Mitochondrial‐morphology‐targeted breeding of industrial yeast strains for alcohol fermentation

Kitagaki, Hiroshi

doi:10.1042/ba20090032

Cited by 12 publications

(7 citation statements)

References 120 publications

(127 reference statements)

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“…In addition, azide, an inhibitor of cytochrome c oxidase, inhibited fermentation performance in brewing yeasts . Considering these previous reports, research with sake yeast mitochondria with a molecular biology‐based technique elucidated that the mitochondrial structure fragmented as the fermentation proceeded, and that the mitochondrial morphology had a role in the production profile of organic acids . However, the effect of mitochondrial activity on the organic acid production profile has not yet been studied.…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial activity of sake brewery yeast affects malic and succinic acid production during alcoholic fermentation

2012

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The mitochondrial states and activities of production yeasts used in the fermentation industry vary according to the availability of oxygen, size of the fermentation tank and temperature of the raw material. However, the involvement of the mitochondrial states of these yeasts in the production profile of organic acids during alcoholic fermentation has not been investigated in detail. In this study, the effects of the mitochondrial state of a sake brewing yeast on the organic acid production profile during an alcoholic fermentation process were investigated. It was elucidated that the mitochondrial state during the propagation stage significantly affected the mitochondrial morphology and the organic acid production profile during the alcoholic fermentation. When yeast mitochondria were active, they were highly branched in the propagation stage, and the yeast cells produced significantly more succinate and less malate. In contrast, when the yeast mitochondria were inactive, they were long and filamentous in appearance, and the yeast produced significantly less succinate and more malate. The change in malic acid content was reversed when an uncoupler of mitochondrial membrane potential, carbonylcyanide p-trifluoromethoxyphenylhydrazone, was added to the culture, indicating that the change in the organic acid production profile could be attributed to mitochondrial activity. Furthermore, the content of malic acid and succinic acid could be converted from a respirative to a fermentative profile by exposing the yeast to a mitochondrion-inactivating environment for 12 or 24 h. Taken together, it was shown that the mitochondrial status of the yeast affects malic acid production during alcoholic fermentation.

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Section: Introductionmentioning

confidence: 99%

Mitochondrial activity of sake brewery yeast affects malic and succinic acid production during alcoholic fermentation

2012

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“…Although yeasts undergo autophagy during wine fermentation (17-19), selective modes of autophagy, such as mitophagy, have not been reported. Moreover, there are no published studies on the relationship between mitophagy and the fermentation characteristics of yeast.Our laboratory focuses on the effects of mitochondrial activities and the metabolic engineering of sake yeast strains that influence their ability to ferment substrates (1,(20)(21)(22)(23)(24)(25)(26). Mitochondria depolarize during anaerobiosis, which corresponds to the conditions used for industrial alcoholic fermentation (27-29), and mitophagy occurs when mitochondrial electron potential decreases…”

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confidence: 99%

Enhancement of Ethanol Fermentation in Saccharomyces cerevisiae Sake Yeast by Disrupting Mitophagy Function

Shiroma

Jayakody

Horie

et al. 2014

Appl Environ Microbiol

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c Saccharomyces cerevisiae sake yeast strain Kyokai no. 7 has one of the highest fermentation rates among brewery yeasts used worldwide; therefore, it is assumed that it is not possible to enhance its fermentation rate. However, in this study, we found that fermentation by sake yeast can be enhanced by inhibiting mitophagy. We observed mitophagy in wild-type sake yeast during the brewing of Ginjo sake, but not when the mitophagy gene (ATG32) was disrupted. During sake brewing, the maximum rate of CO 2 production and final ethanol concentration generated by the atg32⌬ laboratory yeast mutant were 7.50% and 2.12% higher than those of the parent strain, respectively. This mutant exhibited an improved fermentation profile when cultured under limiting nutrient concentrations such as those used during Ginjo sake brewing as well as in minimal synthetic medium. The mutant produced ethanol at a concentration that was 2.76% higher than the parent strain, which has significant implications for industrial bioethanol production. The ethanol yield of the atg32⌬ mutant was increased, and its biomass yield was decreased relative to the parent sake yeast strain, indicating that the atg32⌬ mutant has acquired a high fermentation capability at the cost of decreasing biomass. Because natural biomass resources often lack sufficient nutrient levels for optimal fermentation, mitophagy may serve as an important target for improving the fermentative capacity of brewery yeasts. Sake is a traditional Japanese alcoholic beverage produced from steamed rice and koji. During the manufacturing process, glucose is produced (saccharification) from the starch present in rice by the actions of enzymes produced by the koji fungus Aspergillus oryzae. Glucose is fermented to ethanol by Saccharomyces cerevisiae sake yeast strains (1). Sake contains the highest ethanol concentration of all the brewed alcoholic beverages worldwide. This high ethanol concentration is generated by technologies that include successive addition of enzymes and nutrients derived from koji during sake brewing (2, 3), a 3-step pitching process, brewing in winter, and the historical selection of high-ethanol-producing sake yeast strains (1). Sake yeast strains have been selected through a long history of cultivation, ranging from 100 to 400 years. The most frequently used sake yeast at present is Kyokai no. 7 (K7), which was isolated from sake mash in 1946 (4, 5). This strain produces a high concentration of ethanol, because it lacks functions of proteins encoded by MSN4, PPT1, and RIM15, which are required to mount a stress response (6-8). For this reason, researchers in this field believe that it is difficult to further augment the fermentation rate of this sake yeast.Although rice is used as a raw material to brew sake, the surface of rice contains many constituents such as amino acids that impart a heavy and complex taste to sake. Because Japanese consumers tend to prefer a light and clear taste, rice with a polished surface is used for sake brewing. Sake is categorized into...

