Transcriptomic Profiling of an Evolved Yarrowia Lipolytica Strain: Tackling Hexanoic Acid Fermentation to Increase Lipid Production from Short-chain Fatty Acids

Overview

Journal Microb Cell Fact

Publisher Biomed Central

Specialties Biotechnology
Microbiology

Date 2024 Apr 2

PMID 38566056

Authors

Sergio Morales-Palomo

Clara Navarrete

Jose Luis Martinez

Cristina Gonzalez-Fernandez

Elia Tomas-Pejo

Affiliations

Soon will be listed here.

Abstract

Background: Short-chain fatty acids (SCFAs) are cost-effective carbon sources for an affordable production of lipids. Hexanoic acid, the acid with the longest carbon chain in the SCFAs pool, is produced in anaerobic fermentation of organic residues and its use is very challenging, even inhibiting oleaginous yeasts growth.

Results: In this investigation, an adaptive laboratory evolution (ALE) was performed to improve Yarrowia lipolytica ACA DC 50109 tolerance to high hexanoic acid concentrations. Following ALE, the transcriptomic analysis revealed several genetic adaptations that improved the assimilation of this carbon source in the evolved strain compared to the wild type (WT). Indeed, the evolved strain presented a high expression of the up-regulated gene YALI0 E16016g, which codes for FAT1 and is related to lipid droplets formation and responsible for mobilizing long-chain acids within the cell. Strikingly, acetic acid and other carbohydrate transporters were over-expressed in the WT strain.

Conclusions: A more tolerant yeast strain able to attain higher lipid content under the presence of high concentrations of hexanoic acid has been obtained. Results provided novel information regarding the assimilation of hexanoic acid in yeasts.

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References

Drzymala-Kapinos K, Mironczuk A, Dobrowolski A . Lipid production from lignocellulosic biomass using an engineered Yarrowia lipolytica strain. Microb Cell Fact. 2022; 21(1):226. PMC: 9617373. DOI: 10.1186/s12934-022-01951-w. View

Liao Y, Smyth G, Shi W . featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013; 30(7):923-30. DOI: 10.1093/bioinformatics/btt656. View

Wu Y, Jameel A, Xing X, Zhang C . Advanced strategies and tools to facilitate and streamline microbial adaptive laboratory evolution. Trends Biotechnol. 2021; 40(1):38-59. DOI: 10.1016/j.tibtech.2021.04.002. View

Morales-Palomo S, Tomas-Pejo E, Gonzalez-Fernandez C . Phosphate limitation as crucial factor to enhance yeast lipid production from short-chain fatty acids. Microb Biotechnol. 2022; 16(2):372-380. PMC: 9871521. DOI: 10.1111/1751-7915.14197. View

Mavrommati M, Daskalaki A, Papanikolaou S, Aggelis G . Adaptive laboratory evolution principles and applications in industrial biotechnology. Biotechnol Adv. 2021; 54:107795. DOI: 10.1016/j.biotechadv.2021.107795. View

von Loeffelholz O, Pena A, Drummond D, Cross R, Moores C . Cryo-EM Structure (4.5-Å) of Yeast Kinesin-5-Microtubule Complex Reveals a Distinct Binding Footprint and Mechanism of Drug Resistance. J Mol Biol. 2019; 431(4):864-872. PMC: 6378684. DOI: 10.1016/j.jmb.2019.01.011. View

Young M, Wakefield M, Smyth G, Oshlack A . Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010; 11(2):R14. PMC: 2872874. DOI: 10.1186/gb-2010-11-2-r14. View

Wagner S, Paltauf F . Generation of glycerophospholipid molecular species in the yeast Saccharomyces cerevisiae. Fatty acid pattern of phospholipid classes and selective acyl turnover at sn-1 and sn-2 positions. Yeast. 1994; 10(11):1429-37. DOI: 10.1002/yea.320101106. View

Chaker-Margot M, Barandun J, Hunziker M, Klinge S . Architecture of the yeast small subunit processome. Science. 2016; 355(6321). DOI: 10.1126/science.aal1880. View

10.

Simpson-Lavy K, Kupiec M . Carbon Catabolite Repression in Yeast is Not Limited to Glucose. Sci Rep. 2019; 9(1):6491. PMC: 6482301. DOI: 10.1038/s41598-019-43032-w. View

11.

Tanimura A, Sugita T, Endoh R, Ohkuma M, Kishino S, Ogawa J . Lipid production via simultaneous conversion of glucose and xylose by a novel yeast, Cystobasidium iriomotense. PLoS One. 2018; 13(9):e0202164. PMC: 6135397. DOI: 10.1371/journal.pone.0202164. View

12.

Fukui T, Shiomi N, Doi Y . Expression and characterization of (R)-specific enoyl coenzyme A hydratase involved in polyhydroxyalkanoate biosynthesis by Aeromonas caviae. J Bacteriol. 1998; 180(3):667-73. PMC: 106937. DOI: 10.1128/JB.180.3.667-673.1998. View

13.

Lu R, Cao L, Wang K, Ledesma-Amaro R, Ji X . Engineering Yarrowia lipolytica to produce advanced biofuels: Current status and perspectives. Bioresour Technol. 2021; 341:125877. DOI: 10.1016/j.biortech.2021.125877. View

14.

Yamada K, Aiba K, Kitaura Y, Kondo Y, Nomura N, Nakamura Y . Clinical, biochemical and metabolic characterisation of a mild form of human short-chain enoyl-CoA hydratase deficiency: significance of increased N-acetyl-S-(2-carboxypropyl)cysteine excretion. J Med Genet. 2015; 52(10):691-8. DOI: 10.1136/jmedgenet-2015-103231. View

15.

Garrido-Godino A, Gutierrez-Santiago F, Navarro F . Biogenesis of RNA Polymerases in Yeast. Front Mol Biosci. 2021; 8:669300. PMC: 8136413. DOI: 10.3389/fmolb.2021.669300. View

16.

Winter D, Choe E, Li R . Genetic dissection of the budding yeast Arp2/3 complex: a comparison of the in vivo and structural roles of individual subunits. Proc Natl Acad Sci U S A. 1999; 96(13):7288-93. PMC: 22078. DOI: 10.1073/pnas.96.13.7288. View

17.

Beopoulos A, Mrozova Z, Thevenieau F, Le Dall M, Hapala I, Papanikolaou S . Control of lipid accumulation in the yeast Yarrowia lipolytica. Appl Environ Microbiol. 2008; 74(24):7779-89. PMC: 2607157. DOI: 10.1128/AEM.01412-08. View

18.

Greses S, Tomas-Pejo E, Gonzalez-Fernandez C . Agroindustrial waste as a resource for volatile fatty acids production via anaerobic fermentation. Bioresour Technol. 2019; 297:122486. DOI: 10.1016/j.biortech.2019.122486. View

19.

Daskalaki A, Perdikouli N, Aggeli D, Aggelis G . Laboratory evolution strategies for improving lipid accumulation in Yarrowia lipolytica. Appl Microbiol Biotechnol. 2019; 103(20):8585-8596. DOI: 10.1007/s00253-019-10088-7. View

20.

Dobrowolski A, Drzymala K, Mitula P, Mironczuk A . Production of tailor-made fatty acids from crude glycerol at low pH by Yarrowia lipolytica. Bioresour Technol. 2020; 314:123746. DOI: 10.1016/j.biortech.2020.123746. View