russell, 1991b) and various species of lactic acid bacteria (Kashket, 1987). A common feature is the ability to decrease their pH, with pH,, during growth (Russell & Hino, 1985;Nannen & Hutkins, 1991a;Cook & Russell, 1994), and therefore this group of bacteria does not comply with the conventional classification of pH homeostasis. The pronounced organic acid production of these bacteria creates an environment unfavourable for most other organisms (Russell, 1992), which is the basis of many methods of food preservation by fermentation.Food fermentations are often carried out by a concerte...

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“…II), as previously known [11], but to different extents, leading to an increase in the ∆pH. This increase enables the internal pH to be maintained at values compatible with growth and survival [7,18]. The growth rate decreased gradually during the culture, as did the specific rate of energy production (q ATP ), and finally, the growth ceased when the external pH was about 3.7, and the internal pH 4.7, but the true cause of the halt of growth remained to be elucidated.…”

Section: Discussionmentioning

confidence: 93%

Article

Mercade

Duperray

Loubière

2003

Lait

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-Growth and energetic parameters of Lactobacillus delbrueckii subsp. bulgaricus were measured during cultures in synthetic medium, at pH regulated at 6.4 and at free pH. These data enabled the actual biomass yield relative to ATP and the maintenance coefficient to be calculated, and the type of control between catabolism and anabolism to be identified. The cultures of L. delbrueckii subsp. bulgaricus at pH 6.4 or at a non-regulated pH were characterized by a concomitant and early decrease in both catabolism and anabolism. At a regulated pH, the growth decrease seems to be due to the accumulation of toxic compounds, acting on anabolic reactions. This inhibition led to a decrease in the catabolic flux, albeit to a lower extent than the anabolic flux. In this condition, the culture was characterized by an excess of energy. On the contrary, at free pH, the lactic acid production led to a pH decrease responsible for the slowing-down of the catabolic flux. At the same time, maintaining the internal pH in the acidified medium was more energy-consuming. The consequence of both the decrease in the glycolytic flux and the increase in the energy consumption led to an energy limitation of growth, as shown by the lower value of the maintenance coefficient.Lactic acid bacteria / Lactobacillus delbrueckii subsp. bulgaricus / energetic analysis / catabolism / anabolism / maintenance coefficient Résumé -Les apports de l'énergétique microbienne à l'analyse des cultures de Lactobacillus delbrueckii subsp. bulgaricus : identification du type de contrôle entre catabolisme et anabolisme. La croissance et les paramètres énergétiques de Lactobacillus delbrueckii subsp. bulgaricus sont quantifiés en cinétique de culture en milieu synthétique, à pH régulé à 6,4 et à pH libre. Ces données permettent d'estimer le rendement ponctuel de biomasse par rapport à l'ATP et le coefficient de maintenance, paramètres dont l'analyse permet d'identifier le type de contrôle reliant le catabolisme à l'anabolisme. Lors des cultures de L. delbrueckii subsp. bulgaricus à pH régulé à 6,4 comme à pH libre, un ralentissement concomitant du catabolisme et de l'anabolisme est observé très précocement en cours de culture. À pH régulé, le ralentissement de croissance semble dû à l'accumulation de produits toxiques, qui affecte en premier lieu l'anabolisme, l'inhibition de l'anabolisme provoquant un rétro-contrôle du flux catabolique, mais dans des proportions moindres que l'anabolisme. La culture est alors en situation d'excédent énergétique. Inversement, à pH libre, la production d'acide lactique provoque une diminution du pH responsable d'un ralentissement du catabolisme. En même temps, l'acidification engendre un coût énergétique supplémentaire pour le * Corresponding author: loubiere@insa-tlse.fr 40 M. Mercade et al.

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Intracellular pH Effects in Lactic Acid Bacteria

Cited by 66 publications

References 13 publications

Effect of temperature and pH on growth and product formation of Lactococcus lactis ssp. lactis ATCC 19435 growing on maltose

Effect of temperature and pH on growth and product formation of Lactococcus lactis ssp. lactis ATCC 19435 growing on maltose

Use of fluorescence ratio imaging for intracellular pH determination of individual bacterial cells in mixed cultures

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