Stress Resistance of Saccharomyces cerevisiae Strains Overexpressing Yeast Polyphosphatases
Abstract
:1. Introduction
2. Materials and Methods
2.1. Strains and Growth Conditions
2.2. Pi and polyP Extraction and Assay
2.3. Polyphosphatase Activity Assay
2.4. Determination of Yeast Sensitivity to Peroxide, Alkali, and Heavy Metal Ions
2.5. Statistics
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Rao, N.N.; Gómez-García, M.R.; Kornberg, A. Inorganic Polyphosphate: Essential for Growth and Survival. Annu. Rev. Biochem. 2009, 78, 605–647. [Google Scholar] [CrossRef] [PubMed]
- Albi, T.; Serrano, A. Inorganic polyphosphate in the microbial world. Emerging roles for a multifaceted biopolymer. World J. Microbiol. Biotechnol. 2016, 32, 27. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xie, L.; Jakob, U. Inorganic Polyphosphate, a Multifunctional Polyanionic Protein Scaffold. J. Biol. Chem. 2019, 294, 2180–2190. [Google Scholar] [CrossRef] [Green Version]
- Desfougères, Y.; Saiardi, A.; Azevedo, C. Inorganic Polyphosphate in Mammals: Where’s Wally? Biochem. Soc. Trans. 2020, 48, 95–101. [Google Scholar] [CrossRef] [Green Version]
- Rosigkeit, H.; Kneißle, L.; Obruča, S.; Jendrossek, D. The Multiple Roles of Polyphosphate in Ralstonia eutropha and Other Bacteria. Microb. Physiol. 2021, 31, 63–177. [Google Scholar] [CrossRef] [PubMed]
- Denoncourt, A.; Downey, M. Model Systems for Studying Polyphosphate Biology: A Focus on Microorganisms. Curr. Genet. 2021, 67, 331–346. [Google Scholar] [CrossRef] [PubMed]
- Ropelewska, M.; Gross, M.H.; Konieczny, I. DNA and Polyphosphate in Directed Proteolysis for DNA Replication Control. Front. Microbiol. 2020, 11, 585717. [Google Scholar] [CrossRef]
- Sultana, S.; Foti, A.; Dahl, J.U. Bacterial Defense Systems against the Neutrophilic Oxidant Hypochlorous Acid. Infect. Immun. 2020, 88, e00964-19. [Google Scholar] [CrossRef] [PubMed]
- Gross, M.H.; Konieczny, I. Polyphosphate Induces the Proteolysis of ADP-bound Fraction of Initiator to Inhibit DNA Replication Initiation upon Stress in Escherichia coli. Nucleic Acids Res. 2020, 48, 5457–5466. [Google Scholar] [CrossRef]
- Beaufay, F.; Quarles, E.; Franz, A.; Katamanin, O.; Wholey, W.Y.; Jakob, U. Polyphosphate Functions In Vivo as an Iron Chelator and Fenton Reaction Inhibitor. mBio 2020, 11, e01017-20. [Google Scholar] [CrossRef]
- Sanz-Luque, E.; Bhaya, D.; Grossman, A.R. Polyphosphate: A Multifunctional Metabolite in Cyanobacteria and Algae. Front. Plant Sci. 2020, 11, 938. [Google Scholar] [CrossRef] [PubMed]
- Kulakovskaya, T. Inorganic Polyphosphates and Heavy Metal Resistance in Microorganisms. World J. Microbiol. Biotechnol. 2018, 34, 139. [Google Scholar] [CrossRef] [PubMed]
- Rivero, M.; Torres-Paris, C.; Muñoz, R.; Cabrera, R.; Navarro, C.A.; Jerez, C.A. Inorganic Polyphosphate, Exopolyphosphatase, and Pho84-like Transporters May Be Involved in Copper Resistance in Metallosphaera sedula DSM 5348T. Archaea 2018, 2018, 5251061. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Villagrasa, E.; Egea, R.; Ferrer-Miralles, N.; Solé, A. Genomic and Biotechnological Insights on Stress-linked Polyphosphate Production Induced by Chromium(III) in Ochrobactrum anthropi DE2010. World J. Microbiol. Biotechnol. 2020, 36, 97. [Google Scholar] [CrossRef] [PubMed]
- Reddi, A.R.; Jensen, L.T.; Culotta, V.C. Manganese homeostasis in Saccharomyces cerevisiae. Chem. Rev. 2009, 109, 4722–4732. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dai, S.; Xie, Z.; Wang, B.; Yu, N.; Zhao, J.; Zhou, Y.; Hua, Y.; Tian, B. Dynamic Polyphosphate Metabolism Coordinating with Manganese Ions Defends against Oxidative Stress in the Extreme Bacterium Deinococcus radiodurans. Appl. Environ. Microbiol. 2021, 87, e02785-20. [Google Scholar] [CrossRef]
