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Changes in cell wall structure and protein set in Candida maltosa grown on hexadecane

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Abstract

The yeast Candida maltosa is a model organism for studying adaptive changes in the structure and function of the cell wall when consuming water-insoluble nutrient sources. The cells of C. maltosa that utilize hydrocarbons contain supramolecular structures, so-called “canals” in the cell wall. Differences in protein profiles of culture liquids and cell wall extracts of C. maltosa grown on glucose and hexadecane were analyzed. Three proteins specific of cells grown on hexadecane were revealed using mass spectrometry: glycosyl hydrolase EPD2 in the culture liquid; a protein belonging to the cytochrome C family in the 0.5 mol/L NaCl extract; and PPIA_CANAL protein known as chaperone, in the 0.1% SDS extract. The possible role of these proteins in cell wall structures responsible for adaptation to hexadecane utilization is discussed.

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References

  • Beier A, Hahn V, Bornscheuer UT, Schauer F (2014) Metabolism of alkenes and ketones by Candida maltosa and related yeasts. AMB Express 4, eCollection 2014. https://doi.org/10.1186/s13568-014-0075-2

  • Davì V, Chevalier L, Guo H, Tanimoto H, Barrett K, Couturier E, Boudaoud A, Minc N (2019) Systematic mapping of cell wall mechanics in the regulation of cell morphogenesis. Proc Natl Acad Sci U S A116(28):13833–13838. https://doi.org/10.1073/pnas.1820455116

    Article  CAS  Google Scholar 

  • Dižová S, Černáková L, Bujdáková H (2018) The impact of farnesol in combination with fluconazole on Candida albicans biofilm: regulation of ERG20, ERG9, and ERG11 genes. Folia Microbiol 63:363–337. https://doi.org/10.1007/s12223-017-0574-z

    Article  CAS  Google Scholar 

  • Dmitriev VV, Crowley DE, Rogachevsky VV, Negri CM, Rusakova TG, Kolesnikova SA, Akhmetov LI (2011) Microorganisms form exocellular structures, trophosomes, to facilitate biodegradation of oil in aqueous media. FEMS Microbiol Lett 315:134–140

    Article  CAS  Google Scholar 

  • Dmitriev VV, Crowley DE, Zvonarev AN, Rusakova TG, Negri CM, Kolesnikova SA (2016) Modifications of the cell wall of yeasts grown on hexadecane and under starvation conditions. Yeast 33:55–62

    Article  CAS  Google Scholar 

  • Finogenova TV, Morgunov IG, Kamzolova SV, Chernyavskaya OG (2005) Organic acid production by the yeast Yarrowia lipolytica: a review of prospects. Appl Biochem Microbiol 41:418–425

    Article  CAS  Google Scholar 

  • Fukuda R (2013) Metabolism of hydrophobic carbon sources and regulation of it in n-alkane-assimilating yeast Yarrowia lipolytica. Biosci Biotechnol Biochem 77:1149–1154

    Article  CAS  Google Scholar 

  • Fukuda R, Ohta A (2017) Genetic features and regulation of n-alkane metabolism in yeasts. In: Rojo F (ed) Aerobic utilization of hydrocarbons, oils and lipids. Handbook of hydrocarbon and lipid microbiology. Springer, Cham

    Google Scholar 

  • Galat A (2003) Peptidylprolyl cis/trans isomerases (immunophilins): biological diversity-targets functions. Curr Top Med Chem 3:1315–1347

    Article  CAS  Google Scholar 

  • Garcia-Rubio R, de Oliveira HC, Rivera J, Trevijano-Contador N (2020) The fungal cell wall: Candida, Cryptococcus, and Aspergillus species. Front Microbiol 10:2993. https://doi.org/10.3389/fmicb.2019.02993 eCollection 2019

    Article  PubMed  PubMed Central  Google Scholar 

  • Hirai K (1971) Comparison between 3,3'-diaminobenzidine and auto-oxidized 3,3 '-diaminobenzidine in the cytochemical demonstration of oxidative enzymes. J Histochem Cytochem 19:434–442

    Article  CAS  Google Scholar 

  • Huang C, Zhao F, Lin Y, Zheng S, Liang S, Han S (2018) RNA-Seq analysis of global transcriptomic changes suggests a roles for the MAPK pathway and carbon metabolism in cell wall maintenance in a Saccharomyces cerevisiae FKS1 mutant. Biochem Biophys Res Commun 500:603–608

