Abstract
The specific features of halotolerant fungi are analyzed to assess their potential for indicating chemical contamination of saline soils and to search for the promising test species for laboratory mycotesting. The listed halophile and halotolerant micromycete genera comprise the representatives suitable as indicators of pollution by heavy metals, oil products, and other toxicants on the background of increased salinity of soil substrates. The moderately halotolerant species of micromycetes are proposed as promising for biotesting of the soils with moderate salinity. Morphological, physiological, and molecular mechanisms underlying the adaptation of halophilic and halotolerant fungi to an increased salinity of habitats are analyzed. The responses of fungal communities to the combined impact of salinization and toxic substances of different natures are discussed. The methodological aspects of the application of halotolerant fungi for biotesting the degree of disturbance of saline soils are considered, including the composition of media, cultivation conditions, and test responses of fungal cultures optimal for an adequate assessment of the degree of fungal halotolerance and the ecotoxicity of soil samples.
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REFERENCES
V. S. Artamonova, L. Yu. Dits, T. N. Elizarova, and I. V. Lyutykh, “Technogenic salinization of soils and their microbiological characterization,” Contemp. Probl. Ecol. 3 (3), 323–330 (2010). )https://doi.org/10.1134/S1995425510030112
N. I. Bazilevich and E. I. Pankova, “Experience in soil classification based on the content of toxic salts and ions,” Byull. Pochv. Inst. im. V. V. Dokuchaeva 5, 36–40 (1972).
Sh. A. Begmatov, O. V. Selitskaya, L. V. Vasileva, Yu. Yu. Berestovskaja, N. A. Manucharova, and N. V. Drenova, “Morphophysiological features of some cultivable bacteria from saline soils of the Aral Sea region,” Eurasian Soil Sci. 53 (1), 90–96 (2020). https://doi.org/10.1134/S1064229320010044
N. A. Vernigorova, S. I. Kolesnikov, and K. Sh. Kazeev, “Change in the biological activity of Taman solonchaks under conditions of oil and heavy metal pollution,” Izv. Samar. Nauchn. Tsentra Ross. Akad. Nauk 18 (2), 591–593 (2016).
A. O. Gerasimov and Yu. M. Polyak, “Estimation of the effect of salinity on the allelopathic activity of micromycetes in soddy-podzolic soil,” Agrokhimiya, No. 3, 51–59 (2021). https://doi.org/10.31857/S0002188121030078
G. Yu. Gorlacheva, “Remigrant and immigrant micromycetes of the water system of the Kuma–Manych depression and the Caspian Sea,” Vestn. Yuzhn. Nauchn. Tsentra Ross. Akad. Nauk 4 (4), 52–56 (2008).
L. I. Domracheva, S. G. Skugoreva, A. L. Kovina, A. I. Korotkikh, P. A. Starikov, and T. Ya. Ashikhmina, “Specifics of plant-microbial complexes under anthropogenic soil pollution (review),” Teor. Prikl. Ekol., No. 3, 14–25 (2022). https://doi.org/10.25750/1995-4301-2022-3-014-025
M. F. Dorokhova, N. E. Kosheleva, and E. V. Terskaya, “Ecological state of urban soils under conditions of anthropogenic salinization and pollution (using the example of the North-Western District of Moscow),” Teor. Prikl. Ekol., No. 4, 16–24 (2015).
Salinized Soils of Russia, Ed. by L. L. Shishov and E. I. Pankova (IKTs Akademkniga, Moscow, 2006) [in Russian].
D. G. Zvyagintsev, G. M. Zenova, and G. V. Oborotov, “Mycelial bacteria of saline soils,” Eurasian Soil Sci. 41 (10), 1107–1114 (2008). https://doi.org/10.1134/S106422930810013X
Modeling the Processes of Soil Salinization and Alkalinity, Ed. by V. A. Kovda and I. M. Sabol’ch (Nauka, Moscow, 1980) [in Russian].
M. V. Nosova and V. P. Seredina, “Technogenic halogenesis of oil-contaminated soils of floodplain ecosystems under conditions of humid soil formation and its environmental consequences,” Teor. Prikl. Ekol., No. 3, 74–79 (2021). https://doi.org/10.25750/1995-4301-2021-3-074-079
E. I. Pankova, M. I. Gerasimova, and T. V. Korolyuk, “Salt-affected soils in Russian, American, and international soil classification systems,” Eurasian Soil Sci. 51 (11), 1297–1308 (2018). https://doi.org/10.1134/S1064229318110078
E. N. Pisarenko, “Use of sunflower as a remediant of contaminated soils,” Teor. Prikl. Ekol., No. 2, 47–49 (2009).
G. F. Rafikova, E. V. Kuzina, E. A. Stolyarova, S. R. Mukhamatd’yarova, and O. N. Loginov, “Complexes of micromycetes of leached chernozem under oil contamination and the introduction of oil-destructor microorganisms,” Mikol. Fitopatol. 54 (2), 107–115 (2020).
S. S. Sanin, N. P. Neklesova, A. A. Sanina, and E. V. Pacholkova, Methodological Recommendations for Creating Infectious Backgrounds for Immunogenetic Studies in Wheat (Vseross. Nauchno-Issled. Inst. Fitopatol., Moscow, 2008) [in Russian].
E. V. Smolyanyuk, E. N. Bilanenko, V. M. Tereshina, A. V. Kachalkin, and O. V. Kamzolkina, “Effect of sodium chloride concentration in the medium on the composition of the membrane lipids and carbohydrates in the cytosol of the fungus Fusarium sp.,” Microbiology (Moscow) 82 (5), 600–608 (2013). https://doi.org/10.1134/S0026261713050111
V. A. Terekhova, Micromycetes in the Ecological Evaluation of Aquatic and Terrestrial Ecosystems (Nauka, Moscow, 2007) [in Russian].
V. A. Terekhova, A. A. Rakhleeva, E. V. Fedoseeva, and A. P. Kiryushina, Workshop on Biotesting of Soil Ecotoxicity (Moscow, 2022) [in Russian].
A. I. Fokina, L. I. Domracheva, A. S. Ol’kova, S. G. Skugoreva, E. I. Lyalina, G. I. Berezin, and L. V. Darovskikh, “Study of the toxicity of urban soil samples contaminated with heavy metals,” Izv. Samar. Nauchn, Tsentra Ross. Akad. Nauk 18 (2), 544–550 (2016).
D. Khasan, I. S. Kovtun, and M. V. Efimova, “Effect of chloride salinity on seed germination and seedling growth of Brassica napus L.,” Vestn. Tomsk. Gos. Univ. Ser. Biol., No. 4 (16), 108–112 (2011).
R. Kh. Enazarov, A. A. Vasil’eva, S. M. Petrenko, P. V. Makolova, and Yu. A. Litovka, “Screening of salt-tolerant micromycetes promising for bioremediation of saline soils,” in Forest and Chemical Complexes—Problems and Solutions: Collection of Materials on the Results of the All-Russian Scientific and Practical Conference (Krasnoyarsk, 2021), pp. 306–310.
E. A. Ianutsevich, O. A. Danilova, N. V. Groza, and V. M. Tereshina, “Membrane lipids and cytosol carbohydrates in Aspergillus niger under osmotic, oxidative, and cold impact,” Microbiology (Moscow) 85 (3), 302–310 (2016). https://doi.org/10.1134/S0026261716030152
M. Abadias, N. Teixido, J. Usall, I. Vinas, and N. Magan, “Solute stresses affect growth patterns, endogenous water potentials and accumulation of sugars and sugar alcohols in cells of the biocontrol yeast Candida sake,” J. Appl. Microbiol. 89, 1009–1017 (2000). https://doi.org/10.1046/j.1365-2672.2000.01207.x
L. Adler, A. Pedersen, and I. Tunblad-Johansson, “Polyol accumulation by two filamentous fungi grown at different concentrations of NaCl,” Physiol. Plant. 56 (2), 139–142 (1982). https://doi.org/10.1111/j.1399-3054.1982.tb00315.x
A. Bano, J. Hussain, A. Akbar, K. Mehmood, M. Anwar, HasniM. Sharif, S. Ullah, S. Sajid, and I. Ali, “Biosorption of heavy metals by obligate halophilic fungi,” Chemosphere 199, 218–222 (2018). https://doi.org/10.1016/j.chemosphere.2018.02.043
R. A. Batista-García, E. Balcázar-López, E. Miranda-Miranda, A. Sánchez-Reyes, L. Cuervo-Soto, D. Aceves-Zamudio, K. Atriztán-Hernández, C. Morales-Herrera, R. Rodríguez-Hernández, and J. Folch-Mallol, “Characterization of lignocellulolytic activities from a moderate halophile strain of Aspergillus caesiellus isolated from a sugarcane bagasse fermentation,” PLoS One 9, 105893 (2014). https://doi.org/10.1371/journal.pone.0105893
M. Bronicka, A. Raman, D. Hodgkins, and H. Nicol, “Abundance and diversity of fungi in a saline soil in central-west New South Wales, Australia,” Sydowia 59 (1), 7–24 (2007).
O. A. Danilova, E. A. Ianutsevich, S. A. Bondarenko, M. L. Georgieva, D. A. Vikchizhanina, N. V. Groza, E. N. Bilanenko, and V. M. Tereshina, “Osmolytes and membrane lipids in the adaptation of micromycete Emericellopsis alkalina to ambient pH and sodium chloride,” Fungal Biol. 124, 884–891 (2020). https://doi.org/10.1016/j.funbio.2020.07.004
F. de Lima Alves, A. Stevenson, E. Baxter, J. L. M. Gillion, F. Hejazi, S. Hayes, I. E. G. Morrison, et al., “Concomitant osmotic and chaotropicity induced stresses in Aspergillus wentii: compatible solutes determine the biotic window,” Curr. Genet. 61, 457–477 (2015). https://doi.org/10.1007/s00294-015-0496-8
S.-S. Gao, X.-M. Li, F.-Y. Du, C.-S. Li, P. Proksch, and B.-G. Wang, “Secondary metabolites from a marine-derived endophytic fungus Penicillium chrysogenum QEN-24S,” Mar. Drugs 9, 5970 (2010).
D. González-Abradelo, Y. Pérez-Llano, H. Peidro-Guzmána, M. del R. Sánchez-Carbente, J. L. Folch-Mallol, E. Aranda, V. K. Vaidyanathan, H. Cabana, N. Gunde-Cimerman, and R. A. Batista-Garcia, “First demonstration that ascomycetous halophilic fungi (Aspergillus sydowii and Aspergillus destruens) are useful in xenobiotic mycoremediation under high salinity conditions,” Bioresour. Technol. 279, 287–296 (2019). https://doi.org/10.1016/j.biortech.2019.02.002
A. A. Grum-Grzhimaylo, M. L. Georgieva, S. A. Bondarenko, A. J. M. Debets, and E. N. Bilanenko, “On the diversity of fungi from soda soils,” Fungal Diversity 76, 27–74 (2016). https://doi.org/10.1007/s13225-015-0320-2
N. Gunde-Cimerman, J. C. Frisvad, P. Zalar, and A. Plemenitaš, “Halotolerant and halophilic fungi,” in Biodiversity of Fungi—Their Role in Human Life (Oxford & IBH Publishing Co. Pvt. Ltd., New Delhi, 2005), pp. 69–128.
N. Gunde-Cimerman, J. Ramos, and A. Plemenitaš, “Halotolerant and halophilic fungi,” Mycol. Res. 113, 1231–1241 (2009). https://doi.org/10.1016/j.mycres.2009.09.002
N. Gunde-Cimerman, P. Zalar, S. de Hoog, and A. Plemenitaš, “Hypersaline waters in salterns – natural eco-logical niches for halophilic black yeasts,” FEMS Microbiol. Ecol. 32, 235–240 (2000). https://doi.org/10.1111/j.1574-6941.2000.tb00716.x
N. Gunde-Cimerman, P. Zalar, U. Petrovič, M. Turk, T. Kogej, G. S. de Hoog, and A. Plemenitaš, “Fungi in salterns,” in Halophilic Microorganisms (Springer, Berlin, 2004), pp. 103–113. https://doi.org/10.1007/978-3-662-07656-9_7
K. D. Hyde, V. V. Sarma, and E. B. G. Jones, “Morphology and taxonomy of higher marine fungi,” in Marine Mycology. A Practical Approach. Fungal Diversity Research Series 1 (Fungal Diversity Press, Hong Kong, 2000), pp. 172–204.
