Study on ATP Production of Lactic Acid Bacteria in Beer and Development of a Rapid Pre-Screening Method for Beer-Spoilage Bacteria

Suzuki, Koji; Iijima, Kazumaru; Ozaki, Kazutaka; Yamashita, Hiroshi

doi:10.1002/j.2050-0416.2005.tb00691.x

Cited by 19 publications

(19 citation statements)

References 44 publications

(73 reference statements)

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“…Amino acid metabolism. The hop adaptation of L. brevis TMW 1.465A increased the conversion of arginine to ornithine via the ADI pathway (42). The observations concerning the levels of metabolites were substantiated by quantification of the expression of the enzymes of the ADI pathway.…”

Section: Discussionmentioning

confidence: 81%

Characterization of a Highly Hop-ResistantLactobacillus brevisStrain Lacking Hop Transport

Behr

Gänzle

Vogel

2006

Appl Environ Microbiol

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Resistance to hops is a prerequisite for lactic acid bacteria to spoil beer. In this study we analyzed mechanisms of hop resistance of Lactobacillus brevis at the metabolism, membrane physiology, and cell wall composition levels. The beer-spoiling organism L. brevis TMW 1.465 was adapted to high concentrations of hop compounds and compared to a nonadapted strain. Upon adaptation to hops the metabolism changed to minimize ethanol stress. Fructose was used predominantly as a carbon source by the nonadapted strain but served as an electron acceptor upon adaptation to hops, with concomitant formation of acetate instead of ethanol. Furthermore, hop adaptation resulted in higher levels of lipoteichoic acids (LTA) incorporated into the cell wall and altered composition and fluidity of the cytoplasmic membrane. The putative transport protein HitA and enzymes of the arginine deiminase pathway were overexpressed upon hop adaptation. HorA was not expressed, and the transport of hop compounds from the membrane to the extracellular space did not account for increased resistance to hops upon adaptation. Accordingly, hop resistance is a multifactorial dynamic property, which can develop during adaptation. During hop adaptation, arginine catabolism contributes to energy and generation of the proton motive force until a small fraction of the population has established structural improvements. This acquired hop resistance is energy independent and involves an altered cell wall composition. LTA shields the organism from accompanying stresses and provides a reservoir of divalent cations, which are otherwise scarce as a result of their complexation by hop acids. Some of the mechanisms involved in hop resistance overlap with mechanisms of pH resistance and ethanol tolerance and as a result enable beer spoilage by L. brevis.Resistance to hops is a prerequisite for the ability of lactic acid bacteria to grow in beer and thus cause beer spoilage. Hop compounds, mainly iso-␣-acids, were described as ionophores which dissipate the pH gradient across the cytoplasmic membrane and reduce the proton motive force (PMF). Consequently, the low intracellular pH (pH in ) interferes with essential enzyme reactions and PMF-dependent nutrient uptake is hampered, resulting in the death of cells of hop-sensitive strains (34,37,49).Several mechanisms involved in the hop resistance of lactobacilli have recently been characterized (13, 34-36, 38, 24-44, 47, 48). The proteins contributing to hop resistance include multidrug resistance (MDR) transporters that excrete the hop compounds into the outer medium (35, 45) and proton export systems that maintain the intracellular pH. HitA is a putative divalent cation transporter present predominantly in beerspoiling lactobacilli (13). An alteration of the teichoic acids in the cell wall (50) and a changed lipid composition of the cytoplasmic membranes (34) might additionally contribute to the hop resistance. However, the role of these hop resistance mechanisms in beer-spoiling lactobacilli is not fully understood...

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Section: Discussionmentioning

confidence: 81%

Characterization of a Highly Hop-ResistantLactobacillus brevisStrain Lacking Hop Transport

Behr

Gänzle

Vogel

2006

Appl Environ Microbiol

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“…It should also be noted that these hop resistance mechanisms are energy-consuming in nature and may give an extra burden to beer spoilage LAB strains when overexpressed. It was further reported that LAB strains are more dependent on the metabolism of organic acids and amino acids in beer rather than fermentable carbohydrates 32 . Therefore the altered metabolism in beer spoilage LAB can conceivably contribute to the induction of VNC states.…”

Section: Discussionmentioning

confidence: 99%

Induction of Viable but Nonculturable State in Beer Spoilage Lactic Acid Bacteria

