Abstract
The marine environment supports vast habitats with prodigious biodiversity comprising the largest source of unique bioactive compounds biosynthesized by macro and microorganisms, including seaweeds and their associated fungi. In this context, the interest in studying and characterizing marine natural products has increased in the last years. Among these metabolites, lipids and their derivatives play an important role in the metabolism of marine organisms and are sources of substances with therapeutic properties and biotechnological purposes. In this research, it was investigated the lipid amount present in the algae species Ascoseira mirabilis, Adenocystis utricularis, Desmarestia anceps, Phaeurus antarcticus and in their associated endophytic fungi Aspergillus flavus, Penicillium echinulatum, Microascus croci and Penicillium purpurogenum, respectively. This study was achieved by gas chromatography–mass spectrometry, using a standard methodology to analyze all of the components present in the eight organisms. Fatty acids (FAs) and sterols are among the lipids of the highest concentration in the studied algae and fungi. In general, phytol and fucosterol were the most abundant metabolites in all seaweed, while in endophytic fungi, the FAs (palmitic, linoleic, oleic and stearic acid) and ergosterol appeared in major concentrations. This work contributes to new chemical information on the underexploited biodiversity of macroalgae and endophytic fungi belonging to the Antarctic Peninsula and, furthermore, to increase the possibilities for the discovery of bioactive substances and apply it on biotechnological approaches.
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References
Andrade PB, Barbosa M, Matos RP, Lopes G, Vinholes J, Mouga T, Valentão P (2013) Valuable compounds in macroalgae extracts. Food Chem 138:1819–1829. https://doi.org/10.1016/j.foodchem.2012.11.081
Andriamaharavo NR (2014) Retention data. NIST Mass Spectrometry Data Center, NIST Mass Spectrometry Data Center
Ariede MB, Candido TM, Jacome AM, Velasco MVR, de Carvalho JC, Baby AR (2017) Cosmetic attributes of algae—a review. Algal Res 25:483–487. https://doi.org/10.1016/j.algal.2017.05.019
Barot M, Kumar JIN, Kumar RN (2016) Bioactive compounds and antifungal activity of three different seaweed species Ulva lactuca, Sargassum tenerrimum and Laurencia obtusa collected from Okha Coast, Western India. J Coast Life Med 4:284–289. https://doi.org/10.12980/jclm.4.2016J5-185
Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2013) GenBank. Nucleic Acids Res 41:D36–D42. https://doi.org/10.1093/nar/gks1195
Biancarosa I, Belghit I, Bruckner CG, Liland NS, Waagbø R, Amlund H, Heesch S, Lock EJ (2018) Chemical characterization of 21 species of marine macroalgae common in Norwegian waters: benefits of and limitations to their potential use in food and feed. J Sci Food Agric 98:2035–2042. https://doi.org/10.1002/jsfa.8798
Birkemeier C, Kopka J (2007) Design of metabolite recovery by variations of the metabolite profiling protocol. In: Nikolau BJ, Wurtele ES (eds) Concepts in plant metabolomics. Springer, Dordrecht, pp 45–69. https://doi.org/10.1007/978-1-4020-5608-6_4
Blunt JM, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2017) Marine natural products. Nat Prod Rep 34:235–294. https://doi.org/10.1039/c6np00124f
Bouzidi N, Daghbouche Y, Hattab ME, Aliche Z, Culioli G, Piovetti L, Garrigues S, De la Guardia M (2008) Determination of total sterols in brown algae by Fourier transform infrared spectroscopy. Anal Chim Acta 616:185–189. https://doi.org/10.1016/j.aca.2008.04.028