    Article  CAS  Google Scholar 

  • Iwama R, Kobayashi S, Ishimaru C, Ohta A, Horiuchi H, Fukuda R (2016) Functional roles and substrate specificities of twelve cytochromes P450 belonging to CYP52 family in n-alkane assimilating yeast Yarrowia lipolytica. Fungal Genet Biol 91:43–54

    Article  CAS  Google Scholar 

  • Kawamoto S, Tanaka A, Yamamura M, Teranishi Y, Fukui S (1977) Microbody of n-alkane-grown yeast. Arch. Microbiol. 112(1977):1–8

    Article  CAS  Google Scholar 

  • Kelly SL, Kelly DE (2013) Microbial cytochromes P450: biodiversity and biotechnology. Where do cytochromes P450 come from, what do they do and what can they do for us? Phil Trans R Soc B 368. https://doi.org/10.1098/rstb.2012.0476

  • Klis FM, de Jong M, Brul S, de Groot PW (2007) Extraction of cell surface associated proteins from living yeast cells. Yeast 24:253–258

    Article  CAS  Google Scholar 

  • Kogure T, Horiuchi H, Matsuda H, Arie M, Takagi M, Ohta A (2007) Enhanced induction of cytochromes P450alk that oxidize methyl-ends of n-alkanes and fatty acids in the long-chain dicarboxylic acid-hyperproducing mutant of Candida maltosa. FEMS Microbiol Lett 271:106–111

    Article  CAS  Google Scholar 

  • Kogure T, Takagi M, Ohta A (2005) n-Alkane and clofibrate, a peroxisome proliferator, activate transcription of ALK2 gene encoding cytochrome P450alk2 through distinct cis-acting promoter elements in Candida maltosa. Biochem Biophys Res Commun 329:78–86

    Article  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  Google Scholar 

  • Liu ZL, Wang X, Weber SA (2018) Tolerant industrial yeast Saccharomyces cerevisiae possess a more robust cell wall integrity signaling pathway against 2-furaldehyde and 5-(hydroxymethyl)-2-furaldehyde. J Biotechnol 276–277:15–24

    Article  Google Scholar 

  • Mauersberger S, Kärgel E, Matyashova RN, Müller HG (1987) Subcellular organization of alkane oxidation in the yeast Candida maltosa. J Basic Microbiol 27:565–582

    Article  CAS  Google Scholar 

  • Mauersberger S, Ohkuma M, Schunck WH, Takagi M (1996) Candida maltosa. In: Wolf K (ed) Nonconventional Yeasts in Biotechnology. Springer, Berlin, pp 411–580

    Chapter  Google Scholar 

  • Molon M, Woznicka O, Zebrowski J (2018) Cell wall biosynthesis impairment affects the budding lifespan of the Saccharomyces cerevisiae yeast. Biogerontology 19:67–79

    Article  CAS  Google Scholar 

  • Mori K, Iwama R, Kobayashi S, Horiuchi H, Fukuda R, Ohta A (2013) Transcriptional repression by glycerol of genes involved in the assimilation of n-alkanes and fatty acids in yeast Yarrowia lipolytica. FEMS Yeast Res 13:233–240

    Article  CAS  Google Scholar 

  • Nakazawa T, Takahashi M, Horiuchi H, Ohta A, Takagi M (2000) Cloning and characterization of EPD2, a gene required for efficient pseudohyphal formation of a dimorphic yeast, Candida maltosa. Biosci Biotechnol Biochem 64:369–377

    Article  CAS  Google Scholar 

  • Ohkuma M, Muraoka SI, Tanimoto T, Fujii M, Ohta A, Takagi M (1995) CYP52 (Cytochrome P450alk) multigene family in Candida maltosa: identification and characterization of eight members. DNA Cell Biol 14:163–173

    Article  CAS  Google Scholar 

  • Ohkuma M, Tanimoto T, Yano K, Takagi M (1991) CYP52 (Cytochrome P450alk) multigene family in Candida maltosa: molecular cloning and nucleotide sequence of the two tandemly arranged genes. DNA Cell Biol 10:271–282

    Article  CAS  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  CAS  Google Scholar 

