Abstract
Umbelopsis Amos & H.L. Barnett (Umbelopsidales, Mucoromycota) is a fungal genus reported as a producer of lipases and lipids. In the Southern Cone of America, there are a few records of Umbelopsis species. In this work, isolates from Nothofagus forests grown in Patagonia (Argentina) were identified using morphological and molecular criteria and characterized by their lipolytic enzyme production on Tween 20, Tween 80, olive oil, Nothofagus sawdust, and forest soil. Liquid and solid cultures and two different measurement methods were also tested. Furthermore, lipid composition in selected isolates was analyzed. Our results showed that Patagonian isolates belong to U. changbaiensis, U. nana, U. ramanniana, and U. vinacea. LPSc 520 and 521, isolated from forest soils in Tierra del Fuego and previously reported as Mortierella vinacea, were clustered in the U. ramanniana clade. A spectrophotometric method using 1,2-O-dilaurylrac-glycerol-3-glutaric acid-(6′-methylresorufin) ester as enzyme substrate was useful in detecting lipase activity in Umbelopsis isolates grown in liquid cultures; the results were compared with titrimetric analysis using NaOH. The U. ramanniana clade included isolates that showed their highest levels of lipase activity and lipid production in liquid cultures containing olive oil, Nothofagus sawdust, or forest soil. LPSc 521 showed the highest production of triacylglycerides and free fatty acids, such as palmitic acid, and unsaturated acids such as oleic, linoleic, and γ-linolenic. Since this lipid profile might be related to the habitat the fungus was isolated from, LPSc 521 may constitute an outstanding isolate for the synthesis of lipases and/or lipids adapted to cold conditions.








Availability of data and materials
All data generated or analyzed during this study are included in this published article (and its supplementary information files).
References
Amos, Barnett (1966) Umbelopsis versiformis, a new genus and species of the imperfects. Mycologia 58:805–808
Back EL, Allen LH (2000) Pitch control, wood resin and deresination, Eds. Tappi Press, Atlanta
Beisson F, Tiss A, Rivière C, Verger R (2000) Methods for lipase detection and assay: a critical review. Eur J Lipid Sci Technol 102(2):133–153. https://doi.org/10.1002/(SICI)1438-9312(200002)102:2%3c133::AID-EJLT133%3e3.0.CO;2-X
Bruzone MC, Fontenla SB, Vohník M (2015) Is the prominent ericoid mycorrhizal fungus Rhizoscyphus ericae absent in the Southern Hemisphere’s Ericaceae? A case study on the diversity of root mycobionts in Gaultheria spp. from northwest Patagonia, Argentina. Mycorrhiza 25(1):25–40. https://doi.org/10.1007/s00572-014-0586-3
Buráňová L, Řezanka T, Jandera A (1990) Screening for strains of the genus Mortierella, showing elevated production of highly unsaturated fatty acids. Folia Microbiol 35(6):578–582. https://doi.org/10.1007/BF02819994
Burkert JFM, Maugeri F, Rodrigues MI (2004) Optimization of extracellular lipase production by Geotrichum sp. using factorial design. Bioresour Technol 91(1):77–84. https://doi.org/10.1016/S0960-8524(03)00152-4
Cabello MN (1997) El género Mortierella (Zygomycotima, Mucorales) en Tierra del Fuego (Argentina). Bol Soc Argent Bot 33:53–58
Chatzifragkou A, Fakas S, Galiotou-Panayotou M, Komaitis M, Aggelis G, Papanikolaou S (2010) Commercial sugars as substrates for lipid accumulation in Cunninghamella echinulata and Mortierella isabellina fungi. Eur J Lipid Sci Technol 112(9):1048–1057. https://doi.org/10.1002/ejlt.201000027