Suzuki

Iijima

Asano

et al. 2006

Journal of the Institute of Brewing

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Strong beer spoilage strains Lactobacillus lindneri DSM 20692 and Lactobacillus paracollinoides JCM 11969 T were repeatedly subcultured in degassed beer and their culturability on MRS agar was examined. As a result, the two strains were found to show decreased culturability, suggesting that the prolonged contact with beer reduces the culturability of beer spoilage lactic acid bacteria (LAB). After 30 subcultures in degassed beer, both strains were subjected to sublethal heat treatment. As a consequence, L. lindneri DSM 20692 and L. paracollinoides JCM 11969 T were no longer detectable on MRS agar despite the presence of 460 viable cells, indicating that the viable but nonculturable (VNC) states were induced for both strains. Problematically, the heat treated VNC strains were shown to exhibit beer spoilage ability, suggesting that spoilage incidents can occur without detection by culture media. It was also shown that, once acquired, the VNC states are stably maintained in beer without further heat treatment. These results suggest the possibility that beer spoilage LAB strains remain hidden in pitching yeast and work-in-process products without detection. Furthermore L. lindneri DSM 20692 and L. paracollinoides JCM 11969 T in VNC states were successfully stored at -80°C with 10% dimethylsulfoxide as a cryoprotectant and reconstituted in degassed beer without losing VNC characteristics. Taken together, these findings show that valuable bioresources can be acquired from culturable beer spoilage LAB strains and maintained for long-term storage as frozen culture stocks.

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“…Despite these disadvantages, beer spoilage LAB strains are still capable of growth in beer. Indeed three beer spoilage LAB strains, L. brevis ABBC45, L. lindneri DSM 20690 T and L. paracollinoides JCM 11969 T , were found to exhibit strong ATP-yielding ability in beer 145 . In addition, the ATP pool in the hop-resistant LAB strains was found to be larger than in the hop-sensitive strains 129 .…”

Section: Part 2: Hop Resistance In Beer Spoilage Labmentioning

confidence: 99%

“…It was shown that citrate, pyruvate, malate and arginine were consumed to support the growth of the beer spoilage LAB strains 145 . The four components induced considerable ATP production, even in the presence of hop compounds, accounting for the ATP-yielding ability of the beer spoilage LAB strains observed in beer.…”

Section: Part 2: Hop Resistance In Beer Spoilage Labmentioning

confidence: 99%

125th Anniversary Review: Microbiological Instability of Beer Caused by Spoilage Bacteria

Suzuki

2011

Journal of the Institute of Brewing

128

130

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Beer has been generally recognized as a microbiologically stable beverage. However, microbiological incidents occasionally occur in the brewing industry. The microbiological instability of beer is often caused by bacteria consisting of four genera, Lactobacillus, Pediococcus, Pectinatus and Megasphaera. Lactobacillus and Pediococcus belong to the lactic acid bacteria (LAB), whereas Pectinatus and Megasphaera form a group of strict anaerobes that are known as intermediates between Gram‐positive and Gram‐negative bacteria. The frequencies of beer spoilage incidents caused by these four genera have been reported to exceed 90% in Europe and therefore Lactobacillus, Pediococcus, Pectinatus and Megasphaera are considered to be the principal spoilage agents in the brewing industry. Thus, this review consists of three parts involving these four genera. The first part describes spoilage LAB in alcoholic beverages with some emphasis on beer spoilage LAB. In this part, the emergence and evolution of these spoilage LAB is discussed, the insight of which is useful for developing quality control methods for these beverages. The second part is devoted to the hop resistance in beer spoilage LAB. This area of research is evolving rapidly and recent progress in this field is summarized. The third part concerns Pectinatus and Megasphaera. Although this group of beer spoilage bacteria has been described relatively recently, the incident reports in Europe increased in the early 1990s, reaching around 30% of spoilage incidents. Various aspects of Pectinatus and Megasphaera, ranging from their taxonomy and beer spoilage ability to detection and eradication methods are described.

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Study on ATP Production of Lactic Acid Bacteria in Beer and Development of a Rapid Pre-Screening Method for Beer-Spoilage Bacteria

Cited by 19 publications

References 44 publications

Characterization of a Highly Hop-ResistantLactobacillus brevisStrain Lacking Hop Transport

Characterization of a Highly Hop-ResistantLactobacillus brevisStrain Lacking Hop Transport

Induction of Viable but Nonculturable State in Beer Spoilage Lactic Acid Bacteria

125th Anniversary Review: Microbiological Instability of Beer Caused by Spoilage Bacteria

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