P. L. Kashyap, A. Rai, R. Singh, H. Chakdar, S. Kumar, and A. K. Srivastava, “Deciphering the salinity adaptation mechanism in Penicilliopsis clavariiformis AP, a rare salt tolerant fungus from mangrove,” J. Basic Microbiol. 56, 779–791 (2016). https://doi.org/10.1002/jobm.201500552
Q. A. Mandeel, “Biodiversity of the genus Fusarium in saline soil habitats,” J. Basic Microbiol. 46 (6), 480–494 (2006). https://doi.org/10.1002/jobm.200510128
M. U. Marghoob, A. Rodriguez-Sanchez, A. Imran, F. Mubeen, and L. Hoagland, “Diversity and functional traits of indigenous soil microbial flora associated with salinity and heavy metal concentrations in agricultural fields within the Indus Basin region, Pakistan,” Front. Microbiol. 13, (2022). https://doi.org/10.3389/fmicb.2022.1020175
H. Musa, F. H. Kasim, GunnyA. A. Nagoor, and S. C. B. Gopinath, “Salt-adapted moulds and yeasts: Potentials in industrial and environmental biotechnology,” Process Biochem. (Oxford, U. K.) 69, 33–44 (2018). https://doi.org/doi:10.1016/j.procbio.2018.03.026
A. Plemenitaš and N. Gunde-Cimerman, “Cellular responses in the halophilic black yeast Hortaea werneckii to high environmental salinity,” in Adaptation to Life at High Salt Concentrations in Archaea, Bacteria, and Eukarya. Cellular Origin, Life in Extreme Habitats and Astrobiology (Springer, Dordrecht, 2005), Vol. 9, pp. 453–470. https://doi.org/10.1007/1-4020-3633-7_29
T. Ramesh, R. Yamunadevi, A. Sundaramanickam, M. Thangaraj, R. Kumaran, and D. Annadurai, “Biodiversity of the fungi in extreme marine environments,” in Fungi Bio-Prospects in Sustainable Agriculture, Environment and Nano-Technology (2021), pp. 75–100. https://doi.org/10.1016/B978-0-12-821925-6.00005-8
D. E. N. Rangel, G. U. L. Braga, E. K. K. Fernandes, C. A. Keyser, J. E. Hallsworth, and D. W. Roberts, “Stress tolerance and virulence of insect-pathogenic fungi are determined by environmental conditions during conidial formation,” Curr. Genet. 61, 383–404 (2015). https://doi.org/10.1007/s00294-015-0477-y
G. Sambuu, L. A. Garetova, E. L. Imranova, O. A. Kirienko, N. K. Fischer, Kh. Gantumur, and G. V. Kharitonova, “Biogeochemical characteristics of soils in the Dzunb-ayan oil-producing area (Eastern Mongolia),” Biogeosyst. Tech. 6 (1), 46–58 (2019). https://doi.org/10.13187/bgt.2019.1.46
E. V. Smolyanuk and E. N. Bilanenko, “Communities of halotolerant micromycetes from the areas of natural salinity,” Microbiology (Moscow) 80 (6), 877–883 (2011). https://doi.org/10.1134/S002626171106021X
S. Tibell, L. Tibell, K-L. Pang, M. Calabon, and E. B. Gareth Jones, “Marine fungi of the Baltic Sea,” Mycology 11, 195–213 (2020). https://doi.org/10.1080/21501203.2020.1729886
A. N. Yadav, P. Verma, V. Kumar, P. Sangwan, S. Mishra, N. Panjiar, V. K. Gupta, and A. K. Saxena, “Biodiversity of the genus Penicillium in different habitats,” in New and Future Developments in Microbial Biotechnology and Bioengineering (2018). https://doi.org/10.1016/B978-0-444-63501-3.00001-6
P. H. Yancey, “Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses,” J. Exp. Biol. 208, 2819–2830 (2005). https://doi.org/10.1242/jeb.01730
J. Zajc, P. Zalar, A. Plemenitaš, and N. Gunde-Cimerman, “The mycobiota of the salterns,” in Biology of Marine Fungi (Springer, Berlin, 2012), Vol. 53, pp. 133–158. https://doi.org/10.1007/978-3-642-23342-5_7
P. Zalarc, G. S. de Hoog, H. J. Schroers, J. Crous, and J. Z. Groenewald, “Phylogeny and ecology of the ubiquitous saprobe Cladosporium shpaerospermum, with descriptions of seven new species from hypersaline environments,” Stud. Mycol. 58, 157–183 (2007). https://doi.org/10.3114/sim.2007.58.06
W-W. Zhang, C. Wang, R. Xue, and L-J. Wang, “Effects of salinity on the soil microbial community and soil fertility,” J. Integr. Agric. 18 (6), 1360–1368 (2019). https://doi.org/10.1016/S2095-3119(18)62077-5
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Fedoseeva, E.V., Terekhova, V.A. Salt Tolerance of Fungi and Prospects for Mycodiagnostics of Contamination in Saline Soils: A Review. Eurasian Soil Sc. 57, 635–645 (2024). https://doi.org/10.1134/S1064229323603165
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DOI: https://doi.org/10.1134/S1064229323603165