Chatzifragkou A, Makri A, Belka A, Bellou S, Mavrou M, Mastoridou M, Mystrioti P, Onjaro G, Aggelis G, Papanikolaou S (2011) Biotechnological conversions of biodiesel derived waste glycerol by yeast and fungal species. Energy 36(2):1097–1108. https://doi.org/10.1016/j.energy.2010.11.040
Chemnitius GC, Erdmann H, Schmid RD (1992) Solubilized substrates for the on-line measurement of lipases by flow injection analysis during chromatographic enzyme purification. Anal Biochem 202(1):16–24. https://doi.org/10.1016/0003-2697(92)90199-H
Colen G, Junqueira RG, Moraes-Santos T (2006) Isolation and screening of alkaline lipase-producing fungi from Brazilian savanna soil. World J Microbiol Biotechnol 22(8):881–885
Collins T, Gerday C (2017) Enzyme catalysis in psychrophiles. In: Psychrophiles: from biodiversity to biotechnology. Springer, Cham, pp 209–235. https://doi.org/10.1007/s11274-005-9118-9
Czumaj A, Śledziński T (2020) Biological role of unsaturated fatty acid desaturases in health and disease. Nutrients 12(2):356. https://doi.org/10.3390/nu12020356
Di Rienzo J, Casanoves F, Balzarini M, Gonzalez L, Tablada M, Robledo C (2010) Infostat - Software estadístico. Grupo Infostat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar/
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:39–40
Dzurendova S, Zimmermann B, Kohler A, Tafintseva V, Slany O, Certik M, Shapaval V (2020) Microcultivation and FTIR spectroscopy-based screening revealed a nutrient-induced co-production of high-value metabolites in oleaginous Mucoromycota fungi. PLoS ONE 15(6):e0234870. https://doi.org/10.1371/journal.pone.0245016
Economou CN, Aggelis G, Pavlou S, Vayenas DV (2011) Single cell oil production from rice hulls hydrolysate. Bioresour Technol 102(20):9737–9742. https://doi.org/10.1016/j.biortech.2011.08.025
El-Baz HA, Elazzazy AM, Saleh TS, Dritsas P, Mahyoub JA, Baeshen MN, Madian HR, Alkhaled M, Aggelis G (2021) Single cell oil (SCO)–based bioactive compounds: I—enzymatic synthesis of fatty acid amides using SCOs as acyl group donors and their biological activities. Appl Biochem Biotechnol 193(3):822–845. https://doi.org/10.1007/s12010-020-03450-3
Elíades LA, Cabello MN, Pancotto V, Moretto A, Ferreri NA, Saparrat MC, Barrera MD (2019) Soil mycobiota under managed and unmanaged forests of Nothofagus pumilio in Tierra del Fuego, Argentina. N Z J For Sci 49. https://doi.org/10.33494/nzjfs492019x53x
Ellaiah P, Prabhakar T, Ramakrishna B, Taleb AT, Adinarayana K (2004) Production of lipase by immobilized cells of Aspergillus niger. Process Biochem 39(5):525–528. https://doi.org/10.1016/S0032-9592(01)00340-5
Fakas S, Papanikolaou S, Galiotou-Panayotou M, Komaitis M, Aggelis G (2009) Biochemistry and biotechnology of single cell oil. In Pandey A, Larroche C (eds) New horizons in biotechnology. Asiatech Publishers, pp 38–60
Folch J, Lees M, Stanley GS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1):497–509
Gardeli C, Athenaki M, Xenopoulos E, Mallouchos AKAA, Koutinas AA, Aggelis G, Papanikolaou S (2017) Lipid production and characterization by Mortierella (Umbelopsis) isabellina cultivated on lignocellulosic sugars. J Appl Microbiol 123(6):1461–1477. https://doi.org/10.1111/jam.13587
Gaspar ML, Cunningham M, Pollero R, Cabello M (1999) Occurrence and properties of an extracellular lipase in Mortierella vinacea. Mycologia 91(1):108–113. https://doi.org/10.1080/00275514.1999.12060997
