Abstract
Salterns are hypersaline extreme environments with unique physicochemical properties such as a salinity gradient. Although the investigation of microbiota in salterns has focused on archaea and bacteria, diverse fungi also thrive in the brine and soil of salterns. Fungi isolated from salterns are represented by black yeasts (Hortaea werneckii, Phaeotheca triangularis, Aureobasidium pullulans, and Trimmatostroma salinum), Cladosporium, Aspergillus, and Penicillium species. Most studies on saltern-derived fungi gave attention to black yeasts and their physiological characteristics, including growth under various culture conditions. Since then, biochemical and molecular tools have been employed to explore adaptation of these fungi to salt stress. Genome databases of several fungi in salterns are now publicly available and being used to elucidate salt tolerance mechanisms and discover the target genes for agricultural and industrial applications. Notably, the number of enzymes and novel metabolites known to be produced by diverse saltern-derived fungi has increased significantly. Therefore, fungi in salterns are not only interesting and important subjects to study fungal biodiversity and adaptive mechanisms in extreme environments, but also valuable bioresources with potential for biotechnological applications.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Alamillo, E., Reyes-Becerril, M., Cuesta, A., and Angulo, C. 2017. Marine yeast Yarrowia lipolytica improves the immune responses in Pacific red snapper (Lutjanus peru) leukocytes. Fish Shellfish Immunol. 70, 48–56.
Ali, I., Kanhayuwa, L., Rachdawong, S., and Rakshit, S.K. 2013. Identification, phylogenetic analysis and characterization of obligate halophilic fungi isolated from a man-made solar saltern in Phetchaburi province, Thailand. Ann. Microbiol. 63, 887–895.
Ali, I., Siwarungson, N., Punnapayak, H., Lotrakul, P., Prasongsuk, S., Bankeeree, W., and Rakshit, S. 2014. Screening of potential biotechnological applications from obligate halophilic fungi, isolated from a man-made solar saltern located in phetchaburi province, Thailand. Pak. J. Bot. 46, 983–988.
Brauers, G., Ebel, R., Edrada, R., Wray, V., Berg, A., Grafe, U., and Proksch, P. 2001. Hortein, a new natural product from the fungus Hortaea werneckii associated with the sponge Aplysina aerophoba. J. Nat. Prod. 64, 651–652.
Butinar, L., Frisvad, J.C., and Gunde-Cimerman, N. 2011. Hypersaline waters - a potential source of foodborne toxigenic aspergilli and penicillia. FEMS Microbiol. Ecol. 77, 186–199.
Butinar, L., Sonjak, S., Zalar, P., Plemenitas, A., and Gunde-Cimerman, N. 2005a. Melanized halophilic fungi are eukaryotic members of microbial communities in hypersaline waters of solar salterns. Bot. Mar. 48, 73–79.
Butinar, L., Zalar, P., Frisvad, J.C., and Gunde-Cimerman, N. 2005b. The genus Eurotium - members of indigenous fungal community in hypersaline waters of salterns. FEMS Microbiol. Ecol. 51, 155–166.
Cantrell, S.A., Casillas-Martinez, L., and Molina, M. 2006. Characterization of fungi from hypersaline environments of solar salterns using morphological and molecular techniques. Mycol. Res. 110, 962–970.
Cantrell, S.A., Dianese, J.C., Fell, J., Gunde-Cimerman, N., and Zalar, P. 2011. Unusual fungal niches. Mycologia 103, 1161–1174.
Cantrell, S.A., Tkavc, R., Gunde-Cimerman, N., Zalar, P., Acevedo, M., and Baez-Felix, C. 2013. Fungal communities of young and mature hypersaline microbial mats. Mycologia 105, 827–836.
Castellani, A. 1964. A note on Glenosporella peralbida n. sp., a fungus found in three cases of Tinea alba palmaris. Mycopathol. Mycol. Appl. 23, 161–166.
Chavez, R., Fierro, F., Garcia-Rico, R.O., and Vaca, I. 2015. Filamentous fungi from extreme environments as a promising source of novel bioactive secondary metabolites. Front. Microbiol. 6, 903.
Chen, J., Xing, X.K., Zhang, L.C., Xing, Y.M., and Guo, S.X. 2012. Identification of Hortaea werneckii Isolated from mangrove plant Aegiceras comiculatum based on morphology and rDNA sequences. Mycopathologia 174, 457–466.