Brooks CJW, Horning EC, Young JS (1968) Characterization of sterols by gas chromatography–mass spectrometry of the trimethylsilyl ethers. Lipids 3:391–402. https://doi.org/10.1007/BF02531277
Brooks CJW, Cole WJ, McIntyre HB, Smith AG (1980) Selective reactions in the analysis and characterization of steroids by gas chromatography–mass spectrometry. Lipids 15:745–755. https://doi.org/10.1007/BF02534028
Chintalapati S, Kiran MD, Shivaji S (2004) Role of membrane lipid fatty acids in cold adaptation. Cell Mol Biol 50:631–664
Dame ZT, Silima B, Gryzenhout M, Van Ree T (2015) Bioactive compounds from the endophytic fungus Fusarium proliferatum. Nat Prod Res 30:1301–1304. https://doi.org/10.1080/14786419.2015.1053089
Das M, Zuniga E, Ojima I (2009) Novel taxoid-based tumor-targeting drug conjugates. Chim Oggi 27:54–56
Dauner ALL, MacCormack WP, Hernández EA, Martins CC (2017) Sources and distribution of biomarkers in surficial sediments from a polar marine ecosystem (Potter Cove, King George Island, Antarctica). Polar Biol 40:2015–2015. https://doi.org/10.1007/s00300-017-2120-5
Debbab A, Aly AH, Lin WH, Proksch P (2011) Bioactive compounds from marine bacteria and fungi. Microb Biotechnol 3:544–563. https://doi.org/10.1111/j.1751-7915.2010.00179.x
Dey P, Banerjee J, Maiti MK (2011) Comparative lipid profiling of two endophytic fungal isolates—Colletotrichum sp. and Alternaria sp. having potential utilities as biodiesel feedstock. Bioresour Technol 102:5815–5823. https://doi.org/10.1016/j.biortech.2011.02.064
Duarte N, Ferreira MJ, Martins M, Viveiros M, Amaral L (2007) Antibacterial activity of ergosterol peroxide against Mycobacterium tuberculosis: dependence upon system and medium employed. Phytother Res 21:601–604. https://doi.org/10.1002/ptr.2119
Dufourc EJ (2008) Sterols and membrane dynamics. J Chem Biol 1:63–77. https://doi.org/10.1007/s12154-008-0010-6
Erbert C, Lopes AA, Yokoya NS, Furtado NAJC, Conti R, Pupo MT, Lopes JLC, Debonsi HM (2012) Antibacterial compound from the endophytic fungus Phomopsis longicolla isolated from the tropical red seaweed Bostrychia radicans. Bot Mar 55:435–440. https://doi.org/10.1515/bot-2011-0023
Fangkrathok N, Sripanidkulchai B, Umehara K, Noguchi H (2013) Bioactive ergostanoids and a new polyhydroxyoctane from Lentinus polychrous mycelia and their inhibitory effects on E2-enhanced cell proliferation of T47D cells. Nat Prod Res 27:1611–1619. https://doi.org/10.1080/14786419.2012.742079
Fariman GA, Shastan SJ, Zahedi MM (2016) Seasonal variation of total lipid, fatty acids, fucoxanthin content, and antioxidant properties of two tropical brown algae (Nizamuddinia zanardinii and Cystoseira indica) from Iran. J Appl Phycol 28:1323. https://doi.org/10.1007/s10811-015-0645-y
Fernando IPS, Nah JW, Jeon YJ (2016) Potential anti-inflammatory natural products from marine algae. Environ Toxicol Pharmacol 48:22–30. https://doi.org/10.1016/j.etap.2016.09.023
Ferreira I, Vaz J, Vasconcelos M, Martins A (2010) Compounds from wild mushrooms with antitumor potential. Anticancer Agents Med Chem 10:424–436. https://doi.org/10.2174/1871520611009050424
Field CJ, Schley PD (2004) Evidence for potential mechanisms for the effect of conjugated linoleic acid on tumor metabolism and immune function: lessons from n-3 fatty acids. Am J Clin Nutr 79:1190–1198. https://doi.org/10.1093/ajcn/79.6.1190S
Flewelling AJ, Currie J, Gray CA, Johnson JA (2015) Endophytes from marine macroalgae: promising sources of novel natural products. Curr Sci 109:88–111
Furbino LE, Godinho VM, Santiago IF, Pellizari FM, Alves TM, Zani CL, Junior PAS, Romanha AJ, Carvalho AGO, Gil LHVG, Rosa AC, Minnis AM, Rosa LH (2014) Diversity patterns, ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic Peninsula. Microb Ecol 67:775–787. https://doi.org/10.1007/s00248-014-0374-9
Furbino LE, Pellizzari FM, Neto PC, Rosa CA, Rosa LH (2017) Isolation of fungi associated with macroalgae from maritime Antarctica and their production of agarolytic and carrageenolytic activities. Polar Biol 41:527–535. https://doi.org/10.1007/s00300-017-2213-1
Fuwa H, Sasaki M (2016) Exploiting ruthenium carbene-catalyzed reactions in total synthesis of marine oxacyclic natural products. Bull Chem Soc Jpn 89:1403–1415. https://doi.org/10.1246/bcsj.20160224
Gambato G, Baroni EG, Garcia CSC, Frassini R, Frozza COS, Moura S, Pereira CMP, Fujii MT, Colepicolo P, Lambert APF, Henriques JAP, Roesch-Ely M (2014) Brown algae Himantothallus grandifolius (Desmarestiales, Phaeophyceae) suppresses proliferation and promotes apoptosis-mediated cell death in tumor cells. Adv Biol Chem 4:98–108
Graeve M, Dauby P, Scailteur Y (2001) Combined lipid, fatty acid and digestive tract content analyses: a penetrating approach to estimate feeding modes of Antarctic amphipods. Polar Biol 24:853–862. https://doi.org/10.1007/s003000100295
Graeve M, Kattner G, Wiencke C, Karsten U (2002) Fatty acid composition of Arctic and Antarctic macroalgae: indicator of phylogenetic and trophic relationships. Mar Ecol Prog Ser 231:67–74. https://doi.org/10.3354/meps231067
Gressler V, Yokoya NS, Fujii MT, Colepicolo P, Torres RP, Pinto E (2010) Lipid, fatty acid, protein, amino acid and ash contents in four Brazilian red algae species. Food Chem 120:585–590. https://doi.org/10.1002/btpr.575
Guedes AC, Amaro HM, Malcata FX (2011) Microalgae as sources of high added-value compounds—a brief review of recent work. Biotechnol Prog 27:597–613. https://doi.org/10.1002/btpr.575
Gupta R, Sharma AK, Dobhal MP, Sharma MC, Gupta RS (2011) Antidiabetic and antioxidant potential of β-sitosterol in streptozotocin-induced experimental hyperglycemia. J Diabetes 3:29–37. https://doi.org/10.1111/j.1753-0407.2010.00107.x
Huang CB, Ebersole JL (2010) A novel bioactivity of omega-3 polyunsaturated fatty acids and their ester derivatives. Mol Oral Microbiol 25:75–80. https://doi.org/10.1111/j.2041-1014.2009.00553.x
Isidorov VA, Szczepaniak L (2009) Gas chromatographic retention indices of biologically and environmentally important organic compounds on capillary columns with low-polar stationary phases. J Chromatogr A 1216:8998–9007. https://doi.org/10.1016/j.chroma.2009.10.079
Jonsson P, Johansson AI, Gullberg J, Trygg J, Jiye A, Grung B, Marklund S, Sjöström M, Antti H, Moritz T (2005) High-throughput data analysis for detecting and identifying differences between samples in GC/MS-based metabolomic analyses. Anal Chem 77:5635–5642. https://doi.org/10.1021/ac050601e
Kamenarska Z, Gasic MJ, Zlatovic M, Rasovic A, Sladic D, Kljajic Z, Stefanov K, Seizova K, Najdenski H, Kujumgiev A, Tsvetkova I, Popov S (2002) Chemical composition of the brown Alga Padina pavonia (L.) Gaill from the Adriatic Sea. Bot Mar 45:339–345. https://doi.org/10.1515/BOT.2002.034
Kamenarska Z, Stefanov K, Stancheva R, Dimitrova-Konaklieva S, Popov S (2006) Comparative investigation on sterols some Black Sea red algae. Nat Prod Res 20:113–118. https://doi.org/10.1080/14786410500045051
Kjer J, Debbab A, Aly AH, Proksch P (2010) Methods for isolation of marine-derived endophytic fungi and their bioactive secondary products. Nat Protoc 5:479–490. https://doi.org/10.1038/nprot.2009.233
Kumari P, Kumar M, Reddy CRK, Jha B (2013a) Algal lipids, fatty acids and sterols. In: Domínguez H (ed) Functional ingredients from algae for foods and nutraceuticals, 1st edn. Woodhead Publishing, Cambridge, pp 87–134
