Abstract
Natural hypersaline environments are inhabited by an abundance of prokaryotic and eukaryotic microorganisms capable of thriving under extreme saline conditions. Yeasts represent a substantial fraction of halotolerant eukaryotic microbiomes and are frequently isolated as food contaminants and from solar salterns. During the last years, a handful of new species has been discovered in moderate saline environments, including estuarine and deep-sea waters. Although Saccharomyces cerevisiae is considered the primary osmoadaptation model system for studies of hyperosmotic stress conditions, our increasing understanding of the physiology and molecular biology of halotolerant yeasts provides new insights into their distinct metabolic traits and provides novel and innovative opportunities for genome mining of biotechnologically relevant genes. Yeast species such as Debaryomyces hansenii, Zygosaccharomyces rouxii, Hortaea werneckii and Wallemia ichthyophaga show unique properties, which make them attractive for biotechnological applications. Select halotolerant yeasts are used in food processing and contribute to aromas and taste, while certain gene clusters are used in second generation biofuel production. Finally, both pharmaceutical and chemical industries benefit from applications of halotolerant yeasts as biocatalysts. This comprehensive review summarizes the most recent findings related to the biology of industrially-important halotolerant yeasts and provides a detailed and up-to-date description of modern halotolerant yeast-based biotechnological applications.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ali SS, Al-Tohamy R, Xie R, El-Sheekh MM, Sun J (2020) Construction of a new lipase- and xylanase-producing oleaginous yeast consortium capable of reactive azo dye degradation and detoxification. Bioresour Technol 313:123631. https://doi.org/10.1016/j.biortech.2020.123631
Almagro A, Prista C, Castro S, Quintas C, Madeira-Lopes A, Ramos J, Loureiro-Dias MC (2000) Effects of salts on Debaryomyces hansenii and Saccharomyces cerevisiae under stress conditions. Int J Food Microbiol 56:191–197. https://doi.org/10.1016/s0168-1605(00)00220-8
Al-Tohamy R, Sun J, Fareed MF, Kenawy ER, Ali SS (2020) Ecofriendly biodegradation of Reactive Black 5 by newly isolated Sterigmatomyces halophilus SSA1575, valued for textile azo dye wastewater processing and detoxification. Sci Rep 10:12370. https://doi.org/10.1038/s41598-020-69304-4
Anastas P, Eghbali N (2010) Green chemistry: principles and practice. Chem Soc Rev 39:301–312. https://doi.org/10.1039/b918763b
Anderson NG (2012) Solvent selection. In: Anderson NG (ed) Practical processes & development—a guide for organic chemists, 2nd edn. Academic Press, Oxford, pp 121–168
Andreu C, Del Olmo M (2018) Biotransformation using halotolerant yeast in seawater: a sustainable strategy to produce R-(-)-phenylacetylcarbinol. Appl Microbiol Biotechnol 102:4717–4727. https://doi.org/10.1007/s00253-018-8945-1
Andreu C, del Olmo M (2019) Improved biocatalytic activity of the Debaryomyces species in seawater. ChemCatChem 11:3085. https://doi.org/10.1002/cctc.201900558
Andreu C, Del Olmo M (2020) Whole-cell biocatalysis in seawater: new halotolerant yeast strains for the regio- and stereoselectivity reduction of 1-phenylpropane-1,2-dione in saline-rich media. ChemBioChem 21:1621–1628. https://doi.org/10.1002/cbic.202000023