  • Sabirzyanov FA, Sabirzyanova TA, Rekstina VV, Adzhubei AA, Kalebina TS (2018) C-Terminal sequence is involved in the incorporation of Bgl2p glucanosyltransglycosylase in the cell wall of Saccharomyces cerevisiae. FEMS Yeast Res 18. https://doi.org/10.1093/femsyr/fox093

  • Sanz AB, García R, Rodríguez-Peña JM, Arroyo J (2017) The CWI Pathway: regulation of the transcriptional adaptive response to cell wall stress in yeast. J Fungi 4. https://doi.org/10.3390/jof4010001

  • Schägger H, von Jagow G (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379

    Article  Google Scholar 

  • Schunck W-H, Kärgel E, Gross B, Wiedmann B, Mauersberger S, Köpke K, Kießling U, Strauss M, Gaestel MM, Müller H-G (1989) Molecular cloning and characterization of the primary structure of the alkane hydroxylating cytochrome P450 from the yeast Candida maltosa. Biochem Biophys Res Commun 161:843–850

    Article  CAS  Google Scholar 

  • Suchodolski J, Derkacz D, Muraszko J, Panek JJ, Jezierska A, Łukaszewicz M, Krasowska A (2020) Fluconazole and lipopeptide surfactin interplay during Candida albicans plasma membrane and cell wall remodeling increases fungal immune system exposure. Pharmaceutics 12(4):E314. https://doi.org/10.3390/pharmaceutics12040314

    Article  CAS  PubMed  Google Scholar 

  • Takagi M, Ohkuma M, Kobayashi N, Watanabe W, Yano K (1989) Purification of cytochrome P-450alk from n-alkane-grown cells of Candida maltosa, and cloning and nucleotide sequencing of the encoding gene. Agric Biol Chem 53:2217–2226

    CAS  Google Scholar 

  • Vogel F, Kargel E, Schunck W-H (1991) In situ localization of cytochrome P-450, the first enzyme involved in aliphatic hydrocarbon degradation in the yeast Candida maltose. Prog Histochem Cytochem 23:383–389

    Article  CAS  Google Scholar 

  • Willaert RG (2018) Adhesins of yeasts: protein structure and interactions. J Fungi (Basel) 4(4):E119. https://doi.org/10.3390/jof4040119

    Article  CAS  Google Scholar 

  • Yeh YC, Wang HY, Lan CY (2020) Candida albicans Aro1 affects cell wall integrity, biofilm formation and virulence. J Microbiol Immunol Infect 53(1):115–124. https://doi.org/10.1016/j.jmii.2018.04.002

    Article  CAS  PubMed  Google Scholar 

  • Zvonarev AN, Crowley DE, Ryazanova LP, Lichko LP, Rusakova TG, Kulakovskaya TV, Dmitriev VV (2017) Cell wall canals formed upon growth of Candida maltosa in the presence of hexadecane are associated with polyphosphates. FEMS Yeast Res 17. https://doi.org/10.1093/femsyr/fox026

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Acknowledgements

Electron Microscopy Core Facilities of the Pushchino Center of Biological Research (http://www.ckp-rf.ru/ckp/670266/)

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Authors and Affiliations

  1. G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Pushchino Center for Biological Research of the Russian Academy of Sciences, prosp. Nauki 5, Pushchino, Moscow Region, 142290, Russia

    Anton Zvonarev, Vasilina Farofonova, Ekaterina Kulakovskaya, Tatiana Kulakovskaya, Andrey Machulin & Vladimir Dmitriev

  2. Belozersky Research Institute of Physico-Chemical Biology, MSU, Leninskiye Gory, Moscow, 119899, Russia

    Svyatoslav Sokolov

Authors
  1. Anton Zvonarev
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  2. Vasilina Farofonova
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  3. Ekaterina Kulakovskaya
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  4. Tatiana Kulakovskaya
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  5. Andrey Machulin
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  6. Svyatoslav Sokolov
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  7. Vladimir Dmitriev
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Correspondence to Tatiana Kulakovskaya.

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Zvonarev, A., Farofonova, V., Kulakovskaya, E. et al. Changes in cell wall structure and protein set in Candida maltosa grown on hexadecane. Folia Microbiol 66, 247–253 (2021). https://doi.org/10.1007/s12223-020-00840-2

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  • DOI: https://doi.org/10.1007/s12223-020-00840-2

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