Chi, Z., Ma, C., Wang, P., and Li, H.F. 2007. Optimization of medium and cultivation conditions for alkaline protease production by the marine yeast Aureobasidium pullulans. Bioresour. Technol. 98, 534–538.
de Hoog, G.S. 1999. Ecology and evolution of black yeasts and their relatives. Stud. Mycol. 43, 3–4.
de Hoog, G.S., Beguin, H., and Batenburg-van de Vegte, W.H. 1997. Phaeotheca triangularis, a new meristematic black yeast from a himidifier. Antonie van Leeuwenhoek 71, 289–295.
De Leo, F., Lo Giudice, A., Alaimo, C., De Carlo, G., Rappazzo, A.C., Graziano, M., De Domenico, E., and Urzi, C. 2019. Occurrence of the black yeast Hortaea werneckii in the Mediterranean Sea. Extremophiles 23, 9–17.
Dolapsakis, N.P., Tafas, T., Abatzopoulos, T.J., Ziller, S., and Economou-Amilli, A. 2005. Abundance and growth response of microalgae at Megalon Embolon solar saltworks in northern Greece: An aquaculture prospect. J. Appl. Phycol. 17, 39–49.
Figueroa, L., Jimenez, C., Rodriguez, J., Areche, C., Chavez, R., Henriquez, M., de la Cruz, M., Diaz, C., Segade, Y., and Vaca, I. 2015. 3-Nitroasterric acid derivatives from an Antarctic sponge-derived Pseudogymnoascus sp. fungus. J. Nat. Prod. 78, 919–923.
Gasparic, M.B., Lenassi, M., Gostincar, C., Rotter, A., Plemenitas, A., Gunde-Cimerman, N., Gruden, K., and Zel, J. 2013. Insertion of a specific fungal 3′-phosphoadenosine-5′-phosphatase motif into a plant homologue improves halotolerance and drought tolerance of plants. PLoS One 8, e81872.
Gostincar, C., Grube, M., de Hoog, S., Zalar, P., and Gunde-Cimerman, N. 2010. Extremotolerance in fungi: evolution on the edge. FEMS Microbiol. Ecol. 71, 2–11.
Gunde-Cimerman, N., Plemenitas, A., and Oren, A. 2018. Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations. FEMS Microbiol. Rev. 42, 353–375.
Gunde-Cimerman, N., Ramos, J., and Plemenitas, A. 2009. Halotolerant and halophilic fungi. Mycol. Res. 113, 1231–1241.
Gunde-Cimerman, N. and Zalar, P. 2014. Extremely halotolerant and halophilic fungi inhabit brine in solar salterns around the globe. Food Technol. Biotechnol. 52, 170–179.
Gunde-Cimerman, N., Zalar, P., Hoog, S., and Plemenitas, A. 2000. Hypersaline waters in salterns - natural ecological niches for halophilic black yeasts. FEMS Microbiol. Ecol. 32, 235–240.
Gunde-Cimerman, N., Zalar, P., Petrovic, U., Turk, M., Kogej, T., de Hoog, S., and Plemenitas, A. 2004. Fungi in salterns, pp. 103–113. In Ventosa, A. (ed.), Halophilic microorganisms. Springer Berling Heidelberg, Germany.
He, J., Wijeratne, E.M., Bashyal, B.P., Zhan, J., Seliga, C.J., Liu, M.X., Pierson, E.E., Pierson 3rd, L.S., VanEtten, H.D., and Gunatilaka, A.A. 2004. Cytotoxic and other metabolites of Aspergillus inhabiting the rhizosphere of Sonoran desert plants. J. Nat. Prod. 67, 1985–1991.
Hohmann, S. 2002. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 66, 300–372.
Javor, B.J. 1983. Nutrients and ecology of the Western Salt and Exportadora de Sal saltern brines, pp. 195–205. In Schreiber, B.C. and Harner, H.L. (eds.), 6th Symposium on Salt, The Salt Institute, Toronto, Canada.
Javor, B.J. 2002. Industrial microbiology of solar salt production. J. Ind. Microbiol. Biotechnol. 28, 42–47.
Jiang, W., Ye, P., Chen, C.T., Wang, K., Liu, P., He, S., Wu, X., Gan, L., Ye, Y., and Wu, B. 2013. Two novel hepatocellular carcinoma cycle inhibitory cyclodepsipeptides from a hydrothermal vent crab-associated fungus Aspergillus clavatus C2WU. Mar. Drugs 11, 4761–4772.