Bansal PK, Mondal AK (2000) Isolation and sequence of the HOG1 homologue from Debaryomyces hansenii by complementation of the hog1Delta strain of Saccharomyces cerevisiae. Yeast 16(1):81–88. https://doi.org/10.1002/(SICI)1097-0061(20000115)16:1%3c81::AID-YEA510%3e3.0.CO;2-I
Bizzarri M, Cassanelli S, Pryszcz LP, Gawor J, Gromadka R, Solieri L (2018) Draft genome sequences of the highly halotolerant strain Zygosaccharomyces rouxii ATCC 42981 and the novel allodiploid strain Zygosaccharomyces sapae ATB301T obtained using the MinION platform. Microbiol Resour Announc 7:e00874-e918. https://doi.org/10.1128/MRA.00874-18
Bizzarri M, Cassanelli S, Dušková M, Sychrová H, Solieri L (2019) A set of plasmids carrying antibiotic resistance markers and Cre recombinase for genetic engineering of nonconventional yeast Zygosaccharomyces rouxii. Yeast 36:711–722. https://doi.org/10.1002/yea.3438
Breuer U, Harms H (2006) Debaryomyces hansenii—an extremophilic yeast with biotechnological potential. Yeast 23:415–437. https://doi.org/10.1002/yea.1374
Butinar L, Santos S, Spencer-Martins I, Oren A, Gunde-Cimerman N (2005) Yeast diversity in hypersaline habitats. FEMS Microbiol Lett 244:229–234. https://doi.org/10.1016/j.femsle.2005.01.043
Capusoni C, Arioli S, Donzella S, Guidi B, Serra I, Compagno C (2019) Hyper-osmotic stress elicits membrane depolarization and decreased permeability in halotolerant marine Debaryomyces hansenii strains and in Saccharomyces cerevisiae. Front Microbiol 10:64. https://doi.org/10.3389/fmicb.2019.00064
Chung D, Kim H, Choi HS (2019) Fungi in salterns. J Microbiol 57:717–724. https://doi.org/10.1007/s12275-019-9195-3
da Silva S, Calado S, Lucas C, Aguiar C (2008) Unusual properties of the halotolerant yeast Candida nodaensis Killer toxin, CnKT. Microbiol Res 163:243–251. https://doi.org/10.1016/j.micres.2007.04.002
Dakal TC, Solieri L, Giudici P (2014) Adaptive response and tolerance to sugar and salt stress in the food yeast Zygosaccharomyces rouxii. Int J Food Microbiol 185:140–157. https://doi.org/10.1016/j.ijfoodmicro.2014.05.015
Demirci H, Kurt-Gur G, Ordu E (2021) Microbiota profiling and screening of the lipase active halotolerant yeasts of the olive brine. World J Microbiol Biotechnol 37:23. https://doi.org/10.1007/s11274-020-02976-2
Domínguez de María P (2013) On the use of seawater as reaction media for large-scale applications in biorefineries. ChemCatChem 5:1643–1648. https://doi.org/10.1002/cctc.201200877
Dujon B, Sherman D, Fischer G et al (2004) Genome evolution in yeasts. Nature 430:35–44. https://doi.org/10.1038/nature02579
Génolevures Consortium, Souciet JL, Dujon B, Gaillardin C et al (2009) Comparative genomics of protoploid Saccharomycetaceae. Genome Res 19:1696–1709. https://doi.org/10.1101/gr.091546.109
Gong Y, Ding P, Xu MJ, Zhang CM, Xing K, Qin S (2021) Biodegradation of phenol by a halotolerant versatile yeast Candida tropicalis SDP-1 in wastewater and soil under high salinity conditions. J Environ Manag 289:112525. https://doi.org/10.1016/j.jenvman.2021.112525
Gordon JL, Wolfe KH (2008) Recent allopolyploid origin of Zygosaccharomyces rouxii strain ATCC 42981. Yeast 25:449–456. https://doi.org/10.1002/yea.1598
Gori K, Mortensen HD, Arneborg N, Jespersen L (2005) Expression of the GPD1 and GPP2 orthologues and glycerol retention during growth of Debaryomyces hansenii at high NaCl concentrations. Yeast 22:1213–1222. https://doi.org/10.1002/yea.1306
Gori K, Hébraud M, Chambon C, Mortensen HD, Arneborg N, Jespersen L (2007) Proteomic changes in Debaryomyces hansenii upon exposure to NaCl stress. FEMS Yeast Res 7:293–303. https://doi.org/10.1111/j.1567-1364.2006.00155.x
Gostinčar C, Lenassi M, Gunde-Cimerman N, Plemenitaš A (2011) Fungal adaptation to extremely high salt concentrations. In: Laskin AI, Sariaslani S, Gadd GM (eds) Advances in applied microbiology, vol 77. Elsevier, Amsterdam, pp 71–96
Gostinčar C, Sun X, Zajc J, Fang C, Hou Y, Luo Y, Gunde-Cimerman N, Song Z (2019) Population genomics of an obligately halophilic Basidiomycete Wallemia ichthyophaga. Front Microbiol 10:2019. https://doi.org/10.3389/fmicb.2019.02019
Gostinčar C, Stajich JE, Kejžar A, Sinha S, Nislow C, Lenassi M, Gunde-Cimerman N (2021) Seven years at high salinity—experimental evolution of the extremely halotolerant black yeast Hortaea werneckii. J Fungi 7:723. https://doi.org/10.3390/jof7090723
Grande PM, Bergs C, Domínguez de María P (2012) Chemo-enzymatic conversion of glucose into 5-hydroxymethylfurfural in seawater. Chemsuschem 5:1203–1206. https://doi.org/10.1002/cssc.201200065
Gunde-Cimerman N, Ramos J, Plemenitas A (2009) Halotolerant and halophilic fungi. Mycol Res 113:1231–1241. https://doi.org/10.1016/j.mycres.2009.09.002
Hadibarata T, Khudhair AB, Kristanti RA, Kamyab H (2017) Biodegradation of pyrene by Candida sp. S1 under high salinity conditions. Bioprocess Biosyst Eng 40:1411–1418. https://doi.org/10.1007/s00449-017-1798-7
Hernáiz MJ, Alcántara AR, García JI, Sinisterra JV (2010) Applied biotransformations in green solvents. Chem Eur J 16:9422–9437. https://doi.org/10.1002/chem.201000798
Herrera R, Salazar A, Ramos-Moreno L, Ruiz-Roldan C, Ramos J (2017) Vacuolar control of subcellular cation distribution is a key parameter in the adaptation of Debaryomyces hansenii to high salt concentrations. Fungal Genet Biol 100:52–60. https://doi.org/10.1016/j.fgb.2017.02.002
Iwaki T, Tamai Y, Watanabe Y (1999) Two putative MAP kinase genes, ZrHOG1 and ZrHOG2, cloned from the salt-tolerant yeast Zygosaccharomyces rouxii are functionally homologous to the Saccharomyces cerevisiae HOG1 gene. Microbiology (Reading) 145:241–248. https://doi.org/10.1099/13500872-145-1-241
Iwaki T, Kurono S, Yokose Y, Kubota K, Tamai Y, Watanabe Y (2001) Cloning of glycerol-3-phosphate dehydrogenase genes (ZrGPD1 and ZrGPD2) and glycerol dehydrogenase genes (ZrGCY1 and ZrGCY2) from the salt-tolerant yeast Zygosaccharomyces rouxii. Yeast 18:737–744. https://doi.org/10.1002/yea.722
Jančič S, Frisvad JC, Kocev D, Gostinčar C, Džeroski S, Gunde-Cimerman N (2016) Production of secondary metabolites in extreme environments: food- and airborne Wallemia spp. produce toxic metabolites at hypersaline conditions. PLoS ONE 11:e0169116. https://doi.org/10.1371/journal.pone.0169116
Jiang Y, Yang K, Wang H, Shang Y, Yang X (2015) Characteristics of phenol degradation in saline conditions of a halophilic strain JS3 isolated from industrial activated sludge. Mar Pollut Bull 99:230–234. https://doi.org/10.1016/j.marpolbul.2015.07.021