Kumari P, Bijo AJ, Mantri VA, Reddy CRK, Jha B (2013b) Fatty acid profiling of tropical marine macroalgae: an analysis from chemotaxonomic and nutritional perspectives. Phytochemistry 86:44–56. https://doi.org/10.1016/j.phytochem.2012.10.015
Lee YS, Shin KH, Kim BK, Lee S (2004) Anti-diabetic activities of fucosterol from Pelvetia siliquosa. Arch Pharmacal Res 27:1120–1122. https://doi.org/10.1007/BF02975115
Lopes G, Sousa C, Bernardo J, Andrade PB, Valentão P (2011) Sterol profiles in 18 macroalgae of the Portuguese Coast. J Phycol 47:1210–1218. https://doi.org/10.1111/j.1529-8817.2011.01028.x
Lopes G, Sousa C, Valentão P, Andrade PB (2013) Sterols in algae and health. In: Hernández-Ledesma B, Herrero M (eds) Bioactive compounds from marine foods: plant and animal sources. Wiley, Chichester, pp 173–187. https://doi.org/10.1002/9781118412893.ch9
Loque CP, Medeiros AQ, Pellizzari FM, Oliveira EC, Rosa CA, Rosa LH (2010) Fungal community associated with marine macroalgae from Antarctica. Polar Biol 33:641–648. https://doi.org/10.1007/s00300-009-0740-0
Lytovchenko A, Beleggia R, Schauer N, Isaacson T, Leuendorf JE, Hellmann H, Rose JKC, Fernie AR (2009) Application of GC–MS for the detection of lipophilic compounds in diverse plant tissues. Plant Methods 5:1–11. https://doi.org/10.1186/1746-4811-5-4
Maciel OMC, Tavares RSN, Caluz DRE, Gaspar LR, Debonsi HM (2018) Photoprotective potential of metabolites isolated from algae-associated fungi Annulohypoxylon stygium. J Photochem Photobiol B 178:316–322. https://doi.org/10.1016/j.jphotobiol.2017.11.018
Madeiros R, Otuki MF, Avellar MC, Calixto JB (2007) Mechanisms underlying the inhibitory actions of the pentacyclic triterpene-amyrin in the mouse skin inflammation induced by phorbol ester 12-otetradecanoylphorbol-13-acetate. Eur J Pharmacol 55:227–235. https://doi.org/10.1016/j.ejphar.2006.12.005
Marella ER, Holkenbrink C, Siewers V, Borodina I (2017) Engineering microbial fatty acid metabolism for biofuels and biochemical. Curr Opin Biotechnol 50:39–46. https://doi.org/10.1016/j.copbio.2017.10.002
Melo IS, Santos SN, Rosa LH, Parma MM, Silva LJ, Queiroz SCN, Pellizari VH (2014) Isolation and biological activities of an endophytic Mortierella alpina strain from the Antarctic moss Schistidium antarctici. Extremophiles 18:15–23. https://doi.org/10.1007/s00792-013-0588-7
Mourente G, Bell JG, Tocher DR (2007) Does dietary tocopherol level affect fatty acid metabolism in fish? Fish Physiol Biochem 33:269–280. https://doi.org/10.1007/s10695-007-9139-4
Mozaffarian D, Wu JH (2011) Omega-3 fatty acids and cardiovascular disease effects on risk factors, molecular pathways and clinical events. J Am Coll Cardiol 58:2047–2067. https://doi.org/10.1016/j.jacc.2011.06.063
Muñoz PA, Flores PA, Boehmwald F, Blamey JM (2011) Thermophilic bacteria present in a sample from Fumarole Bay, Deception Island. Antarct Sci 23:549–555. https://doi.org/10.1017/S0954102011000393
Nadaf M, Halimi M, Mortazavi M (2012) Identification of nonpolar chemical composition Spartium junceum flower growing in Iran by GC–MS. Middle East J Sci Res 11:221–224
Nicoletti R, Trincone A (2016) Bioactive compounds produced by strains of Penicillium and Talaromyces of marine origin. Mar Drugs 14:1–37. https://doi.org/10.3390/md14020037
Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541–568. https://doi.org/10.1146/annurev.arplant.47.1.541
NIST Library/standard non-polar and semi-standard non-polar. https://www.nist.gov/srd/nist1a.cfm. Accessed 5 March 2018
Nogala-Kałucka ME (2003) Fat-soluble vitamins. In: Sikorski ZE, Kołakowska A (eds) Chemical and functional properties of food lipids, 1st edn. CRC Press, New York, pp 109–128