Grantina-Ievina L, Berzina A, Nikolajeva V, Mekss P, Muiznieks I (2014) Production of fatty acids by Mortierella and Umbelopsis species isolated from temperate climate soils. Environ Exp Biol 12:15–27
Gujjala LKS, Kumar JSP, Talukdar B, Das A, Kumar S, Sherpa KCh, Banerjee R (2017) Biodiesel from oleaginous microbes: opportunities and challenges. Biofuels 10(1):45–59. https://doi.org/10.1080/17597269.2017.1402587
Hankin L, Anagnostakis SL (1975) The use of solid media for detection of enzyme production by fungi. Mycologia 67(3):597–607. https://doi.org/10.1080/00275514.1975.12019782
Hansson L, Dostalek (1988) Effect of culture conditions on mycelial growth and production of gamma-linolenic acid by the fungus Mortierella ramanniana. Appl Microbiol Biotechnol 28:240–246. https://doi.org/10.1007/BF00250448
Hasan F, Shah AA, Hameed A (2009) Methods for detection and characterization of lipases: a comprehensive review. Biotechnol Adv 27(6):782–798
Hassan N, Rafiq M, Hayat M, Shah AA, Hasan F (2016) Psychrophilic and psychrotrophic fungi: a comprehensive review. Rev Environ Sci Biotechnol 15(2):147–172. https://doi.org/10.1016/j.biotechadv.2009.06.001
Híreš M, Rapavá N, Šimkovič M, Varečka Ľ, Berkeš D, Kryštofová S (2018) Development and optimization of a high-throughput screening assay for rapid evaluation of lipstatin production by Streptomyces strains. Curr Microbiol 75(5):580–587. https://doi.org/10.1007/s00284-017-1420-x
Huang Q, An H, Song H, Mao H, Shen W, Dong J (2015) Diversity and biotransformative potential of endophytic fungi associated with the medicinal plant Kadsura angustifolia. Res Microbiol 166(1):45–55. https://doi.org/10.1016/j.resmic.2014.12.004
Hynes M (2010) Gluconeogenesis. In: Borkovich KA, Ebbole DJ (eds) Cellular and molecular biology of filamentous fungi. Washington, DC, ASM Press, pp 312–324. https://doi.org/10.1128/9781555816636.ch22
Iftikhar T, Niaz M, Jabeen R, Haq IU (2011) Purification and characterization of extracellular lipases. Pak J Bot 43(3):1541–1545
Kanmani P, Aravind J, Kumaresan K (2015) An insight into microbial lipases and their environmental facet. Int J Environ Sci Technol 12:1147–1162. https://doi.org/10.1007/s13762-014-0605-0
Kashmiri MA, Adnan A, Butt BW (2006) Production, purification and partial characterization of lipase from Trichoderma viride. Afr J Biotechnol 5(10):878–882. https://doi.org/10.4314/ajb.v5i10.42916
Kennedy MJ, Reader SL, Davies RJ (1993) Fatty acid production characteristics of fungi with particular emphasis on gamma linolenic acid production. Biotechnol Bioeng 42(5):625–634. https://doi.org/10.1002/bit.260420511
Keyhani NO (2018) Lipid biology in fungal stress and virulence: entomopathogenic fungi. Fungal Biol 122(6):420–429. https://doi.org/10.1016/j.funbio.2017.07.003
Khunyoshyeng S, Cheevadhanarak S, Rachdawong S, Tanticharoen M (2002) Differential expression of desaturases and changes in fatty acid composition during sporangiospore germination and development in Mucor rouxii. Fungal Genet Biol 37(1):13–21. https://doi.org/10.1016/S1087-1845(02)00028-2
Klempova T, Basil E, Kubatova A, Certik M (2013) Biosynthesis of gamma-linolenic acid and beta-carotene by Zygomycetes fungi. Biotechnol J 8(7):794–800. https://doi.org/10.1002/biot.201200099
Kosa G, Zimmermann B, Kohler A, Ekeberg D, Afseth NK, Mounier J, Shapaval V (2018) High-throughput screening of Mucoromycota fungi for production of low-and high-value lipids. Biotechnol Biofuels 11(1):1–17