Jiang Y, Shang Y, Yang K, Wang H (2016) Phenol degradation by halophilic fungal isolate JS4 and evaluation of its tolerance of heavy metals. Appl Microbiol Biotechnol 100:1883–1890. https://doi.org/10.1007/s00253-015-7180-2
Jiang Y, Yang K, Deng T, Ji B, Shang Y, Wang H (2018) Immobilization of halophilic yeast for effective removal of phenol in hypersaline conditions. Water Sci Technol 77:706–713. https://doi.org/10.2166/wst.2017.576
Jones EBG, Suetrong S, Sakayaroj J et al (2015) Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Divers 73:1–72. https://doi.org/10.1007/s13225-015-0339-4
Kamyabi A, Nouri H, Moghimi H (2018) Characterization of pyrene degradation and metabolite identification by Basidioascus persicus and mineralization enhancement with bacterial-yeast co-culture. Ecotoxicol Environ Saf 15:471–477. https://doi.org/10.1016/j.ecoenv.2018.07.098
Karatay SE, Demiray E, Dönmez G (2019) Bioethanol production by newly isolated halotolerant Kluyveromyces marxianus strains. Environ Prog Sustain Energy 38:542–547. https://doi.org/10.1002/ep.12935
Kejžar A, Grötli M, Tamás MJ, Plemenitaš A, Lenassi M (2015a) HwHog1 kinase activity is crucial for survival of Hortaea werneckii in extremely hyperosmolar environments. Fungal Genet Biol 74:45–58. https://doi.org/10.1016/j.fgb.2014.11.004
Kejžar A, Cibic M, Grøtli M, Plemenitaš A, Lenassi M (2015b) The unique characteristics of HOG pathway MAPKs in the extremely halotolerant Hortaea werneckii. FEMS Microbiol Lett 362:fnv046. https://doi.org/10.1093/femsle/fnv046
Kinclová O, Potier S, Sychrová H (2001) The Zygosaccharomyces rouxii strain CBS732 contains only one copy of the HOG1 and the SOD2 genes. J Biotechnol 88:151–158. https://doi.org/10.1016/s0168-1656(01)00274-7
Kogej T, Stein M, Volkmann M, Gorbushina AA, Galinski EA, Gunde-Cimerman N (2007) Osmotic adaptation of the halophilic fungus Hortaea werneckii: role of osmolytes and melanization. Microbiology (Reading) 153:4261–4273. https://doi.org/10.1099/mic.0.2007/010751-0
Konte T, Plemenitas A (2013) The HOG signal transduction pathway in the halophilic fungus Wallemia ichthyophaga: identification and characterisation of MAP kinases WiHog1A and WiHog1B. Extremophiles 17:623–636. https://doi.org/10.1007/s00792-013-0546-4
Konte T, Terpitz U, Plemenitaš A (2016) Reconstruction of the high-osmolarity glycerol (HOG) signaling pathway from the halophilic fungus Wallemia ichthyophaga in Saccharomyces cerevisiae. Front Microbio 7:901. https://doi.org/10.3389/fmicb.2016.00901
Kralj Kuncic M, Kogej T, Drobne D, Gunde-Cimerman N (2010) Morphological response of the halophilic fungal genus Wallemia to high salinity. Appl Environ Microbiol 76:329–337. https://doi.org/10.1128/AEM.02318-09
Lenassi M, Plemenitas A (2007) Novel group VII histidine kinase HwHhk7B from the halophilic fungi Hortaea werneckii has a putative role in osmosensing. Curr Genet 51:393–405. https://doi.org/10.1007/s00294-007-0131-4
Lenassi M, Zajc J, Gostinčar C, Gorjan A, Gunde-Cimerman N, Plemenitaš A (2011) Adaptation of the glycerol-3-phosphate dehydrogenase Gpd1 to high salinities in the extremely halotolerant Hortaea werneckii and halophilic Wallemia ichthyophaga. Fungal Biol 115:959–970. https://doi.org/10.1016/j.funbio.2011.04.001
