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An Evolutionary Perspective on Linoleic Acid Synthesis in Animals

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Malcicka, Miriama [Department of Ecological Sciences, Section Animal EcologyVrije Universiteit, AmsterdamAmsterdam, The Netherlands] Visser, Bertanne [UCL] Ellers, Jacintha [Department of Ecological Sciences, Section Animal EcologyVrije Universiteit, AmsterdamAmsterdam, The Netherlands]

The diet of organisms generally provides a sufficient supply of energy and building materials for healthy growth and development, but should also contain essential nutrients. Species differ in their exogenous requirements, but it is not clear why some species are able to synthesize essential nutrients, while others are not. The unsaturated fatty acid, linoleic acid (LA; 18:2n-6) plays an important role in functions such as cell physiology, immunity, and reproduction, and is an essential nutrient in diverse organisms. LA is readily synthesized in bacteria, protozoa and plants, but it was long thought that all animals lacked the ability to synthesize LA de novo and thus required a dietary source of this fatty acid. Over the years, however, an increasing number of studies have shown active LA synthesis in animals, including insects, nematodes and pulmonates. Despite continued interest in LA metabolism, it has remained unclear why some organisms can synthesize LA while others cannot. Here, we review the mechanisms by which LA is synthesized and which biological functions LA supports in different organisms to answer the question why LA synthesis was lost and repeatedly gained during the evolution of distinct invertebrate groups. We propose several hypotheses and compile data from the available literature to identify which factors promote LA synthesis within a phylogenetic framework. We have not found a clear link between our proposed hypotheses and LA synthesis; therefore we suggest that LA synthesis may be facilitated through bifunctionality of desaturase enzymes or evolved through a combination of different selective pressures.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2017
Language Anglais
Journal information "Evolutionary Biology" - Vol. 11, p. 1-12 (2017)
Peer reviewed yes
Publisher Springer New York LLC (New York)
issn 0071-3260
e-issn 1934-2845
Publication status Publié
Affiliation UCL - SST/ELI/ELIB - Biodiversity
Keywords Ecology ; Evolution ; Behavior and Systematics ; De novo synthesis ; Arthropods ; Essential nutrients ; Fatty acids ; PUFAs ; Desaturase
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  1. Aboshi Takako, Shimizu Nobuhiro, Nakajima Yuji, Honda Yoshiyuki, Kuwahara Yasumasa, Amano Hiroshi, Mori Naoki, Biosynthesis of linoleic acid in Tyrophagus mites (Acarina: Acaridae), 10.1016/j.ibmb.2013.08.002
  2. López Alonso D., García-Maroto F., Rodríguez-Ruiz J., Garrido J.A., Vilches M.A., Evolution of the membrane-bound fatty acid desaturases, 10.1016/s0305-1978(03)00041-3
  3. Alonso Jana, Schimpl Marianne, van Aalten Daan M. F., O-GlcNAcase: Promiscuous Hexosaminidase or Key Regulator ofO-GlcNAc Signaling?, 10.1074/jbc.r114.609198
  4. Anderson, G. J., & Connor, W. E. (1989). On the demonstration of ω-3 essential-fatty-acid deficiency in humans. The American Journal of Clinical Nutrition, 49, 585–587.
  5. Belury Martha A., DIETARYCONJUGATEDLINOLEICACID INHEALTH: Physiological Effects and Mechanisms of Action, 10.1146/annurev.nutr.22.021302.121842
  6. Blaul Birgit, Steinbauer Robert, Merkl Philipp, Merkl Rainer, Tschochner Herbert, Ruther Joachim, Oleic acid is a precursor of linoleic acid and the male sex pheromone in Nasonia vitripennis, 10.1016/j.ibmb.2014.05.007
  7. Blomquist Gary J., Dwyer Lawrence A., Chu Arthur J., Ryan Robert O., de Renobales Mertxe, Biosynthesis of linoleic acid in a termite, cockroach and cricket, 10.1016/0020-1790(82)90093-2
  8. Blomquist Gary J., Nelson Dennis R., De Renobales Mertxe, Chemistry, biochemistry, and physiology of insect cuticular lipids, 10.1002/arch.940060404
  9. Booth-Kewley Stephanie, Friedman Howard S., Psychological predictors of heart disease: A quantitative review., 10.1037/0033-2909.101.3.343
  10. Borgeson C. E., Kurtti T. J., Munderloh U. G., Blomquist G. J., Insect tissues, not microorganisms, produce linoleic acid in the house cricket and the American cockroach, 10.1007/bf01958146
  11. Brandstetter Birgit, Ruther Joachim, An insect with a delta-12 desaturase, the jewel wasp Nasonia vitripennis, benefits from nutritional supply with linoleic acid, 10.1007/s00114-016-1365-0
  12. Brock Gareth R, Chapple Iain L C, The Potential Impact of Essential Nutrients Vitamins C and D upon Periodontal Disease Pathogenesis and Therapeutic Outcomes, 10.1007/s40496-016-0116-9
  13. Browse J, Somerville C, Glycerolipid Synthesis: Biochemistry and Regulation, 10.1146/annurev.pp.42.060191.002343
  14. Buček Aleš, Matoušková Petra, Sychrová Hana, Pichová Iva, Hrušková-Heidingsfeldová Olga, Δ12-Fatty Acid Desaturase from Candida parapsilosis Is a Multifunctional Desaturase Producing a Range of Polyunsaturated and Hydroxylated Fatty Acids, 10.1371/journal.pone.0093322
  15. Büyükgüzel Ender, EICOSANOIDS MEDIATE CELLULAR IMMUNE RESPONSE AND PHENOLOXIDASE REACTION TO VIRAL INFECTION IN ADULT Pimpla turionellae : Adult Cellular Immune Response to Viral Infection, 10.1002/arch.21031
  16. