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Salt Tolerance of Fungi and Prospects for Mycodiagnostics of Contamination in Saline Soils: A Review

  • SOIL BIOLOGY
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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

  1. 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

    Article  Google Scholar 

  2. 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).

    Google Scholar 

  3. 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

    Article  CAS  Google Scholar 

  4. 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).

    Google Scholar 

  5. 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

    Article  Google Scholar 

  6. 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).

    Google Scholar 

  7. 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

  8. 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).

  9. Salinized Soils of Russia, Ed. by L. L. Shishov and E. I. Pankova (IKTs Akademkniga, Moscow, 2006) [in Russian].

  10. 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

    Article  Google Scholar 

  11. Modeling the Processes of Soil Salinization and Alkalinity, Ed. by V. A. Kovda and I. M. Sabol’ch (Nauka, Moscow, 1980) [in Russian].

    Google Scholar 

  12. 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

  13. 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

    Article  CAS  Google Scholar 

  14. E. N. Pisarenko, “Use of sunflower as a remediant of contaminated soils,” Teor. Prikl. Ekol., No. 2, 47–49 (2009).

  15. 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).

    Google Scholar 

  16. 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].

    Google Scholar 

  17. 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

    Article  CAS  Google Scholar 

  18. V. A. Terekhova, Micromycetes in the Ecological Evaluation of Aquatic and Terrestrial Ecosystems (Nauka, Moscow, 2007) [in Russian].

    Google Scholar 

  19. V. A. Terekhova, A. A. Rakhleeva, E. V. Fedoseeva, and A. P. Kiryushina, Workshop on Biotesting of Soil Ecotoxicity (Moscow, 2022) [in Russian].

  20. 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).

    Google Scholar 

  21. 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).

  22. 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.

  23. 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

    Article  CAS  Google Scholar 

  24. 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

    Article  CAS  Google Scholar 

  25. 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

    Article  CAS  Google Scholar 

  26. 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

    Article  CAS  Google Scholar 

  27. 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

    Article  CAS  Google Scholar 

  28. 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).

    Google Scholar 

  29. 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

    Article  CAS  Google Scholar 

  30. 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

    Article  CAS  Google Scholar 

  31. 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).

    Article  Google Scholar 

  32. 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

    Article  CAS  Google Scholar 

  33. 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

    Article  Google Scholar 

  34. 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.

    Google Scholar 

  35. 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

    Article  CAS  Google Scholar 

  36. 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

    Article  CAS  Google Scholar 

  37. 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

  38. 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.

    Google Scholar 

  39. 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

    Article  CAS  Google Scholar 

  40. 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

    Article  Google Scholar 

  41. 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

  42. 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

  43. 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

  44. 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

  45. 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

    Article  CAS  Google Scholar 

  46. 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

    Article  Google Scholar 

  47. 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

    Article  CAS  Google Scholar 

  48. 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

    Article  CAS  Google Scholar 

  49. 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

  50. 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

    Article  CAS  Google Scholar 

  51. 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

  52. 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

    Article  Google Scholar 

  53. 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

    Article  CAS  Google Scholar 

  54. https://fgis.gost.ru/fundmetrology/registry/16

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This work was supported by the Russian Science Foundation, project no. 22-24-00666.

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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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