Unravelling the Lipids Content and the Fatty Acid Profiles of Eight Recently Described Halophytophthora Species and H. avicennae from the South Coast of Portugal
Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
UIDB/04326/2020
Fundação para a Ciência e Tecnologia
UIDP/04326/2020
Fundação para a Ciência e Tecnologia
LA/P/0101/2020
Fundação para a Ciência e Tecnologia
SFRH/BD/136277/2018
Fundação para a Ciência e Tecnologia
CEECIND/00425/2017
Fundação para a Ciência e Tecnologia
CZ.02.1.01/0.0/0.0/15_003/0000453
Czech Ministry for Education, Youth and Sports and the European Regional Development Fund
PubMed
37103366
PubMed Central
PMC10145237
DOI
10.3390/md21040227
PII: md21040227
Knihovny.cz E-resources
- Keywords
- FAMEs, lipids, marine biotechnology, marine oomycetes,
- MeSH
- Phylogeny MeSH
- Oleic Acid * MeSH
- Palmitic Acid MeSH
- Fatty Acids * MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Portugal MeSH
- Names of Substances
- Oleic Acid * MeSH
- Palmitic Acid MeSH
- Fatty Acids * MeSH
In this study, mycelia of eight recently described species of Halophytophthora and H. avicennae collected in Southern Portugal were analysed for lipids and fatty acids (FA) content to evaluate their possible use as alternative sources of FAs and understand how each species FAs profile relates to their phylogenetic position. All species had a low lipid percentage (0.06% in H. avicennae to 0.28% in H. frigida). Subclade 6b species contained more lipids. All species produced monounsaturated (MUFA), polyunsaturated (PUFA) and saturated (SFA) FAs, the latter being most abundant in all species. H. avicennae had the highest FA variety and was the only producer of γ-linolenic acid, while H. brevisporangia produced the lowest number of FAs. The best producer of arachidonic acid (ARA) and eicosapentaenoic acid (EPA) was H. thermoambigua with 3.89% and 9.09% of total FAs, respectively. In all species, palmitic acid (SFA) was most abundant and among the MUFAs produced oleic acid had the highest relative percentage. Principal component analysis (PCA) showed partial segregation of species by phylogenetic clade and subclade based on their FA profile. H. avicennae (Clade 4) differed from all other Clade 6 species due to the production of γ-linolenic and lauric acids. Our results disclosed interesting FA profiles in the tested species, adequate for energy (biodiesel), pharmaceutical and food industries (bioactive FAs). Despite the low amounts of lipids produced, this can be boosted by manipulating culture growth conditions. The observed interspecific variations in FA production provide preliminary insights into an evolutionary background of its production.
Centre of Marine Sciences University of Algarve 8005 139 Faro Portugal
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Fell J.W., Master I.M. Phycomycetes (Phytophthora spp. nov. and Pythium sp. nov.) associated with degrading mangrove (Rhizophora mangle) leaves. Canad. J. Bot. 1975;53:2908–2922. doi: 10.1139/b75-320. DOI
Gerrettson-Cornell L., Simpson J. Three new marine Phytophthora species from New South Wales. Mycotaxon. 1984;19:453–470.
Nakagiri A., Ito T., Manoch L., Tanticharoen M. A new Halophytophthora species, H. porrigovesica, from subtropical and tropical mangroves. Mycoscience. 2001;42:33. doi: 10.1007/BF02463973. DOI
Anastasiou C.J., Churchland L.M. Churchland LM Fungi on decaying leaves in marine habitats. Canad. J. Bot. 1969;47:251–257. doi: 10.1139/b69-035. DOI
Nigrelli L., Thines M. Tropical oomycetes in the German Bight—Climate warming or overlooked diversity? Fungal Ecol. 2013;6:152–160. doi: 10.1016/j.funeco.2012.11.003. DOI
Man in’t Veld W.A., Rosendahl K.C.H.M., van Rijswick P.C.J., Meffert J.P., Boer E., Westenberg M., van der Heide T., Govers L.L. Multiple Halophytophthora spp. and Phytophthora spp. including P. gemini, P. inundata and P. chesapeakensis sp. nov. isolated from the seagrass Zostera marina in the Northern hemisphere. Eur. J. Plant Pathol. 2018;153:341–357. doi: 10.1007/s10658-018-1561-1. DOI
Yang X., Hong C. Halophytophthora fluviatilis sp. nov. from freshwater in Virginia. FEMS Microbiol. Lett. 2014;352:230–237. doi: 10.1111/1574-6968.12391. PubMed DOI
Caballol M., Štraus D., Macia H., Ramis X., Redondo M.Á., Oliva J. Halophytophthora fluviatilis Pathogenicity and Distribution along a Mediterranean-Subalpine Gradient. J. Fungi. 2021;7:112. doi: 10.3390/jof7020112. PubMed DOI PMC
Nakagiri A. Ecology and biodiversity of Halophytophthora species. Fungal Divers. 2000;5:153–164.