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“…In contrast, Kitagaki et al . proposed a new pathway that involves manipulation of mitochondrial phenotypes such as morphology and activity to increase the rate of malic acid synthesis (Kitagaki & Shimoi, ; Kitagaki et al ., ; Kitagaki, ; Motomura et al ., ; Kitagaki & Takagi, ; Shiroma et al ., ). Furthermore, Nakayama et al .…”

Section: Introductionmentioning

confidence: 97%

“…Because mitochondria are the site of oxidative respiration, their role in determining the fermentation profile during alcoholic fermentation has long been debated (Albertin et al, 2013). However, we previously demonstrated that mitochondrial membrane potential affects fermentation profiles (Kitagaki & Shimoi, 2007;Kitagaki et al, 2008;Kitagaki, 2009;Motomura et al, 2012;Kitagaki & Takagi, 2013;Shiroma et al, 2014). For example, mitochondrial morphology was first shown to affect the rate of malic acid synthesis.…”

Section: Introductionmentioning

confidence: 99%

“…This hypothesis is supported as well by the decrease of malic acid in strains overexpressing malic enzyme, which catalyzes the conversion of malic acid to pyruvic acid in mitochondria (Redzepovic et al, 2003). In contrast, Kitagaki et al proposed a new pathway that involves manipulation of mitochondrial phenotypes such as morphology and activity to increase the rate of malic acid synthesis (Kitagaki & Shimoi, 2007;Kitagaki et al, 2008;Kitagaki, 2009;Motomura et al, 2012;Kitagaki & Takagi, 2013;Shiroma et al, 2014). Furthermore, Nakayama et al (2012) demonstrated that the high level of malic acid produced by the sake yeast strain No.…”

Section: Introductionmentioning

confidence: 99%

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Variations in mitochondrial membrane potential correlate with malic acid production by natural isolates ofSaccharomyces cerevisiaesake strains

et al. 2014

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Research on the relationship between mitochondrial membrane potential and fermentation profile is being intensely pursued because of the potential for developing advanced fermentation technologies. In the present study, we isolated naturally occurring strains of yeast from sake mash that produce high levels of malic acid and demonstrate that variations in mitochondrial membrane potential correlate with malic acid production. To define the underlying biochemical mechanism, we determined the activities of enzymes required for malic acid synthesis and found that pyruvate carboxylase and malate dehydrogenase activities in strains that produce high levels of malic acid were elevated compared with the standard sake strain K901. These results inspired us to hypothesize that decreased mitochondrial membrane potential was responsible for increased malic acid synthesis, and we present data supporting this hypothesis. Thus, the mitochondrial membrane potential of high malic acid producers was lower compared with standard strains. We conclude that mitochondrial membrane potential correlates with malic acid production.

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Mitochondrial‐morphology‐targeted breeding of industrial yeast strains for alcohol fermentation

Cited by 12 publications

References 120 publications

Mitochondrial activity of sake brewery yeast affects malic and succinic acid production during alcoholic fermentation

Mitochondrial activity of sake brewery yeast affects malic and succinic acid production during alcoholic fermentation

Enhancement of Ethanol Fermentation in Saccharomyces cerevisiae Sake Yeast by Disrupting Mitophagy Function

Variations in mitochondrial membrane potential correlate with malic acid production by natural isolates ofSaccharomyces cerevisiaesake strains

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