Abstract
Fungi that tolerate very high environmental NaCl concentrations are good model systems to study mechanisms that enable them to endure osmotic and salinity stress. The whole genome sequences of six such fungal species have been analysed: Hortaea werneckii, Wallemia ichthyophaga and four Aureobasidium spp.: A. pullulans, A. subglaciale, A. melanogenum and A. namibiae. These fungi show different levels of halotolerance, with the presence of numerous membrane transport systems uncovered here that are believed to maintain physiological intracellular concentrations of alkali metal cations. Despite some differences, the intracellular cation contents of H. werneckii, A. pullulans and W. ichthyophaga remain low even under extreme extracellular salinities, which suggests that these species have efficient cation transport systems. We speculate that cation transporters prevent intracellular accumulation of Na+, and thus avoid the toxic effects that such Na+ accumulation would have, while also maintaining the high K+/Na+ ratio that is required for the full functioning of the cell – another crucial task in high-Na+ environments. This chapter primarily summarises the cation transport systems of these selected fungi, and it also describes other membrane transporters that might be involved in their mechanisms of halotolerance.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alleva K, Chara O, Amodeo G (2012) Aquaporins: another piece in the osmotic puzzle. FEBS Lett 586(19):2991–2999. doi:10.1016/j.febslet.2012.06.013
Ambesi A, Miranda M, Petrov VV, Slayman CW (2000) Biogenesis and function of the yeast plasma-membrane H+-ATPase. J Exp Biol 203(1):155–160
Andrews JH, Spear RN, Nordheim EV (2002) Population biology of Aureobasidium pullulans on apple leaf surfaces. Can J Microbiol 48(6):500–513
Arino J, Ramos J, Sychrova H (2010) Alkali metal cation transport and homeostasis in yeasts. Microbiol Mol Biol Rev 74(1):95–120. doi:10.1128/MMBR.00042-09
Banuelos MA, Sychrova H, Bleykasten-Grosshans C, Souciet JL, Potier S (1998) The Nha1 antiporter of Saccharomyces cerevisiae mediates sodium and potassium efflux. Microbiology 144:2749–2758
Benito B, Garciadeblas B, Rodriguez-Navarro A (2002) Potassium- or sodium-efflux ATPase, a key enzyme in the evolution of fungi. Microbiology 148:933–941
Benito B, Garciadeblas B, Schreier P, Rodriguez-Navarro A (2004) Novel P-type ATPases mediate high-affinity potassium or sodium uptake in fungi. Eukaryot Cell 3(2):359–368. doi:10.1128/Ec.3.2.359-368.2004
Benito B, Garciadeblas B, Fraile-Escanciano A, Rodriguez-Navarro A (2011) Potassium and sodium uptake systems in fungi. The transporter diversity of Magnaporthe oryzae. Fungal Genet Biol 48(8):812–822. doi:10.1016/j.fgb.2011.03.002
Borgnia MJ, Agre P (2001) Reconstitution and functional comparison of purified GlpF and AqpZ, the glycerol and water channels from Escherichia coli. Proc Natl Acad Sci U S A 98(5):2888–2893. doi:10.1073/pnas.051628098
Borgnia M, Nielsen S, Engel A, Agre P (1999) Cellular and molecular biology of the aquaporin water channels. Annu Rev Biochem 68:425–458. doi:10.1146/annurev.biochem.68.1.425
Cagnac O, Leterrier M, Yeager M, Blumwald E (2007) Identification and characterization of Vnx1p, a novel type of vacuolar monovalent Cation/H+ antiporter of Saccharomyces cerevisiae. J Biol Chem 282(33):24284–24293. doi:10.1074/jbc.M703116200
Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Schulte U, Kothe GO, Jedd G, Mewes W, Staben C, Marcotte E, Greenberg D, Roy A, Foley K, Naylor J, Stange-Thomann N, Barrett R, Gnerre S, Kamal M, Kamvysselis M, Mauceli E, Bielke C, Rudd S, Frishman D, Krystofova S, Rasmussen C, Metzenberg RL, Perkins DD, Kroken S, Cogoni C, Macino G, Catcheside D, Li W, Pratt RJ, Osmani SA, DeSouza CP, Glass L, Orbach MJ, Berglund JA, Voelker R, Yarden O, Plamann M, Seiler S, Dunlap J, Radford A, Aramayo R, Natvig DO, Alex LA, Mannhaupt G, Ebbole DJ, Freitag M, Paulsen I, Sachs MS, Lander ES, Nusbaum C, Birren B (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422(6934):859–868
Garciadeblas B, Rubio F, Quintero FJ, Banuelos MA, Haro R, Rodriguez-Navarro A (1993) Differential expression of two genes encoding isoforms of the ATPase involved in sodium efflux in Saccharomyces cerevisiae. Mol Gen Genet 236(2–3):363–368
Gorjan A, Plemenitas A (2006) Identification and characterization of ENA ATPases HwENA1 and HwENA2 from the halophilic black yeast Hortaea werneckii. FEMS Microbiol Lett 265(1):41–50. doi:10.1111/j.1574-6968.2006.00473.x
Gostinčar C, Grube M, de Hoog S, Zalar P, Gunde-Cimerman N (2010) Extremotolerance in fungi: evolution on the edge. FEMS Microbiol Ecol 71(1):2–11. doi:10.1111/j.1574-6941.2009.00794.x
Gostinčar C, Lenassi M, Gunde-Cimerman N, Plemenitas A (2011) Fungal adaptation to extremely high salt concentrations. Adv Appl Microbiol 77:71–96. doi:10.1016/B978-0-12-387044-5.00003-0
Gostinčar C, Ohm RA, Kogej T, Sonjak S, Turk M, Zajc J, Zalar P, Grube M, Sun H, Han J, Sharma A, Chiniquy J, Ngan CY, Lipzen A, Barry K, Grigoriev IV, Gunde-Cimerman N (2014) Genome sequencing of four Aureobasidium pullulans varieties: biotechnological potential, stress tolerance, and description of new species. BMC Genomics 15:549. doi:10.1186/1471-2164-15-549
Graham LA, Powell B, Stevens TH (2000) Composition and assembly of the yeast vacuolar H(+)-ATPase complex. J Exp Biol 203(Pt 1):61–70
Grube M, Schmid F, Berg G (2011) Black fungi and associated bacterial communities in the phyllosphere of grapevine. Fungal Biol 115(10):978–986. doi:10.1016/j.funbio.2011.04.004
Gunde-Cimerman N, Zalar P, de Hoog S, Plemenitas A (2000) Hypersaline waters in salterns – natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32(3):235–240
Gunde-Cimerman N, Zalar P, Petrovič U, Turk M, Kogej T, De Hoog GS, Plemenitaš A (2004) Fungi in the salterns. In: Ventosa A (ed) Halophilic microorganisms. Springer, Berlin, pp 103–111
Gunde-Cimerman N, Ramos J, Plemenitaš A (2009) Halotolerant and halophilic fungi. Mycol Res 113(Pt 11):1231–1241. doi:10.1016/j.mycres.2009.09.002
Haro R, Garciadeblas B, Rodriguez-Navarro A (1991) A novel P-type ATPase from yeast involved in sodium-transport. FEBS Lett 291(2):189–191. doi:10.1016/0014-5793(91)81280-L
Hohmann S, Bill RM, Kayingo G, Prior BA (2000) Microbial MIP channels. Trends Microbiol 8(1):33–38. doi:10.1016/S0966-842x(99)01645-5
Kane PM, Yamashiro CT, Wolczyk DF, Neff N, Goebl M, Stevens TH (1990) Protein splicing converts the yeast Tfp1 gene-product to the 69-Kd subunit of the vacuolar H+-adenosine triphosphatase. Science 250(4981):651–657. doi:10.1126/science.2146742
Ketchum KA, Joiner WJ, Sellers AJ, Kaczmarek LK, Goldstein SA (1995) A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem. Nature 376(6542):690–695. doi:10.1038/376690a0
Kinclova O, Poitier S, Sychrova H (2001) The Zygosaccharomyces rouxii strain CBS732 contains only one copy of the HOG1 and the SOD2 genes. J Biotechnol 88(2):151–158
Kinclova-Zimmermannova O, Gaskova D, Sychrova H (2006) The Na+, K+/H+ -antiporter Nha1 influences the plasma membrane potential of Saccharomyces crevisiae. FEMS Yeast Res 6(5):792–800. doi:10.1111/j.1567-1364.2006.00062.x
Ko CH, Gaber RF (1991) Trk1 and Trk2 encode structurally related K+ transporters in Saccharomyces cerevisiae. Mol Cell Biol 11(8):4266–4273