Kogej, T., Gorbushina, A.A., and Gunde-Cimerman, N. 2006. Hypersaline conditions induce changes in cell-wall melanization and colony structure in a halophilic and a xerophilic black yeast species of the genus Trimmatostroma. Mycol. Res. 110, 713–724.
Kogej, T., Gostincar, C., Volkmann, M., Gorbushina, A.A., and Gunde Cimerman, N. 2005a. Mycosporines in extremophilic fungi-novel compelemntary osmolytes? Environ. Chem. 3, 105–110.
Kogej, T., Ramos, J., Plemenitas, A., and Gunde-Cimerman, N. 2005b. The halophilic fungus Hortaea werneckii and the halotolerant fungus Aureobasidium pullulans maintain low intracellular cation concentrations in hypersaline environments. Appl. Environ. Microbiol. 71, 6600–6605.
Kogej, T., Stein, M., Volkmann, M., Gorbushina, A.A., Galinski, E.A., and Gunde-Cimerman, N. 2007. Osmotic adaptation of the halophilic fungus Hortaea werneckii: role of osmolytes and melanization. Microbiology 153, 4261–4273.
Kozakiewicz, Z. 1989. Aspergillus species on stored products. Mycological Papers 161, 1–188.
Kralj Kuncic, M., Kogej, T., Drobne, D., and Gunde-Cimerman, N. 2010. Morphological response of the halophilic fungal genus Wallemia to high salinity. Appl. Environ. Microbiol. 76, 329–337.
Kushiner, D.J. 1978. Life in high salt and solute concentrations, pp. 317–368. In Kushiner, D.J. (ed.), Microbial life in extreme environments. Academic Press, London, UK.
Larsen, H. 1986. Halophilic and halotolerant microorganisms-an overview and historical perspective. FEMS Microbiol. Rev. 2, 3–7.
Lebogang, L., Taylor, J.E., and Mubyana-John, T. 2009. A preliminary study of the fungi associated with saltpans in Botswana and their anti-microbial properties. Biorem. Biodiv. Bioavail. 3, 61–71.
Lenassi, M., Gostincar, C., Jackman, S., Turk, M., Sadowski, I., Nislow, C., Jones, S., Birol, I., Cimerman, N.G., and 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, e71328.
Lenassi, M., Zajc, J., Gostincar, C., Gorjan, A., Gunde-Cimerman, N., and Plemenitas, 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.
Li, Y., Ye, D., Chen, X., Lu, X., Shao, Z., Zhang, H., and Che, Y. 2009. Breviane spiroditerpenoids from an extreme-tolerant Penicillium sp. isolated from a deep sea sediment sample. J. Nat. Prod. 72, 912–916.
Liu, T., Zhang, S., Zhu, J., Pan, H., Bai, J., Li, Z., Guan, L., Liu, G., Yuan, C., Wu, X., et al. 2015. Two new amides from a halotolerant fungus, Myrothecium sp. GS-17. J. Antibiot. (Tokyo) 68, 267–270.
Lu, Z.Y., Lin, Z.J., Wang, W.L., Du, L., Zhu, T.J., Fang, Y.C., Gu, Q.Q., and Zhu, W.M. 2008. Citrinin dimers from the halotolerant fungus Penicillium citrinum B-57. J. Nat. Prod. 71, 543–546.
Ma, L.J., Roggers, S.O., Catranis, C.M., and Starmer, W.T. 2000. Detection and characterization of ancient fungi entrapped in glacial ice. Mycologia 92, 286–295.
Madkour, F.F. and Gaballah, M.M. 2012. Phytoplankton assemblage of a solar saltern in Port Fouad, Egypt. Oceanologia 54, 687–700.
Maturrano, L., Santos, F., Rossello-Mora, R., and Anton, J. 2006. Microbial diversity in Maras salterns, a hypersaline environment in the Peruvian Andes. Appl. Environ. Microbiol. 72, 3887–3895.
Mok, W.Y., Catelo, F.P., and Barreto Da Silva, M.S. 1981. Occurrence of Exophiala werneckii on salted freshwater fish Osteoglossum bicirrhosum. Int. J. Food Sci. Technol. 16, 505–512.
Mudau, M.M. and Setati, M.E. 2006. Screening and identification of endomannanase-producing microfungi from hypersaline environments. Curr. Microbiol. 52, 477–481.
Nayak, S.S., Gonsalves, V., and Nazareth, S.W. 2012. Isolation and salt tolerance of halophilic fungi from mangroves and solar salterns in Goa - India. Indian J. Mar. Sci. 41, 164–172.
Nazareth, S. and Gonsalves, V. 2013. Aspergillus penicillioides-a true halophile existing in hypersaline and polyhaline econiches. Ann. Microbiol. 64, 397–402.
Nazareth, S.W. and Gonsalves, V. 2014. Halophilic Aspergillus penicillioides from athalassohaline, thalassohaline, and polyhaline environments. Front. Microbiol. 5, 412.
Niu, S., Liu, D., Hu, X., Proksch, P., Shao, Z., and Lin, W. 2014. Spiromastixones A-O, antibacterial chlorodepsidones from a deep-sea-derived Spiromastix sp. fungus. J. Nat. Prod. 77, 1021–1030.
Ohtsuki, T. 1962. Studies on the glass mould: On two species of Aspergillus isolated from glass. Bot. Mag. Tokyo 75, 436–442.
Oren, A. 2009. Saltern evaporation ponds as model systems for the study of primary production processes under hypersaline conditions. Aquat. Microb. Ecol. 56, 193–204.
Oren, A., Stambler, N., and Dubinsky, Z. 1992. On the red coloration of saltern crystallizer ponds. Int. J. Salt Lake Res. 1, 77–89.
Pedros-Alio, C. 2004. Trophic ecology of solar salterns, pp. 33–48. In Ventosa, A. (ed.), Halophilic microorganisms. Springer, Berlin, Heidelberg, Germany.
Petrovic, U., Gunde-Cimerman, N., and Plemenitas, A. 2002. Cellular responses to environmental salinity in the halophilic black yeast Hortaea werneckii. Mol. Microbiol. 45, 665–672.
Pinto, C., Custodio, V., Nunes, M., Songy, A., Rabenoelina, F., Courteaux, B., Clement, C., Gomes, A.C., and Fontaine, F. 2018. Understand the potential role of Aureobasidium pullulans, a resident microorganism from grapevine, to prevent the infection caused by Diplodia seriata. Front. Microbiol. 9, 3047.
Prasongsuk, S., Lotrakul, P., Ali, I., Bankeeree, W., and Punnapayak, H. 2018. The current status of Aureobasidium pullulans in biotechnology. Folia Microbiol. (Praha) 63, 129–140.
Rampelotto, P.H. 2013. Extremophiles and extreme environments. Life (Basel) 3, 482–485.
Raol, G.G., Raol, B.V., Prajapati, V.S., and Bhavsar, N.H. 2015. Utilization of agro-industrial waste for beta-galactosidase production under solid state fermentation using halotolerant Aspergillus tubingensis GR1 isolate. 3 Biotech. 5, 411–421.
Stierle, D.B., Stierle, A.A., Patacini, B., McIntyre, K., Girtsman, T., and Bolstad, E. 2011. Berkeleyones and related meroterpenes from a deep water acid mine waste fungus that inhibit the production of interleukin 1-β from induced inflammasomes. J. Nat. Prod. 74, 2273–2277.
Tepsic, K., Gunde-Cimerman, N., and Frisvad, J.C. 1997. Growth and mycotoxin production by Aspergillus fumigatus strains isolated from a saltern. FEMS Microbiol. Lett. 157, 9–12.
Turk, M., Abramovic, Z., Plemenitas, A., and Gunde-Cimerman, N. 2007. Salt stress and plasma-membrane fluidity in selected extremophilic yeasts and yeast-like fungi. FEMS Yeast Res. 7, 550–557.
Turk, M., Mejanelle, L., Sentjurc, M., Grimalt, J.O., Gunde-Cimerman, N., and Plemenitas, A. 2004. Salt-induced changes in lipid composition and membrane fluidity of halophilic yeast-like melanized fungi. Extremophiles 8, 53–61.
Vaupotic, T., Gunde-Cimerman, N., and Plemenitas, A. 2007. Novel 3′-phosphoadenosine-5′-phosphatases from extremely halotolerant Hortaea werneckii reveal insight into molecular determinants of salt tolerance of black yeasts. Fungal Genet. Biol. 44, 1109–1122.
Ventosa, A. and Arahal, D.R. 2011. Physicochemical characteristics of hypersaline environments and their biodiversity. Extremophiles 2, 247–262.
Wang, L., Chi, Z., Wang, X., Liu, Z., and Li, J. 2007a. Diversity of lipase-producing yeasts from marine environments and oil hydrolysis by their crude enzymes. Ann. Microbiol. 57, 495–501.