Nomura M, Kamogawa H, Susanto E, Kawagoe C, Yasui H, Saga N, Hosokawa M, Miyashita K (2013) Seasonal variations of total lipids, fatty acid composition, and fucoxanthin contents of Sargassum horneri (Turner) and Cystoseira hakodatensis (Yendo) from the northern seashore of Japan. J Appl Phycol 25:1159–1169. https://doi.org/10.1007/s10811-012-9934-x
Ogaki MB, de Paula MT, Ruas D, Pellizzari FM, García-Laviña CX, Rosa LH (2019) Marine fungi associated with Antarctic macroalgae. In: Castro-Sowinski S (ed) The ecological role of micro-organisms in the Antarctic environment. Springer Polar Science. pp 239–255. https://doi.org/10.1007/978-3-030-02786-5_11
Okoye NN, Ajaghaku DL, Okeke HN, Ilodigwe EE, Nworu CS, Okoye FBC (2014) Beta-Amyrin and alpha-amyrin acetate isolated from the stem bark of Alstonia boonei display profound anti-inflammatory activity. Pharm Biol 52:1478–1486. https://doi.org/10.3109/13880209.2014.898078
Otuki C, Ferreira J, Lima F, Meyre-Silva C, Malheiros A, Muller L, Cani G, Santos A, Yunes R, Calixto J (2005) Antinociceptive properties of a mixture of α-amyrin and β-amyrin triterpenes: evidence for participation of protein kinase C and protein kinase A pathways. J Pharmacol Exp Ther 31:310–318. https://doi.org/10.1124/jpet.104.071779
Payghami N, Jamili S, Rustaiyan A, Saeidnia S, Nikan M, Gohari AR (2015) Alpha-amylase inhibitory activity and sterol composition of the marine algae, Sargassum glaucescens. Pharmacogn Res 7:314–321. https://doi.org/10.4103/0974-8490.167893
Pedraza RO, Torres-Díaz C, Lavin P, Retamales-Molina P, Atala C, Acuna-Rodríguez I, Molina-Montenegro MA (2018) Root fungal endophytes improve the growth of Antarctic plants through an enhanced nitrogen acquisition. PeerJ 6:e26774v1. https://doi.org/10.7287/peerj.preprints.26774v1
Pereira H, Barreira L, Figueiredo F, Custódio L, Vizetto-Duarte C, Polo C, Resek E, Engelen A, Varela J (2012) Polyunsaturated fatty acids of marine macroalgae: potential for nutritional and pharmaceutical applications. Mar Drugs 10:1920–1935. https://doi.org/10.3390/md10091920
Pereira DM, Correia-da-Silva G, Valentão P, Teixeira N, Andrade PB (2014) Anti-inflammatory effect of unsaturated fatty acids and ergosta-7,22-dien-3-ol from Marthasterias glacialis: prevention of CHOP-mediated ER-stress and NF-κB activation. PLoS ONE 9:e88341. https://doi.org/10.1371/journal.pone.0088341
Pereira CMP, Nunes CFP, Zambotti-Villela L, Streit NM, Dias D, Pinto E, Gomes CB, Colepicolo P (2017) Extraction of sterols in brown macroalgae from Antarctica and their identification by liquid chromatography coupled with tandem mass spectrometry. J Appl Phycol 29:751–757. https://doi.org/10.1007/s10811-016-0905-5
Perez MJ, Falqué E, Domínguez H (2016) Antimicrobial action of compounds from marine seaweed. Mar Drugs 14:1–52. https://doi.org/10.3390/md14030052
Plaza M, Herrero M, Cifuentes A, Ibáñez E (2009) Innovative natural functional ingredients from microalgae. J Agric Food Chem 57:7159–7170. https://doi.org/10.1021/jf901070g
Pora B, Qian Y, Caulier B, Comini S, Looten P, Segueilha L (2014) Method for the preparation and extraction of squalene from microalgae. 14/118, 641. United States Patent Application 20140088201
Rabelo VW, Romeiro NC, Abreu PA (2017) Design strategies of oxidosqualene cyclase inhibitors: targeting the sterol biosynthetic pathway. J Steroid Biochem Mol Biol 171:305–317. https://doi.org/10.1016/j.jsbmb.2017.05.002
Radulovic NS, Dordevic N (2011) Steroids from poison hemlock (Conium maculatum L.): a GC–MS analysis. J Serb Chem Soc 76:1471–1483. https://doi.org/10.2298/JSC110206128R
Recio MC, Giner RM, Manez S, Rios JL (1995) Structural requirements for the anti-inflammatory activity of natural triterpenoids. Planta Med 61:181–185. https://doi.org/10.1055/s-2006-958045
