Assessing physio-macromolecular effects of lactic acid on<i>Zygosaccharomyces bailii</i>cells during microaerobic fermentation

Kuanyshev, Nurzhan; Ami, Diletta; Signori, Lorenzo; Porro, Danilo; Morrissey, John P.; Branduardi, Paola

doi:10.1093/femsyr/fow058

Cited by 17 publications

(27 citation statements)

References 51 publications

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“…Previous research on tolerance to weak organic acids revealed the capability of Z. bailii sensu lato to catabolize acetic and benzoic acids even in the presence of glucose ( 17 , 18 ). In addition, different Z. bailii strains display specific adaptation traits such as the ability to modulate their cell wall and membrane composition in order to decrease the influx of weak acids ( 19 , 20 ).…”

Section: Introductionmentioning

confidence: 99%

“…We are exploring the possibility of using Z. bailii sensu lato species as alternative yeast hosts for lactic acid production. We focused on Z. parabailii strain ATCC 60483 because our previous work demonstrated its high tolerance to lactic acid at low pH, characterized by growth without any detectable lag phase or acid consumption ( 20 ), under microaerobic conditions. These natural characteristics are promising in terms of possible exploitation for organic acid production, and the potential to develop commercial strains will be enhanced when the molecular basis of its unusual tolerance to low pH, high inhibitor concentrations, and other traits of interest are clarified.…”

Section: Introductionmentioning

confidence: 99%

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Transcriptional Response to Lactic Acid Stress in the Hybrid Yeast Zygosaccharomyces parabailii

Ortiz‐Merino

Kuanyshev

Byrne

et al. 2018

Appl Environ Microbiol

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Lactic acid has a wide range of applications starting from its undissociated form, and its production using cell factories requires stress-tolerant microbial hosts. The interspecies hybrid yeast Zygosaccharomyces parabailii has great potential to be exploited as a novel host for lactic acid production, due to high organic acid tolerance at low pH and a fermentative metabolism with a high growth rate. Here we used mRNA sequencing (RNA-seq) to analyze Z. parabailii's transcriptional response to lactic acid added exogenously, and we explore the biological mechanisms involved in tolerance. Z. parabailii contains two homeologous copies of most genes. Under lactic acid stress, the two genes in each homeolog pair tend to diverge in expression to a significantly greater extent than under control conditions, indicating that stress tolerance is facilitated by interactions between the two gene sets in the hybrid. Lactic acid induces downregulation of genes related to cell wall and plasma membrane functions, possibly altering the rate of diffusion of lactic acid into cells. Genes related to iron transport and redox processes were upregulated, suggesting an important role for respiratory functions and oxidative stress defense. We found differences in the expression profiles of genes putatively regulated by Haa1 and Aft1/Aft2, previously described as lactic acid responsive in Saccharomyces cerevisiae. Furthermore, formate dehydrogenase (FDH) genes form a lactic acid-responsive gene family that has been specifically amplified in Z. parabailii in comparison to other closely related species. Our study provides a useful starting point for the engineering of Z. parabailii as a host for lactic acid production.IMPORTANCE Hybrid yeasts are important in biotechnology because of their tolerance to harsh industrial conditions. The molecular mechanisms of tolerance can be studied by analyzing differential gene expression under conditions of interest and relating gene expression patterns to protein functions. However, hybrid organisms present a challenge to the standard use of mRNA sequencing (RNA-seq) to study transcriptional responses to stress, because their genomes contain two similar copies of almost every gene. Here we used stringent mapping methods and a high-quality genome sequence to study the transcriptional response to lactic acid stress in Zygosaccharomyces parabailii ATCC 60483, a natural interspecies hybrid yeast that contains two complete subgenomes that are approximately 7% divergent in sequence. Beyond the insights we gained into lactic acid tolerance in this study, the methods we developed will be broadly applicable to other yeast hybrid strains.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Transcriptional Response to Lactic Acid Stress in the Hybrid Yeast Zygosaccharomyces parabailii

Ortiz‐Merino

Kuanyshev

Byrne

et al. 2018

Appl Environ Microbiol

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“…Other WOAs could also evoke additional and/or different changes: the above‐mentioned FTIR‐based study showed that the phosphatidylcholine content decreased under lactic acid treatment, once more suggesting a mechanism of adaptation through changes in membrane fluidity (Kuanyshev et al ., ), and strengthening the active role of the Z. bailii lipidome dynamic adaptation in providing stress tolerance.…”

Section: Weak Organic Acid Tolerance Of Z Bailii From a S Cerevisiamentioning

confidence: 94%

“…The same defence mechanism might occur in Z. bailii . Recent studies on Z. bailii using Fourier transform infrared micro‐spectroscopy (FTIR) showed lactic acid‐dependent changes in the signals of bands corresponding to glucans and mannans, an indication of cell wall reorganization (Kuanyshev et al ., ).…”

Section: Weak Organic Acid Tolerance Of Z Bailii From a S Cerevisiamentioning

confidence: 97%

The spoilage yeastZygosaccharomyces bailii: Foe or friend?