Lenassi M, Gostinčar C, Jackman S, Turk M, Sadowski I, Nislow C, Jones S, Birol I, Cimerman NG, Plemenitaš 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:e71328. https://doi.org/10.1371/journal.pone.0071328
Martínez-Ávila L, Peidro-Guzmán H, Pérez-Llano Y et al (2021) Tracking gene expression, metabolic profiles, and biochemical analysis in the halotolerant basidiomycetous yeast Rhodotorula mucilaginosa EXF-1630 during benzo[a]pyrene and phenanthrene biodegradation under hypersaline conditions. Environ Pollut 271:116358. https://doi.org/10.1016/j.envpol.2020.116358
Masuda K, Guo X-F, Uryu N, Hagiwara T, Watabe S (2008) Isolation of marine yeasts collected from the Pacific Ocean showing a high production of γ-aminobutyric acid. Biosci Biotechnol Biochem 72:3265–3272. https://doi.org/10.1271/bbb.80544
Minhas AP, Biswas D (2019) Development of an efficient transformation system for halotolerant yeast Debaryomyces hansenii CBS767. Bio Protoc 9:e3352. https://doi.org/10.21769/BioProtoc.3352
Minhas A, Biswas D, Mondal AK (2009) Development of host and vector for high-efficiency transformation and gene disruption in Debaryomyces hansenii. FEMS Yeast Res 9:95–102. https://doi.org/10.1111/j.1567-1364.2008.00457.x
Mitchison-Field LMY, Vargas-Muñiz JM, Stormo BM, Vogt EJD, Van Dierdonck S, Pelletier JF, Ehrlich C, Lew DJ, Field CM, Gladfelter AS (2019) Unconventional cell division cycles from marine-derived yeasts. Curr Biol 29:3439-3456.e5. https://doi.org/10.1016/j.cub.2019.08.050
Mogi R, Watanabe J (2020) Identification of SFL1 as a positive regulator for flor formation in Zygosaccharomyces rouxii. Biosci Biotechnol Biochem 84:1291–1298. https://doi.org/10.1080/09168451.2020.1732187
Mohite P, Kumar AR, Zinjarde S (2017) Relationship between salt tolerance and nanoparticle synthesis by Williopsis saturnus NCIM 3298. World J Microbiol Biotechnol 33:163. https://doi.org/10.1007/s11274-017-2329-z
Ni Y, Holtmann D, Hollmann F (2014) How green is biocatalysis? To calculate is to know. ChemCatChem 6:930–943. https://doi.org/10.1002/cctc.201300976
Nikolaivits E, Agrafiotis A, Baira E, Le Goff G, Tsafantakis N, Chavanich SA, Benayahu Y, Ouazzani J, Fokialakis N, Topakas E (2020) Degradation mechanism of 2,4-dichlorophenol by fungi isolated from marine invertebrates. Int J Mol Sci 21:3317. https://doi.org/10.3390/ijms21093317
Okai M, Betsuno A, Shirao A, Obara N, Suzuki K, Takei T, Takashio M, Ishida UN (2016) Citeromyces matritensis M37 is a salt-tolerant yeast that produces ethanol from salted algae. Can J Microbiol 63:20–26. https://doi.org/10.1139/cjm-2016-0259
Perea-Sanz L, Peris D, Belloch C, Flores D (2019) Debaryomyces hansenii metabolism of sulfur amino acids as precursors of volatile sulfur compounds of interest in meat products. Agric Food Chem 67(33):9335–9343. https://doi.org/10.1021/acs.jafc.9b03361
Petersen KM, Jespersen L (2004) Genetic diversity of the species Debaryomyces hansenii and the use of chromosome polymorphism for typing of strains isolated from surface-ripened cheeses. J Appl Microbiol 97:205–213. https://doi.org/10.1111/j.1365-2672.2004.02293.x
Pitt JI, Hocking AD (2009) Fungi and food spoilage, 3rd edn. Springer, Boston
Plemenitas A, Vaupotic T, Lenassi M, Kogej T, Gunde-Cimerman N (2008) Adaptation of extremely halotolerant black yeast Hortaea werneckii to increased osmolarity: a molecular perspective at a glance. Stud Mycol 61:67–75. https://doi.org/10.3114/sim.2008.61.06
Plemenitaš A, Lenassi M, Konte T, Kejžar 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. https://doi.org/10.3389/fmicb.2014.00199
Posas F, Chambers JR, Heyman JA, Hoeffler JP, de Nadal E, Ariño J (2000) The transcriptional response of yeast to saline stress. J Biol Chem 275:17249–17255. https://doi.org/10.1074/jbc.M910016199
Prista C, Michán C, Miranda IM, Ramos J (2016) The halotolerant Debaryomyces hansenii, the Cinderella of non-conventional yeasts. Yeast 33:523–533. https://doi.org/10.1002/yea.3177
Qi W, Fan ZC, Wang CL, Hou LH, Liu JF, Cao XH (2014a) Non-targeted metabolomic reveals the effect of salt stress on global metabolite of halotolerant yeast Candida versatilis and principal component analysis. J Ind Microbiol Biotechnol 41:1553–1562. https://doi.org/10.1007/s10295-014-1475-7
Qi W, Hou LH, Guo HL, Wang CL, Fan ZC, Liu JF, Cao XH (2014b) Effect of salt-tolerant yeast of Candida versatilis and Zygosaccharomyces rouxii on the production of biogenic amines during soy sauce fermentation. J Sci Food Agric 94:1537–1542. https://doi.org/10.1002/jsfa.6454
Ramos-Moreno L, Ramos J, Michán C (2019) Overlapping responses between salt and oxidative stress in Debaryomyces hansenii. World J Microbiol Biotechnol 35:170. https://doi.org/10.1007/s11274-019-2753-3
Ricaurte ML, Govind NS (1999) Construction of plasmid vectors and transformation of the marine yeast Debaryomyces hansenii. Mar Biotechnol (NY) 1:15–19. https://doi.org/10.1007/pl00011745
Romeo O, Marchetta A, Giosa D, Giuffrè L, Urzì C, De Leo F (2020) Whole genome sequencing and comparative genome analysis of the halotolerant deep sea black yeast Hortaea werneckii. Life (Basel) 10:229. https://doi.org/10.3390/life10100229
Ruginescu R, Gomoiu I, Popescu O, Cojoc R, Neagu S, Lucaci I, Batrinescu-Moteau C, Enache M (2020) Bioprospecting for novel halophilic and halotolerant sources of hydrolytic enzymes in brackish, saline and hypersaline lakes of Romania. Microorganisms 8:1903. https://doi.org/10.3390/microorganisms8121903
Sánchez NS, Calahorra M, González J, Defosse T, Papon N, Peña A, Coria R (2020) Contribution of the mitogen-activated protein kinase Hog1 to the halotolerance of the marine yeast Debaryomyces hansenii. Curr Genet 66:1135–1153. https://doi.org/10.1007/s00294-020-01099-3
Sato A, Matsushima K, Oshima K, Hattori M, Koyama Y (2017) Draft genome sequencing of the highly halotolerant and allopolyploid yeast Zygosaccharomyces rouxii NBRC 1876. Genome Announc 5:e01610-e1616. https://doi.org/10.1128/genomeA.01610-16
Scapini T, Dalastra C, Camargo AF, Kubeneck S, Modkovski TA, Júnior SLA, Treichel H (2021) Seawater-based biorefineries: a strategy to reduce the water footprint in the conversion of lignocellulosic biomass. Bioresour Technol 14:126325. https://doi.org/10.1016/j.biortech.2021.126325
Serra I, Guidi B, Burgaud G, Contente ML, Ferraboschi P, Pinto A, Compagno C, Molinari F, Romano D (2016) Seawater-based biocatalytic strategy: stereoselective reductions of ketones with marine yeasts. ChemCatChem 8:3254. https://doi.org/10.1002/cctc.201600947
Serra I, Capusoni C, Molinari F, Musso L, Pellegrino L, Compagno C (2019) Marine microorganisms for biocatalysis: selective hydrolysis of nitriles with a salt-resistant strain of Meyerozyma guilliermondii. Mar Biotechnol (NY) 21:229–239. https://doi.org/10.1007/s10126-019-09875-0
Sharma P, Mondal AK (2005) Evidence that C-terminal non-kinase domain of Pbs2p has a role in high osmolarity-induced nuclear localization of Hog1p. Biochem Biophys Res Commun 328:906–913. https://doi.org/10.1016/j.bbrc.2005.01.039
Sinha S, Flibotte S, Neira M, Formby S, Plemenitaš A, Cimerman NG, Lenassi M, Gostinčar C, Stajich JE, Nislow C (2017) Insight into the recent genome duplication of the halophilic yeast Hortaea werneckii: combining an improved genome with gene expression and chromatin structure. G3 (Bethesda) 7:2015–2022. https://doi.org/10.1534/g3.117.040691
Solieri L (2021) The revenge of Zygosaccharomyces yeasts in food biotechnology and applied microbiology. World J Microbiol Biotechnol 37:96. https://doi.org/10.1007/s11274-021-03066-7
Solieri L, Cassanelli S, Croce MA, Giudici P (2008) Genome size and ploidy level: new insights for elucidating relationships in Zygosaccharomyces species. Fungal Genet Biol 45:1582–1590. https://doi.org/10.1016/j.fgb.2008.10.001
Stratford M, Steels H, Novodvorska M, Archer DB, Avery SV (2019) Extreme osmotolerance and halotolerance in food-relevant yeasts and the role of glycerol-dependent cell individuality. Front Microbiol 9:3238. https://doi.org/10.3389/fmicb.2018.03238
Strucko T, Andersen NL, Mahler MR, Martínez JL, Mortensen UH (2021) A CRISPR/Cas9 method facilitates efficient oligo-mediated gene editing in Debaryomyces hansenii. Synth Biol 6:ysab031. https://doi.org/10.1093/synbio/ysab031
Tang W, Zhou B, Xing K, Tan L (2020) Co-enhanced activated sludge system by static magnetic field and two halotolerant yeasts for azo dye treatment. Water Environ Res 92:2095–2104. https://doi.org/10.1002/wer.1375
Trincone A (2010) Potential biocatalysts originating from sea environments. J Mol Catal B 66:241–256. https://doi.org/10.1016/j.molcatb.2010.06.004
Turk M, Plemenitas A (2002) The HOG pathway in the halophilic black yeast Hortaea werneckii: isolation of the HOG1 homolog gene and activation of HwHog1p. FEMS Microbiol Lett 216:193–199. https://doi.org/10.1111/j.1574-6968.2002.tb11435.x
Wang D, Zhang M, Huang J, Zhou R, Jin Y, Wu C (2020a) Zygosaccharomyces rouxii combats salt stress by maintaining cell membrane structure and functionality. J Microbiol Biotechnol 30:62–70. https://doi.org/10.4014/jmb.1904.04006
Wang X, Wang Y, Ning S, Shi S, Tan L (2020b) Improving azo dye decolorization performance and halotolerance of Pichia occidentalis A2 by static magnetic field and possible mechanisms through comparative transcriptome analysis. Front Microbiol 11:712. https://doi.org/10.3389/fmicb.2020.00712
Watanabe J, Uehara K, Mogi Y, Suzuki K, Watanabe T, Yamazaki T (2010) Improved transformation of the halo-tolerant yeast Zygosaccharomyces rouxii by electroporation. Biosci Biotechnol Biochem 74:1092–1094. https://doi.org/10.1271/bbb.90865
Wells A, Meyer H-P (2014) Biocatalysis as a strategic green technology for the chemical industry. ChemCatChem 6:918–920. https://doi.org/10.1002/cctc.201402065
Xie D, Miller E, Sharpe P, Jackson E, Zhu Q (2017) Omega-3 production by fermentation of Yarrowia lipolytica: from fed-batch to continuous. Biotechnol Bioeng 114:798–812. https://doi.org/10.1002/bit.26216