Kotogán A, Németh B, Vágvölgyi C, Papp T, Takó M (2014) Screening for extracellular lipase enzymes with transesterification capacity in Mucoromycotina strains. Food Technol Biotechnol 52(1):73–82
Koutinas AA, Chatzifragkou A, Kopsahelis N, Papanikolaou S, Kookos IK (2014) Design and techno-economic evaluation of microbial oil production as a renewable resource for biodiesel and oleochemical production. Fuel 116:566–577. https://doi.org/10.1016/j.fuel.2013.08.045
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molec Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lee LP, Karbul HM, Citartan M, Gopinath SC, Lakshmipriya T, Tang TH (2015) Lipase-secreting Bacillus species in an oil-contaminated habitat: promising strains to alleviate oil pollution. Biomed Res Int. https://doi.org/10.1155/2015/820575
Lee JM, Lee H, Kang S, Park WJ (2016) Fatty acid desaturases, polyunsaturated fatty acid regulation, and biotechnological advances. Nutrients 8(1):23. https://doi.org/10.3390/nu8010023
Liu YY, Xu JH, Hu Y (2000) Enhancing effect of Tween-80 on lipase performance in enantioselective hydrolysis of ketoprofen ester. J Mol Catal B Enzym 10(5):523–529. https://doi.org/10.1016/S1381-1177(00)00093-X
Liu B, Zhao Z (2007) Biodiesel production by direct methanolysis of oleaginous microbial biomass. J Chem Technol Biotechnol. Int Res Process Environ Clean Technol 82(8):775–780. https://doi.org/10.1002/jctb.1744
Mahoney D, Gams W, Meyer W, Starink-Willemse M (2004) Umbelopsis dimorpha sp. nov., a link between U. vinacea and U. versiformis. Mycol Res 108(1):107–111. https://doi.org/10.1017/S0953756203008876
Martínez O, Valenzuela E (2003) Zygomycota citados para Chile. Boletín Micológico 18
Meyer W, Gams W (2003) Delimitation of Umbelopsis (Mucorales, Umbelopsidaceae fam. nov.) based on ITS sequence and RFLP data. Mycol Res 107(3):339–350. https://doi.org/10.1017/S0953756203007226
Mirza AQ, Akhtar MW, Nawazish MN, Chughtai MID (1982) Production of lipids and lipase activity during growth of Mucor hiemalis. Can J Microbiol 28(6):618–622. https://doi.org/10.1139/m82-092
Molina L, Rajchenberg M, de Errasti A, Aime MC, Pildain MB (2020) Sapwood-inhabiting mycobiota and Nothofagus tree mortality in Patagonia: diversity patterns according to tree species, plant compartment and health condition. For Ecol Manage 462:117997. https://doi.org/10.1016/j.foreco.2020.117997
Murphy D (1991) Storage lipid bodies in plants and other organisms. Prog Lipid Res 29:299–324
Naqvi SH, Dahot MU, Ali A, Khan Y, Rafiq M (2011) Production and characterization of extracellular lipase secreted by Mucor geophillus. Afr J Biotechnol 10(84):19589–19606. https://doi.org/10.5897/ajb11.216
Ncube I, Adlercreutz P, Read J, Mattiasson B (1993) Purification of rape (Brassica napus) seedling lipase and its use in organic media. Biotechnol Appl Biochem 17:327–336
Negi S (2019) Lipases: A promising tool for food industry. In: Parameswaran B, Varjani S, Raveendran S (eds) Green bio-processes. Energy, environment, and sustainability. Singapore, Springer. https://doi.org/10.1007/978-981-13-3263-0_10
Neto CP, Freire CS, Pinto PC, Santiago AS, Silvestre AJ, Evtuguin DV (2006) Comparative study of lipophilic extractives of hardwoods and corresponding ECF bleached kraft pulps. BioResources 1(1):3–17
Ochsenreither K, Glück C, Stressler T, Fischer L, Syldatk C (2016) Production strategies and applications of microbial single cell oils. Front Microbiol 7:1539. https://doi.org/10.3389/fmicb.2016.01539