Rees-Owen RL, Gill FL, Newron RJ, Ivanovic RF, Francis JE, Riding JB, Vane CH, dos Santos RAL (2018) The last forests on Antarctica: reconstructing flora and temperature from the Neogene Sirius Group, Transantarctic Mountains. Org Geochem 118:4–14. https://doi.org/10.1016/j.orggeochem.2018.01.001
Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. N Phytol 151:341–353. https://doi.org/10.1046/j.1469-8137.2001.00177.x
Ruess L, Haggablom MM, Zapata G, Dighton J (2002) Fatty acids of fungi and nematodes—possible biomarkers in the soil food chain? Soil Biol Biochem 34:745–756. https://doi.org/10.1016/S0038-0717(01)00231-0
Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Rev Environ Sci Biol 6:127–141. https://doi.org/10.1007/s11157-006-9107-y
Saeidnia S, Manayi A, Gohari AR, Abdollahi M (2014) The story of beta-sitosterol—a review. Eur J Med Plants 4:590–609. https://doi.org/10.9734/EJMP/2014/7764
Santos FA, Frota JT, Arruda BR, Melo TS, Silva AACA, Brito GAC, Chaves MH, Rao VS (2012) Antihyperglycemic and hypolipidemic effects of α, β-amyrin, a triterpenoid mixture from Protium heptaphyllum in mice. Lipids Health Dis 11:98. https://doi.org/10.1186/1476-511X-11-98
Santos SAO, Oliveira CSD, Trindade SS, Abreu MH, Rocha SSM, Silvestre AJD (2016) Bioprospecting for lipophilic-like components of five Phaeophyta macroalgae from the Portuguese Coast. J Appl Phycol 28:3151–3158. https://doi.org/10.1007/s10811-016-0855-y
Santos-Fa FC, Fill TP, Nakamura J, Monteiro MR, Rodrigues-Fo E (2011) Endophytic fungi as a source of biofuel precursors. J Microbiol Biotechnol 21:728–733. https://doi.org/10.4014/jmb.1010.10052
Sarasan M, Puthumana J, Job N, Han J, Lee J, Philip R (2017) Marine algicolous endophytic fungi—a promising drug resource of he era. J Microbiol Biotechnol 27:1039–1052. https://doi.org/10.4014/jmb.1701.01036
Schmid M, Kraft LGK, van der Loos LM, Kraft GT, Virtue P, Nichols PD, Hurd CL (2018) Southern Australian seaweeds: a promising resource for omega-3 fatty acids. Food Chem 265:70–77. https://doi.org/10.1016/j.foodchem.2018.05.060
Schmitz G, Ecker J (2008) The opposing effects of n-3 and n-6 fatty acids. Prog Lipid Res 47:147–155. https://doi.org/10.1016/j.plipres.2007.12.004
Sheeja L, Lakshmi D, Shruthi B, Sajidha P (2016) Anticancer activity of phytol purified from Gracilaria edulis against human breast cancer cell line (MCF-7). Int J Curr Sci 19:36–46
Silva DB, Pott A, Oliveira DCR (2010) Analyses of the headspace volatile constituents of aerial parts (leaves and stems), flowers and fruits of Bidens gardneri Bak. and Bidens sulphurea (Cav.) Sch. Bip. using solid-phase microextraction. J Essent Oil Res 22:560–563. https://doi.org/10.1080/10412905.2010.9700400
Simões JC, Arigony Neto J, Bremer UF (2004) O uso de mapas antárticos em publicações. Pesq Antart Bras 4:191–197
Singh R, Parihar P, Singh M, Bajguz A, Kumar J, Singh S, Singh VP, Prasad SM (2017) Uncovering potential applications of cyanobacteria and algal metabolites in biology, agriculture and medicine: current status and future prospect. Front Microbiol 8:1–37. https://doi.org/10.3389/fmicb.2017.00515
Soldi C, Pizzolatti G, Luiz A, Marcon R, Meotti F, Miotob L, Santos A (2008) Synthetic derivatives of the α- and β-amyrin triterpenes and their antinociceptive properties. Bioorg Med Chem 16:3377–3386. https://doi.org/10.1016/j.bmc.2007.12.008
Souza W, Rodrigues JC (2009) Sterol biosynthesis pathway as target for anti trypanosomatid drugs. Interdiscip Perspect Infect Dis 2009:1–19. https://doi.org/10.1155/2009/642502