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 14:617. https://doi.org/10.1186/1471-2164-14-617
Zajc J, Džeroski S, Kocev D, Oren A, Sonjak S, Tkavc R, Gunde-Cimerman N (2014a) Chaophilic or chaotolerant fungi: a new category of extremophiles? Front Microbiol 5:708. https://doi.org/10.3389/fmicb.2014.00708
Zajc J, Kogej T, Galinski EA, Ramos J, Gunde-Cimerman N (2014b) Osmoadaptation strategy of the most halophilic fungus, Wallemia ichthyophaga, growing optimally at salinities above 15% NaCl. Appl Environ Microbiol 80:247–256. https://doi.org/10.1128/AEM.02702-13
Zaky AS, Tucker GA, Daw ZY, Du C (2014) Marine yeast isolation and industrial application. FEMS Yeast Res 14:813–825. https://doi.org/10.1111/1567-1364.12158
Zaky AS, Greetham D, Tucker GA, Du C (2018) The establishment of a marine focused biorefinery for bioethanol production using seawater and a novel marine yeast strain. Sci Rep 8:12127. https://doi.org/10.1038/s41598-018-30660-x
Zaky AS, French CE, Tucker GA, Du C (2020) Improving the productivity of bioethanol production using marine yeast and seawater-based media. Biomass Bioenergy 139:105615. https://doi.org/10.1016/j.biombioe.2020.105615
Zalar P, Sybren de Hoog G, Schroers HJ, Frank JM, Gunde-Cimerman N (2005) Taxonomy and phylogeny of the xerophilic genus Wallemia (Wallemiomycetes and Wallemiales, cl. et ord. nov.). Antonie Van Leeuwenhoek 87:311–328. https://doi.org/10.1007/s10482-004-6783-x
Zalar P, Zupančič J, Gostinčar C, Zajc J, de Hoog GS, De Leo F, Azua-Bustos A, Gunde-Cimerman N (2019) The extremely halotolerant black yeast Hortaea werneckii—a model for intraspecific hybridization in clonal fungi. IMA Fungus 10:10. https://doi.org/10.1186/s43008-019-0007-5
Zambelli P, Serra I, Fernandez-Arrojo L, Plou FJ, Tamborini L, Conti P, Contente ML, Molinari F, Romano D (2015) Sweet-and-salty biocatalysis: fructooligosaccharides production using Cladosporium cladosporioides in seawater. Process Biochem 50:1086–1090. https://doi.org/10.1016/j.procbio.2015.04.006
Zarnowski R, Sanchez H, Andreu C, Andes D, Del Olmo ML (2021) Formation and characterization of biofilms formed by salt-tolerant yeast strains in seawater-based growth medium. Appl Microbiol Biotechnol 105:2411–2426. https://doi.org/10.1007/s00253-021-11132-1
Zheng C, Li Z, Yang H, Zhang T, Niu H, Liu D, Wang J, Ying H (2019) Computation-aided rational design of a halophilic choline kinase for cytidine diphosphate choline production in high-salt condition. J Biotechnol 290:59–66. https://doi.org/10.1016/j.jbiotec.2018.11.008
Acknowledgements
This work has been supported by Grants UV-INV-AE19-1199043 and UV-INV-AE-1560151 from the Universitat de València. We thank Ms. Hanna Anhalt for linguisitic comments on this manuscript.
Author information
Authors and Affiliations
Contributions
All the authors contributed to the writing, reviewing and editing of the paper.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest, financial or otherwise.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Andreu, C., Zarnowski, R. & del Olmo, M. Recent developments in the biology and biotechnological applications of halotolerant yeasts. World J Microbiol Biotechnol 38, 27 (2022). https://doi.org/10.1007/s11274-021-03213-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-021-03213-0