Govers L.L., van der Zee E.M., Meffert J.P., van Rijswick P.C.J., Man in’t Veld W.A., Heusinkveld J.H.T., van der Heide T. Copper treatment during storage reduces Phytophthora and Halophytophthora infection of Zostera marina seeds used for restoration. Sci. Rep. 2017;7:43172. doi: 10.1038/srep43172. PubMed DOI PMC
Ho H.H., Jong S.C. Halophytophthora, gen. nov., a new member of the family Pythiaceae. Mycotaxon. 1990;36:377–382.
Thines M. Phylogeny and evolution of plant pathogenic oomycetes—A global overview. Eur. J. Plant Pathol. 2014;38:431–447. doi: 10.1007/s10658-013-0366-5. DOI
Li G.J., Hyde K.D., Zhao R.L., Hongsanan S., Abdel-Aziz F.A., Abdel-Wahab M.A., Alvarado P., Alves-Silva G., Ammirati J.F., Ariyawansa H.A., et al. Fungal diversity notes 253–366: Taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. 2016;78:1–237. doi: 10.1007/s13225-016-0366-9. DOI
Bennett R.M., Cock A.W.A.M., Lévesque A., Thines M. Calycofera gen. nov., an estuarine sister taxon to Phytopythium, Peronosporaceae. Mycol. Prog. 2017;16:947–954. doi: 10.1007/s11557-017-1326-9. DOI
Bennet R.M., Thines M. Revisiting Salisapiliaceae. Fungal Syst. Evol. 2019;3:171–184. doi: 10.3114/fuse.2019.03.10. PubMed DOI PMC
Jesus A.L., Marano A.V., Gonçalves D.R., Jerônimo G.H., Pires-Zotarelli C.L.A. Two new species of Halophytophthora from Brazil. Mycol. Prog. 2019;18:1411–1421. doi: 10.1007/s11557-019-01523-0. DOI
Su C.J., Hsieh S.Y., Chiang M.W.L., Pang K.L. Salinity, pH and temperature growth ranges of Halophytophthora isolates suggest their physiological adaptations to mangrove environments. Mycology. 2020;11:256–262. doi: 10.1080/21501203.2020.1714768. PubMed DOI PMC
Maia C., Horta Jung M., Carella G., Milenković I., Janoušek J., Tomšovský M., Mosca S., Schena L., Cravador A., Moricca S., et al. Eight new Halophytophthora species from marine and brackish-water ecosystems in Portugal and an updated phylogeny for the genus. Persoonia. 2022;48:54–90. doi: 10.3767/persoonia.2022.48.02. PubMed DOI PMC
Wang Q., Sen B., Liu X., He Y., Xie Y., Wang G. Enhanced saturated fatty acids accumulation in cultures of newly-isolated strains of Schizochytrium sp. and Thraustochytriidae sp. for large-scale biodiesel production. Sci. Total Environ. 2018;631–632:994–1004. doi: 10.1016/j.scitotenv.2018.03.078. PubMed DOI
Acheampong M., Ertemb F.C., Kappler B., Neubauer P. In pursuit of Sustainable Development Goal (SDG) number 7: Will biofuels be reliable? Renew. Sustain. Energ. Rev. 2017;75:927–937. doi: 10.1016/j.rser.2016.11.074. DOI
Abedi E., Sahari M.A. Long-chain polyunsaturated fatty acid sources and evaluation of their nutritional and functional properties. Food Sci. Nutr. 2014;2:443–463. doi: 10.1002/fsn3.121. PubMed DOI PMC
Adarme-Vega T.C., Thomas-Hall S.R., Schenk P.M. Towards sustainable sources for omega-3 fattu acids production. Curr. Opin. Biotechnol. 2014;26:14–18. doi: 10.1016/j.copbio.2013.08.003. PubMed DOI
Tallima H., Ridi R.E. Arachidonic acid: Physiological roles and potential health benefits—A review. J. Adv. Res. 2018;11:33–41. doi: 10.1016/j.jare.2017.11.004. PubMed DOI PMC
Spencer L., Mann C., Metcalfe M., Webb M., Pollard C., Spencer D., Berry D., Steward W., Dennison A. The effect of omega-3 FAs on tumour angiogenesis and their therapeutic potential. Eur. J. Cancer. 2009;45:2077–2086. doi: 10.1016/j.ejca.2009.04.026. PubMed DOI
Horrocks L.A., Yeo Y.K. Health benefits of docosahexaenoic acid (DHA) Pharmacol. Res. 1999;40:211–225. doi: 10.1006/phrs.1999.0495. PubMed DOI
Adarme-Vega T.C., Lim K.Y.D., Timmins M., Vernen F., Li Y., Schenk P.M. Microalgal biofactories: A promising approach towards sustainable omega-3 fatty acid production. Microb. Cell Factories. 2012;11:96. doi: 10.1186/1475-2859-11-96. PubMed DOI PMC
Kobayashi T., Sakaguchi K., Matsuda T., Abe E., Hama Y., Hayashi M., Honda D., Okita Y., Sugimoto S., Okino N., et al. Increase of eicosapentaenoic acid in thraustochytrids through thraustochytrid ubiquitin promoter-driven expression of a fatty acid Δ5 desaturase gene. Appl. Environ. Microbiol. 2011;77:3870–3876. doi: 10.1128/AEM.02664-10. PubMed DOI PMC
Marchan L.F., Chang K.J.L., Nichols P.D., Mitchell W.J., Polglase J.L., Gutierrez T. Taxonomy, ecology and biotechnological applications of thraustochytrids: A review. Biotechnol. Adv. 2018;36:26–46. doi: 10.1016/j.biotechadv.2017.09.003. PubMed DOI
Stredansky M., Conti E., Salaris A. Production of polyunsaturated fatty acids by Pythium ultimum in solid-state cultivation. Enzyme Microb. Technol. 2000;26:304–307. doi: 10.1016/S0141-0229(99)00146-5. PubMed DOI
Duan C.H., Riley M.B., Jeffers S.N. Effects of growth medium, incubation temperature, and mycelium age on production of five major fatty acids by six species of Phytophthora. Arch. Phytopathol Plant Prot. 2011;44:142–157. doi: 10.1080/03235400902952145. DOI
Pang K.L., Lin H.J., Lin H.Y., Huang Y.F., Chen Y.M. Production of arachidonic and eicosapentaenoic acids by the marine oomycete Halophytophthora. Mar. Biotechnol. 2015;17:121–129. doi: 10.1007/s10126-014-9600-1. PubMed DOI
Say E.K.P., Yabut A.T.V., Cinco N.E.T., Caguimbal N.A.L.E., Devadanera M.K.P., Bennett R.M., Arafiles K.H.V., Aki T., Dedeles G.R. Growth and fatty acid production of Halophytophthora S13005YL1-1.3 under different salinity and pH levels. Philipp. Agric. Sci. 2017;100:6–11.