Suryanarayanan TS (2012) Fungal endosymbionts of seaweeds. In: Raghukumar C (ed) Biology of marine fungi. Springer, Berlin, pp 53–69. https://doi.org/10.1007/978-3-642-23342-5_3
Syad AN, Rajamohamed BS, Shunmugaiah KP, Kasi PD (2016) Neuroprotective effect of the marine macroalga Gelidiella acerosa: identification of active compounds through bioactivity-guided fractionation. Pharm Biol 54:2073–2081. https://doi.org/10.3109/13880209.2016.1145700
Torres S, Cajas D, Palfner G, Astuya A, Aballay A, Pérez C, Hernández V, Becerra J (2016) Steroidal composition and cytotoxic activity from fruiting body of Cortinarius xiphidipus. Nat Prod Res 31:473–476. https://doi.org/10.1080/14786419.2016.1185717
Tret’yakov KV (2007) Retention data. NIST Mass Spectrometry Data Center, NIST Mass Spectrometry Data Center
Tuberoso CIG, Barra A, Angioni A, Sarritzu E, Pirisi FM (2006) Chemical composition of volatiles in sardinian Myrtle (Myrtus communis L.) alcoholic extracts and essential oils. J Agric Food Chem 54:1420–1426. https://doi.org/10.1021/jf052425g
Tunlid A, White DC (1992) Biochemical analysis of biomass, community structure, nutritional status, and metabolic activity of microbial communities in soil. In: Stotzky G, Bollag JM (eds) Soil biochemistry, 7th edn. Marcel Dekker, New York, pp 229–262
Weete JD, Abril M, Blackwell M (2010) Phylogenetic distribution of fungal sterols. PLoS ONE 5:10899. https://doi.org/10.1371/journal.pone.0010899
White TJ, Bruns TD, Lee SB, Taylor JW (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 applications. Academic, London, pp 315–322
Yan BA, Wang G, Lu H, Huang X, Liu Y, Zha W, Hao H, Zhang Y, Liu L, Gu S, Huang Q, Zheng Y, Sun J (2009) Metabolomic investigation into variation of endogenous metabolites in professional athletes subject to strength-endurance training. J Appl Physiol 106:531–538. https://doi.org/10.1152/japplphysiol.90816.2008
Zhao Y, Xie R, Chao X, Zhang Y, Lin R, Sun W (2009) Bioactivity directed isolation, identification of diuretic compounds from Polyporus umbellatus. J Ethnopharmacol 126:184–187. https://doi.org/10.1016/j.jep.2009.07.033
Zheng Y, White E (2008) Retention data. NIST Mass Spectrometry Data Center, NIST Mass Spectrometry Data Center
Zuccaro A., Mitchell JI (2005) Fungal communities of seaweeds. In: Dighton J, White Jr JF, Oudemans P (eds) The fungal community, 3rd edn. CRC Press, New York, pp 533–579. https://doi.org/10.1201/9781420027891.ch27
Acknowledgements
This study had financial and logistic support from the Brazilian Antarctic Program (PROANTAR/MCT/CNPq N° 64/2013) and Brazilian Marine Force. The authors are grateful for the financial and Fellowship Support from the Brazilian research funding agencies Coordination of Improvement of Higher Level Personnel (CAPES), National Council for Scientific and Technological Development (CNPq), National Institute of Science and Technology (INCT: BioNat), Grant # 465637/2014–0, and the State of São Paulo Research Foundation (FAPESP), Grant # 2014/50926–0. The authors are thankful to Renata S. N. Tavares for collection of algae in the Mission XXXIV/2015 and Ludmila Tonani by the support in the identification of fungi. We thank Professor Dr. Norberto Peporine Lopes (School of Pharmaceutical Sciences of Ribeirão Preto-USP) for providing available equipment.
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Teixeira, T.R., Santos, G.S., Turatti, I.C.C. et al. Characterization of the lipid profile of Antarctic brown seaweeds and their endophytic fungi by gas chromatography–mass spectrometry (GC–MS). Polar Biol 42, 1431–1444 (2019). https://doi.org/10.1007/s00300-019-02529-w
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DOI: https://doi.org/10.1007/s00300-019-02529-w