Kogej T, Ramos J, Plemenitas A, Gunde-Cimerman N (2005) The halophilic fungus Hortaea werneckii and the halotolerant fungus Aureobasidium pullulans maintain low intracellular cation concentrations in hypersaline environments. Appl Environ Microbiol 71(11):6600–6605. doi:10.1128/aem.71.11.6600-6605.2005
Kralj Kunčič M, Kogej T, Drobne D, Gunde-Cimerman N (2010) Morphological response of the halophilic fungal genus Wallemia to high salinity. Appl Environ Microbiol 76(1):329–337. doi:10.1128/AEM.02318-09
Kuhlbrandt W (2004) Biology, structure and mechanism of P-type ATPases. Nat Rev Mol Cell Biol 5(4):282–295. doi:10.1038/nrm1354
Leandro MJ, Fonseca C, Goncalves P (2009) Hexose and pentose transport in ascomycetous yeasts: an overview. FEMS Yeast Res 9(4):511–525. doi:10.1111/j.1567-1364.2009.00509.x
Lenassi M, Gostinčar C, Jackman S, Turk M, Sadowski I, Nislow C, Jones S, Birol I, Cimerman NG, Plemenitas A (2013) Whole genome duplication and enrichment of metal cation transporters revealed by de novo genome sequencing of extremely halotolerant black yeast Hortaea werneckii. PLoS ONE 8(8):e71328. doi:10.1371/journal.pone.0071328
Marchi V, Sorin A, Wei Y, Rao R (1999) Induction of vacuolar Ca2+-ATPase and H+/Ca2+ exchange activity in yeast mutants lacking Pmr1, the Golgi Ca2+-ATPase. FEBS Lett 454(3):181–186
Maresova L, Sychrova H (2005) Physiological characterization of Saccharomyces cerevisiae kha1 deletion mutants. Mol Microbiol 55(2):588–600. doi:10.1111/j.1365-2958.2004.04410.x
Mendoza I, Rubio F, Rodrigueznavarro A, Pardo JM (1994) The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae. J Biol Chem 269(12):8792–8796
Nass R, Rao R (1999) The yeast endosomal Na+/H+ exchanger, Nhx1, confers osmotolerance following acute hypertonic shock. Microbiology 145:3221–3228
Nowikovsky K, Froschauer EM, Zsurka G, Samaj J, Reipert S, Kolisek M, Wiesenberger G, Schweyen RJ (2004) The LETM1/YOL027 gene family encodes a factor of the mitochondrial K+ homeostasis with a potential role in the Wolf-Hirschhorn syndrome. J Biol Chem 279(29):30307–30315. doi:10.1074/jbc.M403607200
Olstorpe M, Axelsson L, Schnurer J, Passoth V (2010) Effect of starter culture inoculation on feed hygiene and microbial population development in fermented pig feed composed of a cereal grain mix with wet wheat distillers’ grain. J Appl Microbiol 108(1):129–138. doi:10.1111/j.1365-2672.2009.04399.x
Padamsee M, Kumar TK, Riley R, Binder M, Boyd A, Calvo AM, Furukawa K, Hesse C, Hohmann S, James TY, LaButti K, Lapidus A, Lindquist E, Lucas S, Miller K, Shantappa S, Grigoriev IV, Hibbett DS, McLaughlin DJ, Spatafora JW, Aime MC (2012) The genome of the xerotolerant mold Wallemia sebi reveals adaptations to osmotic stress and suggests cryptic sexual reproduction. Fungal Genet Biol 49(3):217–226. doi:10.1016/j.fgb.2012.01.007
Palmgren MG, Axelsen KB (1998) Evolution of P-type ATPases. Biochim Biophys Acta 1365(1–2):37–45
Plemenitas A, Lenassi M, Konte T, Kejzar A, Zajc J, Gostinčar C, Gunde-Cimerman N (2014) Adaptation to high salt concentrations in halotolerant/halophilic fungi: a molecular perspective. Front Microbiol 5:199. doi:10.3389/fmicb.2014.00199
Prior C, Potier S, Souciet JL, Sychrova H (1996) Characterization of the NHA1 gene encoding a Na+/H+-antiporter of the yeast Saccharomyces cerevisiae. FEBS Lett 387(1):89–93. doi:10.1016/0014-5793(96)00470-X
Ramos J, Arino J, Sychrova H (2011) Alkali-metal-cation influx and efflux systems in nonconventional yeast species. FEMS Microbiol Lett 317(1):1–8. doi:10.1111/j.1574-6968.2011.02214.x
Rodriguez-Navarro A (2000) Potassium transport in fungi and plants. Biochim Biophys Acta Rev Biomembr 1469(1):1–30. doi:10.1016/S0304-4157(99)00013-1
Schlesser A, Ulaszewski S, Ghislain M, Goffeau A (1988) A second transport ATPase gene in Saccharomyces cerevisiae. J Biol Chem 263(36):19480–19487