- Vagabov, V.M.; Trilisenko, L.V.; Kulakovskaya, T.V.; Kulaev, I.S. Effect of a Carbon Source on Polyphosphate Accumulation in Saccharomyces Cerevisiae. FEMS Yeast Res. 2008, 8, 877–882. [Google Scholar] [CrossRef] [Green Version]
- Christ, J.J.; Blank, L.M. Saccharomyces cerevisiae Containing 28% Polyphosphate and Production of a Polyphosphate-Rich Yeast Extract Thereof. FEMS Yeast Res. 2019, 19, foz011. [Google Scholar] [CrossRef]
- Bru, S.; Martínez-Laínez, J.M.; Hernández-Ortega, S.; Quandt, E.; Torres-Torronteras, J.; Martí, R.; Canadell, D.; Ariño, J.; Sharma, S.; Jiménez, J.; et al. Polyphosphate Is Involved in Cell Cycle Progression and Genomic Stability in Saccharomyces cerevisiae. Mol. Microbiol. 2016, 101, 367–380. [Google Scholar] [CrossRef] [Green Version]
- Serra-Cardona, A.; Canadell, D.; Ariño, J. Coordinate Responses to Alkaline pH Stress in Budding Yeast. Microb. Cell 2015, 2, 182–196. [Google Scholar] [CrossRef] [Green Version]
- Trilisenko, L.; Zvonarev, A.; Valiakhmetov, A.; Penin, A.A.; Eliseeva, I.A.; Ostroumov, V.; Kulakovskiy, I.V.; Kulakovskaya, T. The Reduced Level of Inorganic Polyphosphate Mobilizes Antioxidant and Manganese-Resistance Systems in Saccharomyces cerevisiae. Cells 2019, 8, 461. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ikeh, M.; Ahmed, Y.; Quinn, J. Phosphate Acquisition and Virulence in Human Fungal Pathogens. Microorganisms 2017, 5, 48. [Google Scholar] [CrossRef]
- Köhler, J.R.; Acosta-Zaldívar, M.; Qi, W. Phosphate in Virulence of Candida albicans and Candida glabrata. J. Fungi 2020, 6, 40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Andreeva, N.; Ryazanova, L.; Dmitriev, V.; Kulakovskaya, T.; Kulaev, I. Adaptation of Saccharomyces cerevisiae to Toxic Manganese Concentration Triggers Changes in Inorganic Polyphosphates. FEMS Yeast Res. 2013, 13, 463–470. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Andreeva, N.; Ryazanova, L.; Dmitriev, V.; Kulakovskaya, T.; Kulaev, I. Cytoplasmic inorganic polyphosphate participates in the heavy metal tolerance of Cryptococcus humicola. Folia Microbiol. 2014, 59, 381–3899. [Google Scholar] [CrossRef] [PubMed]
- Hovnanyan, K.; Marutyan, S.; Marutyan, S.; Hovnanyan, M.; Navasardyan, L.; Trchounian, A. Ultrastructural Investigation of Acidocalcisomes and ATPase Activity in Yeast Candida Guilliermondii NP-4 as ‘Complementary’ Stress-Targets. Lett. Appl. Microbiol. 2020, 71, 413–419. [Google Scholar] [CrossRef]
- Wurst, H.; Shiba, T.; Kornberg, A. The Gene for a Major Exopolyphosphatase of Saccharomyces cerevisiae. J. Bacteriol. 1995, 177, 898–906. [Google Scholar] [CrossRef] [Green Version]
- Andreeva, N.; Trilisenko, L.; Eldarov, M.; Kulakovskaya, T. Polyphosphatase PPN1 of Saccharomyces cerevisiae: Switching of Exopolyphosphatase and Endopolyphosphatase Activities. PLoS ONE 2015, 10, e0119594. [Google Scholar] [CrossRef]
- Lonetti, A.; Szijgyarto, Z.; Bosch, D.; Loss, O.; Azevedo, C.; Saiardi, A. Identification of an Evolutionarily Conserved Family of Inorganic Polyphosphate Endopolyphosphatases. J. Biol. Chem. 2011, 286, 31966–31974. [Google Scholar] [CrossRef] [Green Version]
- Gerasimait, R.; Mayer, A. Ppn2, a Novel Zn2+-Dependent Polyphosphatase in the Acidocalcisome-like Yeast Vacuole. J. Cell Sci. 2017, 130, 1625–1636. [Google Scholar] [CrossRef] [Green Version]
- Andreeva, N.; Ledova, L.; Ryazanova, L.; Tomashevsky, A.; Kulakovskaya, T.; Eldarov, M. Ppn2 Endopolyphosphatase Overexpressed in Saccharomyces cerevisiae: Comparison with Ppn1, Ppx1, and Ddp1 Polyphosphatases. Biochimie 2019, 163, 101–107. [Google Scholar] [CrossRef] [PubMed]
- Ryazanova, L.P.; Ledova, L.A.; Andreeva, N.A.; Zvonarev, A.N.; Eldarov, M.A.; Kulakovskaya, T.V. Inorganic Polyphosphate and Physiological Properties of Saccharomyces cerevisiae Yeast Overexpressing Ppn2. Biochemistry 2020, 85, 516–522. [Google Scholar] [CrossRef]