Wang, W., Wang, Y., Tao, H., Peng, X., Liu, P., and Zhu, W. 2009. Cerebrosides of the halotolerant fungus Alternaria raphani isolated from a sea salt field. J. Nat. Prod. 72, 1695–1698.
Wang, H., Zheng, J.K., Qu, H.J., Liu, P.P., Wang, Y., and Zhu, W.M. 2011a. A new cytotoxic indole-3-ethenamide from the halotolerant fungus Aspergillus sclerotiorum PT06-1. J. Antibiot. (Tokyo) 64, 679–681.
Wang, Y., Zheng, J., Liu, P., Wang, W., and Zhu, W. 2011b. Three new compounds from Aspergillus terreus PT06-2 grown in a high salt medium. Mar. Drugs 9, 1368–1378.
Wang, W., Zhu, T., Tao, H., Lu, Z., Fang, Y., Gu, Q., and Zhu, W. 2007b. Two new cytotoxic quinone type compounds from the halotolerant fungus Aspergillus variecolor. J. Antibiot. (Tokyo) 60, 603–607.
Wieland, A. and Kuhl, M. 2006. Regulation of photosynthesis and oxygen consumption in a hypersaline cyanobacterial mat (Camargue, France) by irradiance, temperature and salinity. FEMS Microbiol. Ecol. 55, 195–210.
Xiao, L., Liu, H., Wu, N., Liu, M., Wei, J., Zhang, Y., and Lin, X. 2013. Characterization of the high cytochalasin E and rosellichalasin producing-Aspergillus sp. nov. F1 isolated from marine solar saltern in China. World J. Microbiol. Biotechnol. 29, 11–17.
Yang, Y.L., Liao, W.Y., Liu, W.Y., Liaw, C.C., Shen, C.N., Huang, Z.Y., and Wu, S.H. 2009. Discovery of new natural products by intact-cell mass spectrometry and LC-SPE-NMR: malbranpyrroles, novel polyketides from thermophilic fungus Malbranchea sulfurea. Chemistry 15, 11573–11580.
Zafrilla, B., Martinez-Espinosa, R.M., Alonso, M.A., and Bonete, M.J. 2010. Biodiversity of Archaea and floral of two inland saltern ecosystems in the Alto Vinalopo Valley, Spain. Saline Syst. 6, 10.
Zajc, J., Kogej, T., Galinski, E.A., Ramos, J., and Gunde-Cimerman, N. 2014. Osmoadaptation strategy of the most halophilic fungus, Wallemia ichthyophaga, growing optimally at salinities above 15% NaCl. Appl. Environ. Microbiol. 80, 247–256.
Zajc, J., Liu, Y., Dai, W., Yang, Z., Hu, J., Gostincar, C., and Gunde-Cimerman, N. 2013. Genome and transcriptome sequencing of the halophilic fungus Wallemia ichthyophaga: haloadaptations present and absent. BMC Genomics 14, 617.
Zalar, P., de Hoog, G.S., and Gunde-Cimerman, N. 1999a. Ecology of halotolerant dothideaceous black yeasts. Stud. Mycol. 43, 38–48.
Zalar, P., de Hoog, G.S., and Gunde-Cimerman, N. 1999b. Trimmatostroma salinum, a new species from hypersaline water. Stud. Mycol. 43, 57–62.
Zalar, P., de Hoog, G.S., Schroers, H.J., Frank, J.M., and 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.
Zalar, P., Frisvad, J.C., Gunde-Cimerman, N., Varga, J., and Samson, R.A. 2008. Four new species of Emericella from the Mediterranean region of Europe. Mycologia 100, 779–795.
Zheng, J., Wang, Y., Wang, J., Liu, P., Li, J., and Zhu, W. 2013. Antimicrobial ergosteroids and pyrrole derivatives from halotolerant Aspergillus flocculosus PT05-1 cultured in a hypersaline medium. Extremophiles 17, 963–971.
Acknowledgements
This work was supported by two individual grants from the National Marine Biodiversity Institute of Korea (MABIK, 2019M00400 and 2019M00700).
Author information
Authors and Affiliations
Corresponding author
Additional information
Conflicts of Interest
The authors have no conflicts of interest to declare.
Rights and permissions
About this article
Cite this article
Chung, D., Kim, H. & Choi, H.S. Fungi in salterns. J Microbiol. 57, 717–724 (2019). https://doi.org/10.1007/s12275-019-9195-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12275-019-9195-3