Ogawa Y, Suda A, Kusama-Eguchi K, Watanabe K, Tokumasu S (2005) Intraspecific groups of Umbelopsis ramanniana inferred from nucleotide sequences of nuclear rDNA internal transcribed spacer regions and sporangiospore morphology. Mycoscience 46(6):343–351. https://doi.org/10.1007/s10267-005-0257-5
Ogawa Y, Sugiyama M, Hirose D, Kusama-Eguchi K, Tokumasu S (2011) Polyphyly of intraspecific groups of Umbelopsis ramanniana and their genetic and morphological variation. Mycoscience 52(2):91–98. https://doi.org/10.1007/S10267-010-0074-3
Panteghini M, Bonora R, Pagani F (2001) Measurement of pancreatic lipase activity in serum by a kinetic colorimetric assay using a new chromogenic substrate. Ann Clin Biochem 38(4):365–370. https://doi.org/10.1258/0004563011900876
Papanikolaou S, Komaitis M, Aggelis G (2004) Single cell oil (SCO) production by Mortierella isabellina grown on high-sugar content media. Bioresour Technol 95(3):287–291. https://doi.org/10.1016/j.biortech.2004.02.016
Papanikolaou S, Galiotou-Panayotou M, Fakas S, Komaitis M, Aggelis G (2007) Lipid production by oleaginous Mucorales cultivated on renewable carbon sources. Eur J Lipid Sci Technol 109(11):1060–1070. https://doi.org/10.1002/ejlt.200700169
Patel A, Arora N, Sartaj K, Pruthi V, Pruthi PA (2016) Sustainable biodiesel production from oleaginous yeasts utilizing hydrolysates of various non-edible lignocellulosic biomasses. Renew Sust Energ Rev 62:836–855. https://doi.org/10.1016/j.rser.2016.05.014
Plou FJ, Ferrer M, Nuero OM, Calvo MV, Alcalde M, Reyes F, Ballesteros A (1998) Analysis of Tween 80 as an esterase/lipase substrate for lipolytic activity assay. Biotechnol Tech 12(3):183–186. https://doi.org/10.1023/A:1008809105270
Posada D (2008) jModelTest: Phylogenetic model averaging. Mol Biol Evol 25:1253–1256. https://doi.org/10.1093/molbev/msn083
Qin D, Wang L, Han M, Wang J, Song H, Yan X, Duan X, Dong J (2018) Effects of an endophytic fungus Umbelopsis dimorpha on the secondary metabolites of host–plant Kadsura angustifolia. Front Microbiol 9:2845. https://doi.org/10.3389/fmicb.2018.02845
Ratledge C (2013) Microbial oils: an introductory overview of current status and future prospects. Ocl 20(6):D602. https://doi.org/10.1051/ocl/2013029
Rigo E, Polloni AE, Remonatto D, Arbter F, Menoncin S, Oliveira JV, de Olivera D, Treichel H, Kalil SJ, Ninow JL, Di Luccio M (2010) Esterification activity of novel fungal and yeast lipases. Appl Biochem Biotechnol 162(7):1881–1888
Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353. https://doi.org/10.1046/j.1469-8137.2001.00177.x
Romanya J, Fons J, Sauras-Yera T, Gutiérrez E, Vallejo VR (2005) Soil–plant relationships and tree distribution in old growth Nothofagus betuloides and Nothofagus pumilio forests of Tierra del Fuego. Geoderma 124(1–2):169–180. https://doi.org/10.1016/j.geoderma.2004.04.011
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Russell NJ (2008) Membrane components and cold sensing. In: Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, Heidelberg, pp 177–190. https://doi.org/10.1007/978-3-540-74335-4_11
Salameh MD, Wiegel J (2007) Lipases from extremophiles and potential for industrial applications. Adv Appl Microbiol 61:253–283. https://doi.org/10.1016/S0065-2164(06)61007-1
Shimizu S, Jareonkitmongkol S (1995) Mortierella species (Fungi): production of C 20 polyunsaturated fatty acids. In: Medicinal and Aromatic Plants VIII. Springer, Berlin, Heidelberg, pp 308–325