Serrano R, Kiellandbrandt MC, Fink GR (1986) Yeast plasma-membrane ATPase is essential for growth and has homology with (Na++K+), K+- and Ca2+-ATPases. Nature 319(6055):689–693. doi:10.1038/319689a0
Serrano R, Ruiz A, Bernal D, Chambers JR, Arino J (2002) The transcriptional response to alkaline pH in Saccharomyces cerevisiae: evidence for calcium-mediated signalling. Mol Microbiol 46(5):1319–1333. doi:10.1046/j.1365-2958.2002.03246.x
Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133(4):651–669. doi:10.1111/j.1399-3054.2007.01008.x
Simon E, Clotet J, Calero F, Ramos J, Arino J (2001) A screening for high copy suppressors of the sit4 hal3 synthetically lethal phenotype reveals a role for the yeast Nha1 antiporter in cell cycle regulation. J Biol Chem 276(32):29740–29747. doi:10.1074/jbc.M101992200
Vashist S, Frank CG, Jakob CA, Ng DT (2002) Two distinctly localized p-type ATPases collaborate to maintain organelle homeostasis required for glycoprotein processing and quality control. Mol Biol Cell 13(11):3955–3966. doi:10.1091/mbc.02-06-0090
Vaupotic T, Plemenitas A (2007) Differential gene expression and Hog1 interaction with osmoresponsive genes in the extremely halotolerant black yeast Hortaea werneckii. BMC Genomics 8:280. doi:10.1186/1471-2164-8-280
Waschuk SA, Bezerra AG Jr, Shi L, Brown LS (2005) Leptosphaeria rhodopsin: bacteriorhodopsin-like proton pump from a eukaryote. Proc Natl Acad Sci U S A 102(19):6879–6883. doi:10.1073/pnas.0409659102
Wieland J, Nitsche AM, Strayle J, Steiner H, Rudolph HK (1995) The Pmr2 gene-cluster encodes functionally distinct isoforms of a putative Na+ pump in the yeast plasma-membrane. EMBO J 14(16):3870–3882
Xu H, Cooke JEK, Zwiazek JJ (2013) Phylogenetic analysis of fungal aquaporins provides insight into their possible role in water transport of mycorrhizal associations. Botany-Botanique 91(8):495–504. doi:10.1139/cjb-2013-0041
Yale J, Bohnert HJ (2001) Transcript expression in Saccharomyces cerevisiae at high salinity. J Biol Chem 276(19):15996–16007. doi:10.1074/jbc.M008209200
Yan A, Hu X, Wang K, Sun J (2013) Discriminating of ATP competitive Src kinase inhibitors and decoys using self-organizing map and support vector machine. Mol Divers 17(1):75–83. doi:10.1007/s11030-012-9411-0
Zajc J, Liu Y, Dai W, Yang Z, Hu J, Gostinčar C, Gunde-Cimerman N (2013) Genome and transcriptome sequencing of the halophilic fungus Wallemia ichthyophaga: haloadaptations present and absent. BMC Genomics 14(1):617. doi:10.1186/1471-2164-14-617
Zajc J, Kogej T, Galinski EA, Ramos J, Gunde-Cimerman N (2014) Osmoadaptation strategy of the most halophilic fungus, Wallemia ichthyophaga, growing optimally at salinities above 15% NaCl. Appl Environ Microbiol 80(1):247–256. doi:10.1128/AEM.02702-13
Zalar P, Gostinčar C, de Hoog GS, Ursic V, Sudhadham M, Gunde-Cimerman N (2008) Redefinition of Aureobasidium pullulans and its varieties. Stud Mycol 61:21–38. doi:10.3114/sim.2008.61.02
Zotova L, Aleschko M, Sponder G, Baumgartner R, Reipert S, Prinz M, Schweyen RJ, Nowikovsky K (2010) Novel components of an active mitochondrial K+/H+ exchange. J Biol Chem 285(19):14399–14414. doi:10.1074/jbc.M109.059956
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Plemenitaš, A., Konte, T., Gostinčar, C., Cimerman, N.G. (2016). Transport Systems in Halophilic Fungi. In: Ramos, J., Sychrová, H., Kschischo, M. (eds) Yeast Membrane Transport. Advances in Experimental Medicine and Biology, vol 892. Springer, Cham. https://doi.org/10.1007/978-3-319-25304-6_13
Download citation
DOI: https://doi.org/10.1007/978-3-319-25304-6_13
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-25302-2
Online ISBN: 978-3-319-25304-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)