Caguimbal N.A.L.E., Devadanera M.K.P., Bennett R.M., Arafiles K.H.V., Watanabe K., Aki T., Dedeles G.R. Growth and fatty acid profiles of Halophytophthora vesicula and Salispina spinosa from Philippine mangrove leaves. Lett. Appl. Microbiol. 2019;69:221–228. doi: 10.1111/lam.13199. PubMed DOI
Devanadera M.K.P., Bennett R.M., Watanabe K., Santiago M.R., Ramos M.C., Aki T., Dedeles G.R. Marine Oomycetes (Halophytophthora and Salispina): A potential source of fatty acids with cytotoxic activity against breast adenocarcinoma cells (MCF7) J. Oleo Sci. 2019;68:1163–1174. doi: 10.5650/jos.ess19033. PubMed DOI
Su C.J., Ju W.T., Chen Y.M., Chiang M.W.L., Hsieh S.Y., Lin H.J., Gareth Jones E., Pang K.L. Palmitic acid and long-chain polyunsaturated fatty acids dominate in mycelia of mangrove Halophytophthora and Salispina species in Taiwan. Botanica Marina. 2021;64:503–518. doi: 10.1515/bot-2021-0030. DOI
Bartnicki-Garcia S. Chemistry of hyphal walls of Phytophthora. J. Gen. Microbiol. 1966;42:57–69. doi: 10.1099/00221287-42-1-57. PubMed DOI
Lippman E., Erwin D.C., Bartnicki-Garcia S. Isolation and chemical composition of oospore-oogonium walls of Phytophthora megasperma var. sojae. J. Gen. Microbiol. 1974;80:131–141. doi: 10.1099/00221287-80-1-131. DOI
Erwin D.C., Ribeiro O.K. Phytophthora Diseases Worldwide. APS Press; St. Paul, MN, USA: 1996.
Mulgund A. Increasing lipid accumulation in microalgae through environmental manipulation, metabolic and genetic engineering: A review in the energy NEXUS framework. Energy Nexus. 2022;5:100054. doi: 10.1016/j.nexus.2022.100054. DOI
Piligaev A.V., Sorokina K.N., Samoylova Y.V., Parmon V.N. Production of Microalgal Biomass with High Lipid Content and Their Catalytic Processing Into Biodiesel: A Review. Catal. Ind. 2019;11:349–359. doi: 10.1134/S207005041904007X. DOI
Narayan B., Miyashita K., Hosakawa M. Physiological effects of Eicosapentaenoic Acid (EPA) and Docosahexaenoic Acid (DHA)—A review. Food Rev. Int. 2006;22:291–307. doi: 10.1080/87559120600694622. DOI
Lee Chang K.J., Rye L., Dunstan G.A., Grant T., Koutoulis A., Nichols P.D., Blackburn S.I. Life cycle assessment: Heterotrophic cultivation of thraustochytrids for biodiesel production. J. Appl. Phycol. 2015;27:639–647. doi: 10.1007/s10811-014-0364-9. DOI
Patel A., Matsakas L., Pruthi P.A., Pruthi V. Potential of aquatic oomycete as a novel feedstock for microbial oil grown on waste sugarcane bagasse. Environ. Sci. Pollut. Res. 2018;25:33443–33454. doi: 10.1007/s11356-018-3183-8. PubMed DOI PMC
Leaño E.M., Gapasin R.S.J., Polohan B., Vrijmoed L.L.P. Growth and fatty acid production of thraustochytrids from Panay mangroves, Philippines. Fungal Divers. 2003;12:111–122.
Scanu B., Hunter G.C., Linaldeddu B.T., Franceschini A., Maddau L., Jung T., Denman S. A taxonomic re-evaluation reveals that Phytophthora cinnamomi and P. cinnamomic var parvispora are separate species. For. Pathol. 2014;44:1–20. doi: 10.1111/efp.12064. DOI
Jung T., Chang T.T., Bakony J., Seress D., Perez-Sierra A., Yang X., Hong C., Scanu B., Fu C.H., Hsueh K.L., et al. Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathol. 2017;66:194–211. doi: 10.1111/ppa.12564. DOI
Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959;37:911–917. doi: 10.1139/y59-099. PubMed DOI
Lepage G., Roy C.C. Improved recovery of fatty acid through direct transesterification without prior extraction or purification. J. Lipid Res. 1984;25:1391–1396. doi: 10.1016/S0022-2275(20)34457-6. PubMed DOI