Silva WOB, Mitidieri S, Schrank A, Vainstein MH (2005) Production and extraction of an extracellular lipase from the entomopathogenic fungus Metarhizium anisopliae. Process Biochem 40(1):321–326. https://doi.org/10.1016/j.procbio.2004.01.005
Song Z, Liu G, Chen Z, Liu B, Liu X (2019) Preliminary study on fatty acid composition of Umbelopsis. J Fungal Res 17(1):35–42
Soteras F, Ibarra C, Geml J, Barrios-García MN, Domínguez LS, Nouhra ER (2017) Mycophagy by invasive wild boar (Sus scrofa) facilitates dispersal of native and introduced mycorrhizal fungi in Patagonia, Argentina. Fungal Ecol 26:51–58. https://doi.org/10.1016/j.funeco.2016.11.008
Stamatakis A (2014) RAxML 8: a tool for phylogeneticanalysis and post-analysis of large phylogenies. Bioinformatics. 101093/bioinformatics/btu033
Stark S, Hilli S, Willför S, Smeds AI, Reunanen M, Penttinen M, Hautajärvi R (2012) Composition of lipophilic compounds and carbohydrates in the accumulated plant litter and soil organic matter in boreal forests. Eur J Soil Sci 63(1):65–74. https://doi.org/10.1111/j.1365-2389.2011.01411.x
Stoytcheva M, Montero G, Zlatev R, Leon A, J., & Gochev, V. (2012) Analytical methods for lipases activity determination: a review. Curr Anal Chem 8(3):400–407. https://doi.org/10.2174/157341112801264879
Sukdeo N, Teen E, Rutherford PM, Massicotte HB, Egger KN (2019) Bacterial and fungal saprotrophs are strongly stimulated weeks to months after forest soil profile reconstruction. Pedobiologia 73:29–41. https://doi.org/10.1016/j.pedobi.2019.01.001
Takó M, Kotogán A, Németh B, Radulov I, NiþÎ LD, Tãrãu D, Dicu D, Tóth B, Papp T, Vágvölgyi C (2012) Extracellular lipase production of Zygomycetes fungi isolated from soil. Rev Agric Rural Dev 1(1):62–66
Treichel H, de Oliveira D, Mazutti MA, Di Luccio M, Oliveira JV (2010) A review on microbial lipases production. Food Bioprocess Technol 3(2):182–196. https://doi.org/10.1007/s11947-009-0202-2
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 72(8):4238–4246. https://doi.org/10.1128/jb.172.8.42384246.1990
Volford B, Varga M, Szekeres A, Kotogán A, Nagy G, Vágvölgyi C, Papp T, Takó M (2021) β-galactosidase-producing isolates in mucoromycota: screening, enzyme production, and applications for functional oligosaccharide synthesis. J Fungi 7(3):229. https://doi.org/10.3390/jof7030229
Vongsangnak W, Ruenwai R, Tang X, Hu X, Zhang H, Shen B, Song Y, Laoteng K (2013) Genome-scale analysis of the metabolic networks of oleaginous zygomycete fungi. Gene 521(1):180–190. https://doi.org/10.1016/j.gene.2013.03.012
Wagner L, Stielow B, Hoffman K, Petkovits T, Papp T, Vágvölgy C, de Hoog GS, Verkley G, Viogt K (2013) A comprehensive molecular phylogeny of the Mortierellales (Mortierellomycotina) based on nuclear ribosomal DNA. Persoonia: Mol Phylogeny Evol Fungi 30(1):77–93. https://doi.org/10.3767/003158513X666268
Walther G, Pawłowska J, Alastruey-Izquierdo A, Wrzosek M, Rodriguez-Tudela JL, Dolatabadi S, Chakrabarti A, De Hoog GS (2013) DNA barcoding in Mucorales: an inventory of biodiversity. Pers Mol Phylogeny Evol Fungi 30(1):11–47. https://doi.org/10.3767/003158513X665070
Wang D, Xu Y, Shan T (2008) Effects of oils and oil-related substrates on the synthetic activity of membrane-bound lipase from Rhizopus chinensis and optimization of the lipase fermentation media. Biochem Eng J 41(1):30–37. https://doi.org/10.1016/j.bej.2008.03.003
