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Role of Lipids in the Thermal Plasticity of Basidial Fungus Favolaschia Manipularis

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Role of Lipids in the Thermal Plasticity of Basidial Fungus Favolaschia Manipularis Canadian Journal of Microbiology Role of lipids in the thermal plasticity of basidial fungus Favolaschia manipularis Journal: Canadian Journal of Microbiology Manuscript ID cjm-2019-0284.R1 Manuscript Type: Article Date Submitted by the 26-Jul-2019 Author: Complete List of Authors: Senik, Svetlana; Komarov Botanical Institute RAS, lab. of fungal biochemistry Psurtseva, Nadezhda ; Komarov Botanical Institute RAS, lab. of fungal biochemistry Shavarda, DraftAlexey ; Komarov Botanical Institute RAS, lab. of phytochemistry Kotlova, Ekaterina ; Komarov Botanical Institute RAS, lab. of phytochemistry basidiomycetes, Filoboletus manipularis, sterols, 9(11)- Keyword: dehydroergosterol, ergosterol peroxide Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/cjm-pubs Page 1 of 30 Canadian Journal of Microbiology 1 Full paper 2 Role of lipids in the thermal plasticity of basidial fungus Favolaschia manipularis 3 Svetlana V. Senik, Nadezhda V. Psurtseva, Alexey L. Shavarda, Ekaterina R. Kotlova 4 Komarov Botanical Institute, Russian Academy of Sciences, 2 Professor Popov str., St. Petersburg, 5 197376, Russia 6 7 E-mail addresses: [email protected] (S.V. Senik), [email protected] (N.V. Psurtseva), [email protected] (A.L. 8 Shavarda), [email protected] (E.R. Kotlova). 9 10 Corresponding author: S.V. Senik, Komarov Botanical Institute, 2 Professor Popov str., St. Petersburg, 197376, Russia; 11 Tel.: +7 911 221 79 45; fax: +7 812 372 54 43; e-mail address: [email protected]. 12 13 Draft 14 15 1 https://mc06.manuscriptcentral.com/cjm-pubs Canadian Journal of Microbiology Page 2 of 30 16 Abstract 17 In this study, we examined the lipid composition of two strains of the tropical basidiomycete 18 Favolaschia manipularis (Berk.) Teng, which differ in their adaptive potential to high (35°C) and 19 low (5°C) temperatures. The results suggest that adaptation to extreme temperatures involves a 20 change in the molecular composition of sterols, in addition to other well-known mechanisms of 21 regulating membrane thickness and fluidity, such as changes in the lipid unsaturation and in the 22 proportion of bilayer and non-bilayer-forming lipids. It was demonstrated for the first time that 23 adaptation to high temperature stress in fungi is accompanied by the accumulation of 9(11)- 24 dehydroergosterol and ergosterol peroxide. Furthermore, increased thermal plasticity correlates with 25 high storage lipid (triglycerides) content, accumulation of phosphatidic acid in the membrane, and 26 an equal proportion of bilayer and non-bilayer lipids in the membrane. 27 28 Keywords: basidiomycetes, FiloboletusDraft manipularis, sterols, 9(11)-dehydroergosterol, 29 ergosterol peroxide. 30 31 Abbreviations: PC – phosphatidylcholines, PE – phosphatidylethanolamines, PS – 32 phosphatidylserines, PI – phosphatidylinositols, PA – phosphatidic acids, DPG – 33 diphosphatidylglycerols, GlCer – glucosylceramides, TAG – triacylglycerols, SE – sterol esters, 34 FFA – free fatty acids. 35 36 37 2 https://mc06.manuscriptcentral.com/cjm-pubs Page 3 of 30 Canadian Journal of Microbiology 38 1. INTRODUCTION 39 Temperature is one of the most important environmental factors affecting fungal distribution 40 (Heilmann-Clausen and Boddy 2008). Most wood-destroying basidiomycetes from temperate 41 regions are mesothermal organisms, i.e. able to grow at temperatures from 5-40°C with an optimal 42 temperature of about 25°C. Psychrophilic basidiomycetes with optimal growth between 16°C and 43 20°C, as well as psychrotolerants that do not grow but remain viable at temperatures below 5°C, 44 occupy ecological niches in the arctic and subarctic tundras and in cold desert regions (Frisvad 45 2008). Among basidiomycetes, there are no true thermophiles with optimal growth at 40-50°C that 46 do not grow at temperatures below 20°C. Nevertheless, thermotolerant basidial fungi that are able 47 to survive at high temperatures, albeit without active growth, are important components of fungal 48 communities, colonizing substrates such as hay, straw compost, tropical grass, bird nests, or tropical 49 soil (Magan 2007). Most studies on the fundamentalsDraft of fungal thermal plasticity have been carried 50 out in species from temperate regions, and the physiology of tropical fungi has been largely 51 understudied. 