Kuanyshev

Adamo

Porro

et al. 2017

Yeast

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Zygosaccharomyces bailii is a non-Saccharomyces budding yeast known as one of the most aggressive food spoilage microorganisms, often isolated as a contaminant during wine fermentation, as well as from many acidic, high-sugar and canned foods. The spoilage ability relies on the yeast's unique feature of tolerating the most common preservatives such as sulphite, dimethyl dicarbonate, acetic acid and sorbic acid. Therefore, many studies have focused on the description of this peculiar tolerance with the aim of developing preventative measures against Z. bailii food spoilage. These studies demonstrated the involvement of diverse molecular and physiological mechanisms in the yeast resistance, comprising detoxification of preservatives, adaptation of the cytoplasmic pH and modulation of the cell wall/membrane composition. At the same time, the described traits unveiled Z. bailii as a novel potential workhorse for industrial bioprocesses. Here we present the yeast Z. bailii starting from important aspects of its robustness and concluding with the exploitation of its potential in biotechnology. Overall, the article describes Z. bailii from different perspectives, converging in presenting it as one of the most interesting species of the Saccharomycotina subphylum. Copyright © 2017 John Wiley & Sons, Ltd.

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“…Nevertheless, differences can be observed for other lipid categories: this can indicate a diverse ability of the two yeasts to remodel the lipid composition. Indeed, in a different study [45] it was demonstrated that lactic acid stress did not evoke important variations of the sphingolipid content of Z. parabailii cells, but a significant decrease in lipid acyl chain length occurring in the stationary phase of growth. This modification could contribute to lower membrane fluidity of organic acids in their undissociated form.…”

Section: Comparison Of Model With Other Genome-scale Modelsmentioning

confidence: 98%

Genome-scale metabolic reconstruction of the stress-tolerant hybrid yeast Zygosaccharomyces parabailii

Filippo

Ortiz‐Merino

Damiani

et al. 2018

Preprint

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Funding informationGenome-scale metabolic models are powerful tools to understand and engineer cellular systems facilitating their use as cell factories. This is especially true for microorganisms with known genome sequences from which nearly complete sets of enzymes and metabolic pathways are determined, or can be inferred. Yeasts are highly diverse eukaryotes whose metabolic traits have long been exploited in industry, and although many of their genome sequences are available, few genome-scale metabolic models have so far been produced. For the first time, we reconstructed the genomescale metabolic model of the hybrid yeast Zygosaccharomyces parabailii, which is a member of the Z. bailii sensu lato clade notorious for stress-tolerance and therefore relevant to industry. The model comprises 3096 reactions, 2091 metabolites, and 2413 genes. Our own laboratory data were then used to establish a biomass synthesis reaction, and constrain the extracellular environment. Through constraint-based modeling, our model reproduces the co-consumption and catabolism of acetate and glucose posing it as a promising platform for understanding and exploiting the metabolic po-1 2 MARZIA DI FILIPPO ET AL tential of Z. parabailii. K E Y W O R D SGenome-scale metabolic model/ constraint-based modeling / hybrid yeast / stress tolerance / Zygosaccharomyces parabailii 1 | INTRODUCTION Current genome sequencing technologies allow a fast and cheap overview into the genetic composition of virtually any organism, but connecting such genotypes to observed phenotypes remains a challenge. The reconstruction of genome-scale metabolic networks provide structured frameworks to represent the biochemical transformations within a target organism as complex genotype-phenotype relationships. Afterwards, different modeling approaches can be used to simulate, understand, predict and eventually control the behavior of such genome-scale metabolic networks.Flux Balance Analysis (FBA) is a widely used constraint-based modeling approach that relies on linear programming and the optimization of a given objective function (e.g., maximization of growth) for the determination of the metabolic model flux distribution [1,2]. This approach is based on the assumption that organisms operate under a series of constraints limiting their possible functions, and leading to the definition of allowable cell phenotypes from defined metabolic networks [3].In the last two decades, genome-wide reconstructions of metabolism have been produced for a plethora of model organisms, spanning from bacteria to higher eukaryotes [4]. The original versions of these models typically undergo incremental improvements. In particular, 10 different versions of the Saccharomyces cerevisiae metabolic network have been produced to date, by implementing cellular compartments, curated reactions, standard nomenclature, and even transcriptional regulation, as reviewed in [5]. However, less extensive efforts have been dedicated to other so-called non-conventional or non-Saccharomyces yeast species, de...

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Assessing physio-macromolecular effects of lactic acid onZygosaccharomyces bailiicells during microaerobic fermentation

Cited by 17 publications

References 51 publications

Transcriptional Response to Lactic Acid Stress in the Hybrid Yeast Zygosaccharomyces parabailii

Transcriptional Response to Lactic Acid Stress in the Hybrid Yeast Zygosaccharomyces parabailii

The spoilage yeastZygosaccharomyces bailii: Foe or friend?

Genome-scale metabolic reconstruction of the stress-tolerant hybrid yeast Zygosaccharomyces parabailii

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