- Eldarov, M.A.; Baranov, M.V.; Dumina, M.V.; Shgun, A.A.; Andreeva, N.A.; Trilisenko, L.V.; Kulakovskaya, T.V.; Ryasanova, L.P.; Kulaev, I.S. Polyphosphates and Exopolyphosphatase Activities in the Yeast Saccharomyces cerevisiae under Overexpression of Homologous and Heterologous PPN1 Genes. Biochemistry 2013, 78, 946–953. [Google Scholar] [CrossRef] [PubMed]
- Sethuraman, A.; Rao, N.N.; Kornberg, A. The Endopolyphosphatase Gene: Essential in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 2001, 98, 8542–8547. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heinonen, J.K.; Lahti, R.J. A New and Convenient Colorimetric Determination of Inorganic Orthophosphate and its Application to the Assay of Inorganic Pyrophosphatase. Anal. Biochem. 1981, 113, 313–317. [Google Scholar] [CrossRef]
- Morrissette, V.A.; Rolfes, R.J. The Intersection Between Stress Responses and Inositol Pyrophosphates in Saccharomyces cerevisiae. Curr. Genet. 2020, 66, 901–910. [Google Scholar] [CrossRef]
- Qiu, D.; Eisenbeis, V.B.; Saiardi, A.; Jessenm, H.J. Absolute Quantitation of Inositol Pyrophosphates by Capillary Electrophoresis Electrospray Ionization Mass Spectrometry. J. Vis. Exp. 2021, 174, e62847. [Google Scholar] [CrossRef]
- Pascual-Ortiz, M.; Walla, E.; Fleig, U.; Saiardi, A. The PPIP5K Family Member Asp1 Controls Inorganic Polyphosphate Metabolism in S. pombe. J. Fungi 2021, 37, 626. [Google Scholar] [CrossRef]
- Desfougères, Y.; Portela-Torres, P.; Qiu, D.; Livermore, T.M.; Harmel, R.K.; Borghi, F.; Jessen, H.J.; Fiedler, D.; Saiardi, A. The Inositol Pyrophosphate Metabolism of Dictyostelium discoideum does not Regulate Inorganic Polyphosphate (polyP) Synthesis. Adv. Biol. Regul. 2021, 10, 100835. [Google Scholar] [CrossRef]
- De la Torre-Ruiz, M.A.; Mozo-Villarías, A.; Pujol, N.; Petkova, M.I. How Budding Yeast Sense and Transduce the Oxidative Stress Signal and the Impact in Cell Growth and Morphogenesis. Curr. Protein Pept. Sci. 2010, 11, 669–679. [Google Scholar] [CrossRef]
- Li, C.; Yu, J.; Wang, D.; Li, L.; Yang, X.; Ma, H.; Xu, Y. Efficient Removal of Zinc by Multi-stress-tolerant Yeast Pichia kudriavzevii A16. Bioresour. Technol. 2016, 206, 43–49. [Google Scholar] [CrossRef] [PubMed]
- Qiu, L.; Feng, J.; Dai, Y.; Chang, S. Biosorption of Strontium Ions from Simulated High-level Liquid Waste by Living Saccharomyces cerevisiae. Environ. Sci. Pollut. Res. 2018, 25, 17194–17206. [Google Scholar] [CrossRef] [PubMed]
- Sun, G.L.; Reynolds, E.E.; Belcher, A.M. Designing Yeast as Plant-like Hyperaccumulators for Heavy Metals. Nat. Commun. 2019, 10, 5080. [Google Scholar] [CrossRef] [PubMed]
Strain | Cell-Free Extract | Crude Membrane Fraction |
---|---|---|
CRN | 0.342 ± 0.033 | 0.094 ± 0.005 |
CRN/PPX1 | 8.04 ± 0.44 | 1.72 ± 0.04 |
CRN/PPN1 | 1.64 ± 0.123 | 4.6 ± 0.18 |
CRN/PPN2 | 0.874 ± 0.44 | 0.39 ± 0.023 |
CRN/DDP1 | 0.22 ± 0.0136 | 0.099 ± 0.0072 |
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Andreeva, N.; Ryazanova, L.; Ledova, L.; Trilisenko, L.; Kulakovskaya, T. Stress Resistance of Saccharomyces cerevisiae Strains Overexpressing Yeast Polyphosphatases. Stresses 2022, 2, 17-25. https://doi.org/10.3390/stresses2010002
Andreeva N, Ryazanova L, Ledova L, Trilisenko L, Kulakovskaya T. Stress Resistance of Saccharomyces cerevisiae Strains Overexpressing Yeast Polyphosphatases. Stresses. 2022; 2(1):17-25. https://doi.org/10.3390/stresses2010002
Chicago/Turabian StyleAndreeva, Nadeshda, Lubov Ryazanova, Larisa Ledova, Ludmila Trilisenko, and Tatiana Kulakovskaya. 2022. "Stress Resistance of Saccharomyces cerevisiae Strains Overexpressing Yeast Polyphosphatases" Stresses 2, no. 1: 17-25. https://doi.org/10.3390/stresses2010002