52 An important part of cell adaptation to temperature changes is the preservation of the 53 functionality of the membranes. In poikilothermic organisms, whose internal temperature varies 54 considerably, there are several known mechanisms for adaptation of their membranes to 55 temperature fluctuations. One such mechanism is the maintenance of a particular membrane 56 viscosity that is optimal for the functioning of membrane proteins (homeoviscous adaptation), 57 which is implemented by changing the fatty acid unsaturation status of membrane lipids (Sinensky 58 1974; Ernst et al. 2016). Another mechanism is to establish a balance between bilayer (stabilizing 59 bilayer membranes) and non-bilayer-forming lipids and the preservation of the membrane phase 60 state (McElhaney 1984; Hazel 1995). An alternative strategy for protection of membranes from the 61 damaging effects of non-optimal temperature involves the synthesis of membrane-stabilizing 62 compounds, both surrounding the membrane (trehalose and polyols) and intercalating into the 63 membrane (sterols, sphingolipids) (Dufourc 2008; Tereshina et al. 2010). The realization of a 3 https://mc06.manuscriptcentral.com/cjm-pubs Canadian Journal of Microbiology Page 4 of 30 64 particular adaptation strategy in response to thermal impact depends on many factors: the presence 65 of genetic determinants, physiological characteristics, and various external factors (e.g. degree and 66 duration of thermal stress). The effects of short (1-6 h) shock temperature on the physiology of 67 fungi are well studied (Tereshina et al. 2010; Kostadinova et al. 2012). However, very little is 68 known about effects of longer exposures. In this work, we studied the effects of prolonged exposure 69 (4 days) of two tropical basidiomycete strains to high and low positive temperatures. The study of 70 the adaptation of tropical strains to low temperatures is of practical interest due to the fact that most 71 cultures in the collections of microorganisms are stored at 4-5°С. However, many fungal strains 72 isolated from tropical habitats do not survive at this temperature and thus require special storage 73 conditions. 74 One such fungus became the object of the present study – the basidial luminescent mushroom 75 Favolaschia manipularis (Berk.) Teng (≡DraftFiloboletus manipularis (Berk.) Singer; Mycena 76 manipularis (Berk.) Sacc.), which is widely distributed in the tropical forests of Asia, Australia, and 77 Pacific regions. 78 No consensus has been reached regarding the taxonomic affiliation and phylogenetic 79 relationships of this mushroom. Nowadays, the largest mycological databases, such as Mycobank 80 (www.mycobank.org) and Index Fungorum (www.speciesfungorum.org), consider it to belong to 81 Favolashia, whereas some authors categorize it as Mycena (Desjardin et al. 2008), Filoboletus, or 82 Poromycena (Vydryakova et al. 2014). The biology and biochemical properties of this species are 83 still not understood. 84 This paper focuses on analysis of the lipid composition of two F. manipularis strains with 85 different growth rates and adaptive potentials to temperature variations. 86 87 2. MATERIALS AND METHODS 88 2.1. Fungal strains and culture conditions 4 https://mc06.manuscriptcentral.com/cjm-pubs Page 5 of 30 Canadian Journal of Microbiology 89 Strains of F. manipularis were isolated in culture in 2014 in the Cat Tien National Park in 90 Vietnam. According to Fick and Hijmans (2017), the temperature in this national park ranges from 91 18.5°C in January to 32.1°C in April. However, in the mountainous regions of Vietnam, in which 92 fruiting bodies of F. manipularis were also found, the temperature can drop to 9°C. In some other 93 regions of the species range, such as in Australia and on Kyushu island in Japan, it occurs and 94 survives at a temperature of 2-3°C. In hot seasons, the temperature in regions of F. manipularis 95 distribution can reach up to 33°C. 96 Two dikaryon strains of F. manipularis from the Basidiomycetes culture collection of the 97 Komarov Botanical Institute of the Russian Academy of Sciences (LE-BIN) 98 (www.wfcc.info/ccinfo/collection/by_id/1015) were used in this study. In the collection, the strains 99 are maintained by three methods: as stock cultures in tubes on beer wort agar (BWA) slants at 100 20°C, in cryovials under distilled water atDraft room temperature, and in cryovials at -80°C (in 10% 101 glycerol). Preliminary investigation showed that the two strains differed in growth rate – “slow- 102 growing” LE-BIN 3291 and “fast-growing” LE-BIN 3272. Growth rate was recorded every other 103 day in two mutually-perpendicular directions (linear mycelium extension in millimeters, and mean 104 growth rate in millimeters per day). 105 Taxonomical verification of the strains was done using DNA sequence analysis of the nrITS 106 region. DNA extraction from mycelia was performed following the protocol of the AxyPrep 107 Multisource Genomic DNA Miniprep Kit (Axygen Biosciences, California, USA). For 108 amplification and sequencing of the DNA region, the standard primers ITS1F and ITS4b were used 109 (www.biology.duke.edu/fungi/mycolab/primers.htm).
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