journal article·2021-04-29Open access

Lipid Remodeling in the Mitochondria upon Ageing during the Long-Lasting Cultivation of Endomyces magnusii

Elena P. Isakova, Natalya N. Gessler, Daria I. Dergacheva, Vera M. Tereshina, Yulia I. Deryabina, Marek Kieliszek

Applied Sciences· Volume 11· Issue 9

Abstract

In this study, we used Endomyces magnusii yeast with a complete respiratory chain and well-developed mitochondria system. This system is similar to the animal one which makes the yeast species an excellent model for studying ageing mechanisms. Mitochondria membranes play a vital role in the metabolic processes in a yeast cell. Mitochondria participate in the metabolism of several pivotal compounds including fatty acids (FAs) metabolism. The mitochondria respiratory activity, the membrane and storage lipids composition, and morphological changes in the culture during the long-lasting cultivation (for 168 h) were under investigation. High metabolic activity of E. magnusii might be related to the active function of mitochondria increasing in the 96- and 168-h growth phases. Cardiolipin (CL), phosphatidylethanolamine (PE), phosphatidylcholine (PC), and sterols (St) were dominant in the membrane lipids. The St and sphingolipids (SL) shares increased by a lot, whereas the CL and phosphatidylinositol (PI) + PE ones decreased in the membrane lipids. This was the main change in the membrane lipid composition during the cultivation. In contrast, the amount of PE and phosphatidylserine (PS) did not change. Index of Hydrogen Deficiency (IHD) of phospholipids (PL) FAs significantly declined due to a decrease in the linoleic acid share and an increase in the amount of palmitic and oleic acid. There were some storage lipids in the mitochondria where free fatty acids (FFAs) (73–99% of the total) dominated, reaching the highest level in the 96-h phase. Thus, we can conclude that upon long-lasting cultivation, for the yeast assimilating an “oxidative” substrate, the following factors are of great importance in keeping longevity: (1) a decrease in the IHD reduces double bonds and the peroxidation indices of various lipid classes; (2) the amount of long-chain FFAs declines. Moreover, the factor list providing a long lifespan should include some other physiological features in the yeast cell. The alternative oxidase activity induced in the early stationary growth phase and high mitochondria activity maintains intensive oxygen consumption. It determines the ATP production and physiological doses of reactive oxygen species (ROS), which could be regarded as a trend favoring the increased longevity.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Mitochondrial Function and Pathology · Lipid metabolism and biosynthesis · Microbial Metabolic Engineering and Bioproduction

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Research Center of Biotechnology of the Russian Academy of Sciences, A.N. Bach Institute of Biochemistry, bld 33-2, Leninsky Prospect, 119071 Moscow, Russia

Research Center of Biotechnology of the Russian Academy of Sciences, Winogradsky Institute of Microbiology, bld 33-2, Leninsky Prospect, 119071 Moscow, Russia

Department of Food Biotechnology and Microbiology, Institute of Food Sciences, Warsaw University of Life Sciences—SGGW, Nowoursynowska 159c, 02-776 Warsaw, Poland

References (57)

