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Understanding the stress responses of Kluyveromyces marxianus after an arrest during high-temperature ethanol fermentation based on integration of RNA-Seq and metabolite data.
Appl Microbiol Biotechnol. 2019 Mar; 103(6):2715-2729.AM

Abstract

The thermotolerant Kluyveromyces marxianus is a potential candidate for high-temperature ethanol fermentation. Although K. marxianus exhibited high ethanol productivity at 45 °C during the early fermentation stage, we observed a fermentation arrest due to the accumulated inhibitors. The stress responses of K. marxianus during high-temperature fermentation were revealed based on integration of RNA sequencing (RNA-Seq) and metabolite data. High temperature stimulated mitochondrial respiration but repressed the tricarboxylic acid (TCA) cycle, leading to increased generation of reactive oxygen species (ROS) and a lowered ratio of reduced nicotinamide adenine dinucleotide (NADH)/oxidized nicotinamide adenine dinucleotide (NAD+). Glycerol production was enhanced during the early fermentation stage, which might contribute to NADH reoxidation and ROS generation. Excess ROS could be neutralized by reduced nicotinamide adenine dinucleotide phosphate (NADPH) that might be reserved in the following ways: (1) decreased biosynthesis of branched-chain amino acids (BCAAs) reduced NADPH consumption; (2) enhanced acetic acid production increased NADPH regeneration. The degree of fatty acid unsaturation was also reduced to adapt to high temperature. In addition, stress responses were also observed after the fermentation arrest at 45 °C. Genes related to peroxidase activity, iron-sulfur cluster assembly, and flavin mononucleotide (FMN) binding were downregulated, while genes associated with DNA repair and lipid composition of the plasma were upregulated. The yeast also produced more ergosterol to deal with ethanol stress. This study gains comprehensive insights into the K. marxianus transcriptome under various stresses during high-temperature ethanol fermentation, providing rich information for further metabolic engineering towards improved stress tolerance and ethanol production.

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Authors+Show Affiliations

Fu X
MOST-USDA Joint Research Center for Biofuels, Beijing Engineering Research Center for Biofuels, Institute of New Energy Technology, Tsinghua University, Beijing, 100084, China.
Li P
MOST-USDA Joint Research Center for Biofuels, Beijing Engineering Research Center for Biofuels, Institute of New Energy Technology, Tsinghua University, Beijing, 100084, China. lipengsong@tsinghua.edu.cn.
Zhang L
MOST-USDA Joint Research Center for Biofuels, Beijing Engineering Research Center for Biofuels, Institute of New Energy Technology, Tsinghua University, Beijing, 100084, China. Agricultural Utilization Research Center, Nutrition and Health Research Institute, COFCO Corporation, No.4 Road, Future Science and Technology Park South, Beiqijia, Changping, Beijing, 102209, China.
Li S
MOST-USDA Joint Research Center for Biofuels, Beijing Engineering Research Center for Biofuels, Institute of New Energy Technology, Tsinghua University, Beijing, 100084, China. szli@tsinghua.edu.cn.

MeSH

Acetic AcidAmino Acids, Branched-ChainBase SequenceCitric Acid CycleEthanolFermentationGlucoseHot TemperatureKluyveromycesMetabolic EngineeringMitochondriaNADPReactive Oxygen SpeciesSequence Analysis, RNAStress, PhysiologicalTranscriptome

Pub Type(s)

Journal Article

Language

eng

PubMed ID

30673809

Citation

Fu, Xiaofen, et al. "Understanding the Stress Responses of Kluyveromyces Marxianus After an Arrest During High-temperature Ethanol Fermentation Based On Integration of RNA-Seq and Metabolite Data." Applied Microbiology and Biotechnology, vol. 103, no. 6, 2019, pp. 2715-2729.
Fu X, Li P, Zhang L, et al. Understanding the stress responses of Kluyveromyces marxianus after an arrest during high-temperature ethanol fermentation based on integration of RNA-Seq and metabolite data. Appl Microbiol Biotechnol. 2019;103(6):2715-2729.
Fu, X., Li, P., Zhang, L., & Li, S. (2019). Understanding the stress responses of Kluyveromyces marxianus after an arrest during high-temperature ethanol fermentation based on integration of RNA-Seq and metabolite data. Applied Microbiology and Biotechnology, 103(6), 2715-2729. https://doi.org/10.1007/s00253-019-09637-x
Fu X, et al. Understanding the Stress Responses of Kluyveromyces Marxianus After an Arrest During High-temperature Ethanol Fermentation Based On Integration of RNA-Seq and Metabolite Data. Appl Microbiol Biotechnol. 2019;103(6):2715-2729. PubMed PMID: 30673809.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Understanding the stress responses of Kluyveromyces marxianus after an arrest during high-temperature ethanol fermentation based on integration of RNA-Seq and metabolite data. AU - Fu,Xiaofen, AU - Li,Pengsong, AU - Zhang,Lei, AU - Li,Shizhong, Y1 - 2019/01/23/ PY - 2018/07/26/received PY - 2019/01/08/accepted PY - 2019/01/06/revised PY - 2019/1/24/pubmed PY - 2019/7/19/medline PY - 2019/1/24/entrez KW - Acetic acid KW - Ethanol KW - High temperature KW - Kluyveromyces marxianus KW - RNA-Seq KW - Reactive oxygen species (ROS) SP - 2715 EP - 2729 JF - Applied microbiology and biotechnology JO - Appl Microbiol Biotechnol VL - 103 IS - 6 N2 - The thermotolerant Kluyveromyces marxianus is a potential candidate for high-temperature ethanol fermentation. Although K. marxianus exhibited high ethanol productivity at 45 °C during the early fermentation stage, we observed a fermentation arrest due to the accumulated inhibitors. The stress responses of K. marxianus during high-temperature fermentation were revealed based on integration of RNA sequencing (RNA-Seq) and metabolite data. High temperature stimulated mitochondrial respiration but repressed the tricarboxylic acid (TCA) cycle, leading to increased generation of reactive oxygen species (ROS) and a lowered ratio of reduced nicotinamide adenine dinucleotide (NADH)/oxidized nicotinamide adenine dinucleotide (NAD+). Glycerol production was enhanced during the early fermentation stage, which might contribute to NADH reoxidation and ROS generation. Excess ROS could be neutralized by reduced nicotinamide adenine dinucleotide phosphate (NADPH) that might be reserved in the following ways: (1) decreased biosynthesis of branched-chain amino acids (BCAAs) reduced NADPH consumption; (2) enhanced acetic acid production increased NADPH regeneration. The degree of fatty acid unsaturation was also reduced to adapt to high temperature. In addition, stress responses were also observed after the fermentation arrest at 45 °C. Genes related to peroxidase activity, iron-sulfur cluster assembly, and flavin mononucleotide (FMN) binding were downregulated, while genes associated with DNA repair and lipid composition of the plasma were upregulated. The yeast also produced more ergosterol to deal with ethanol stress. This study gains comprehensive insights into the K. marxianus transcriptome under various stresses during high-temperature ethanol fermentation, providing rich information for further metabolic engineering towards improved stress tolerance and ethanol production. SN - 1432-0614 UR - https://www.unboundmedicine.com/medline/citation/30673809/Understanding_the_stress_responses_of_Kluyveromyces_marxianus_after_an_arrest_during_high_temperature_ethanol_fermentation_based_on_integration_of_RNA_Seq_and_metabolite_data_ DB - PRIME DP - Unbound Medicine ER -