Wang J, Guo X, Li L, Qiu H, Zhang Z, Wang Y, Sun G (2018) Application of the fluorescent dye BODIPY in the study of lipid dynamics of the rice blast fungus Magnaporthe oryzae. Molecules 23(7):1594. https://doi.org/10.3390/molecules23071594
Wang YN, Liu XY, Zheng RY (2014) Umbelopsis changbaiensis sp. nov. from China and the typification of Mortierella vinacea. Mycol Prog 13(3):657–669. https://doi.org/10.1007/s11557-013-0948-9
Wang YN, Liu XY, Zheng RY (2015) Umbelopsis longicollis comb. nov. and the synonymy of U. roseonana and U. versiformis with U. nana. Mycologia 107(5):1023–1032. https://doi.org/10.3852/14-339
Wang L, Qin D, Zhang K, Huang Q, Liu S, Han MJ, Dong JY (2017) Metabolites from the co-culture of nigranoic acid and Umbelopsis dimorpha SWUKD3. 1410, an endophytic fungus from Kadsura angustifolia. Nat Prod Res 31(12):1414–1421. https://doi.org/10.1080/14786419.2016.1255891
Weinstein RN, Montiel PO, Johnstone K (2000) Influence of growth temperature on lipid and soluble carbohydrate synthesis by fungi isolated from fellfield soil in the maritime Antarctic. Mycologia 92(2):222–229. https://doi.org/10.1080/00275514.2000.12061148
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: a guide to methods and application. San Diego, CA, Academic Press Inc, pp 315–322
Zheng Y, Yu X, Zeng J, Chen S (2012) Feasibility of filamentous fungi for biofuel production using hydrolysate from dilute sulfuric acid pretreatment of wheat straw. Biotechnol Biofuels 5(1):1–10. https://doi.org/10.1186/1754-6834-5-50
Acknowledgements
We thank Sergio Javier Mijailovsky from the La Plata Biochemical Research Institute (INIBIOLP) for assistance with the total lipid and fatty acid analyses.
Funding
This research was partially financed by the National Agency for Scientific and Technological Promotion (ANPCyT) of the Ministry of Science, Technology and Productive Innovation through PICT 2018–3234 (to MBP) and PICT 2019–00207 (to MCNS) projects, the National Council of Research (CONICET projects PIP 11220200101167CO01 (to MBP) and PUE INFIVE and PIP 11220200100527CO (to MCNS) and UNLP (Argentina) through the R&D Project A344 (MCNS).
Author information
Authors and Affiliations
Contributions
Conceptualization: Mariano Damián Aquino, Mario Carlos Nazareno Saparrat, and Maria Belén Pildain; methodology: Mariano Damián Aquino, Mario Carlos Nazareno Saparrat, and Maria Belén Pildain; formal analysis and investigation: Mariano Damián Aquino, Mario Carlos Nazareno Saparrat, and Maria Belén Pildain; writing—original draft preparation: Mariano Damián Aquino; writing—review and editing: Mario Carlos Nazareno Saparrat, and Maria Belén Pildain; funding acquisition: Mario Carlos Nazareno Saparrat, and Maria Belén Pildain; resources: Mario Carlos Nazareno Saparrat, and Maria Belén Pildain; supervision: Mario Carlos Nazareno Saparrat, and Maria Belén Pildain.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
This article does not contain any studies with animals performed by any of the authors.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Section Editor: Martin Rühl
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
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Aquino, M.D., Saparrat, M.C.N. & Pildain, M.B. Umbelopsis (Mucoromycota) from Patagonia, Argentina: identification, phylogenetic analysis, and expression profiling of lipase activity and lipid accumulation in selected isolates. Mycol Progress 22, 18 (2023). https://doi.org/10.1007/s11557-023-01866-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11557-023-01866-9