Show source-provided references
1. The multifaceted contributions of mitochondria to cellular metabolism10.1038/s41556-018-0124-1 ↗
2. Rogov, A.G., Goleva, T.N., Epremyan, K.K., Kireev, I.I., and Zvyagilskaya, R.A. (2021). Propagation of Mitochondria-Derived Reactive Oxygen Species within the Dipodascus magnusii Cells. Antioxidants, 10.10.3390/antiox10010120 ↗
3. Mitochondria: In sickness and in health10.1016/j.cell.2012.02.035 ↗
4. Annesley, S.J., and Fisher, P.R. (2019). Mitochondria in Health and Disease. Cells, 8.10.3390/cells8070680 ↗
5. The hallmarks of aging10.1016/j.cell.2013.05.039 ↗
7. The role of mitochondria in aging10.1172/JCI120842 ↗
8. Mitochondria in the signaling pathways that control longevity and health span10.1016/j.arr.2019.100940 ↗
9. Oxidative stress and aging: Learning from yeast lessons10.1016/j.funbio.2017.12.003 ↗
10. Lessons on longevity from budding yeast10.1038/nature08981 ↗
11. Exploring the power of yeast to model aging and age-related neurodegenerative disorders10.1007/s10522-016-9666-4 ↗
12. Redox control and oxidative stress in yeast cells10.1016/j.bbagen.2007.12.004 ↗
13. Sphingolipids and lifespan regulation10.1016/j.bbalip.2013.08.006 ↗
14. Mitochondria to nucleus signaling and the role of ceramide in its integration into the suite of cell quality control processes during aging10.1016/j.arr.2014.12.007 ↗
15. Mechanisms underlying the essential role of mitochondrial membrane lipids in yeast chronological aging10.1155/2017/2916985 ↗
16. Handee, W., Li, X., Hall, K.W., Deng, X., Li, P., Benning, C., Williams, B.L., and Kuo, M.-H. (2016). An energy-independent pro-longevity function of triacylglycerol in yeast. PLoS Genet., 12.10.1371/journal.pgen.1005878 ↗
17. Mitochondrial membrane lipidome defines yeast longevity10.18632/aging.100578 ↗
18. A mitochondrially targeted compound delays aging in yeast through a mechanism linking mitochondrial membrane lipid metabolism to mito-chondrial redox biology10.1016/j.redox.2014.01.011 ↗
19. Specific changes in mitochondrial lipidome alter mitochondrial proteome and increase the geroprotective efficiency of lithocholic acid in chronologically aging yeast10.18632/oncotarget.16766 ↗
20. Rsf1p is required for an efficient metabolic shift from fermentative to glycerol-based respiratory growth in S. cerevisiae10.1002/yea.1655 ↗
21. Inhibition of free radical scavenging enzymes affects mitochondrial membrane permeability transition during growth and aging of yeast cells10.1007/s10863-014-9582-8 ↗
22. Isakova, E.P., Matushkina, I.N., Popova, T.N., Dergacheva, D.I., Gessler, N.N., Klein, O.I., Semenikhina, A.V., Deryabina, Y.I., La Porta, N., and Saris, N.L. (2020). Metabolic remodeling during long-lasting cultivation of the Endomyces magnusii yeast on oxidative and fermentative substrates. Microorganisms, 8.10.3390/microorganisms8010091 ↗
23. Breitenbach, M., Jazwinski, S., and Laun, P. (2011). Aging and the survival of quiescent and non-quiescent cells in yeast stationary-phase cultures. Aging Research in Yeast, Springer. Subcellular Biochemistry.10.1007/978-94-007-2561-4 ↗
24. Fatty acids induced uncoupling of Saccharomyces cerevisiae mitochondria requires an intact ADP/ATP carrier10.1016/S0014-5793(97)00778-3 ↗
25. Regulation and physiological role of cyanide-resistant oxidases in fungi and plants
26. Physiological role of alternative oxidase (from yeasts to plants)
27. Cyanide-insensitive respiration. II. Control of the alternate pathway10.1016/S0021-9258(19)43949-5 ↗
28. Reverse electron transfer in mitochondria of the yeast Endomyces magnusii grown on glycerol
29. Exploring the metabolic and genetic control of gene expression on a genomic scale10.1126/science.278.5338.680 ↗
30. Transcriptome profiling of Saccharomyces cerevisiae during a transition from fermentative to glycerol-based respiratory growth reveals extensive metabolic and structural remodeling10.1007/s00438-006-0133-9 ↗
31. The yeast mitochondrial proteome, a study of fermentative and respiratory growth10.1074/jbc.M310160200 ↗
32. Quantitative variations of the mitochondrial proteome and phosphoproteome during fermentative and respiratory growth in Saccharomyces cerevisiae10.1016/j.jprot.2014.04.022 ↗
33. Cyanide-resistant respiration, a very frequent metabolic pathway in yeasts10.1016/S1567-1356(03)00036-9 ↗
34. Alternative oxidase: A mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants10.3390/ijms14046805 ↗
35. Alternative oxidase and plant stress tolerance10.1080/15592324.2016.1256530 ↗
36. Alternative oxidase: A target and regulator of stress responses10.1111/j.1399-3054.2009.01240.x ↗
37. Adaptive response to oxidative stress: Bacteria, fungi, plants, and animals10.1016/j.cbpc.2010.10.004 ↗
38. The slim, the fat, and the obese: Guess who lives the longest?10.1007/s00294-016-0617-z ↗
39. Yeast lipid metabolism at a glance10.1111/1567-1364.12141 ↗
40. The topology and regulation of cardiolipin biosynthesis and remodeling in yeast10.1016/j.chemphyslip.2013.10.008 ↗
41. Role of phospholipids in respiratory cytochrome bc (1) complex catalysis and supercomplex formation10.1016/j.bbabio.2009.02.012 ↗
42. Cellular functions of cardiolipin in yeast10.1016/j.bbamcr.2008.07.024 ↗
43. Cardiolipin and mitochondrial phosphatidylethanolamine have overlapping functions in mitochondrial fusion in Saccharomyces cerevisiae10.1074/jbc.M111.330167 ↗
44. Cardiolipin membrane domains in prokaryotes and eukaryotes10.1016/j.bbamem.2009.04.003 ↗
45. Membrane lipid composition regulates tubulin interaction with mitochondrial voltage-dependent anion channel10.1074/jbc.M112.378778 ↗
46. Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae10.1128/jb.173.6.2026-2034.1991 ↗
47. Metabolic link between phosphatidylethanolamine and triacylglycerol metabolism in the yeast Saccharomyces cerevisiae10.1016/j.bbalip.2011.08.007 ↗
48. Effect of selenium on lipid and amino acid metabolism in yeast cells10.1007/s12011-018-1342-x ↗
49. Sekova, V.Y., Dergacheva, D.I., Isakova, E.P., Gessler, N.N., Tereshina, V.M., and Deryabina, Y.I. (2019). Soluble sugar and lipid readjustments in the Yarrowia lipolytica yeast at various temperatures and pH. Metabolites, 9.10.3390/metabo9120307 ↗
50. Involvement of small heat shock proteins, trehalose, and lipids in the thermal stress management in Schizosaccharomyces pombe10.1007/s12192-015-0662-4 ↗
51. The Ca2+-Transport system of Yeast (Endomyces magnusii) mitochondria: Independent pathways for Ca2+ uptake and release
52. Stimulation of the yeast mitochondrial calcium uniporter by hypotonicity and by ruthenium red10.1016/S0005-2736(98)00004-2 ↗
53. Separation of the lipids of photosynthetic tissues: Improvements in analysis by thin-layer chromatography10.1016/0006-3002(63)90771-6 ↗
54. Work, T.S., and Work, E. (1972). Techniques of lipidology: Isolation, analysis and identifcation of lipids. Laboratory Techniques in Biochemistry and Molecular Biology, North-Holland.
55. Accumulation of a novel glycolipid and a betaine lipid in cells of Rhodobacter sphaeroides grown under phosphate limitation10.1006/abbi.1995.1141 ↗
56. Kates, M. (1988). Techniques of Lipidology: Isolation, Analysis, and Identification of Lipids, Elsevier. [2nd ed.].
57. Kritchevsky, D. (1974). Introduction to fungal lipids. Fungal Lipid Biochemistry, Springer.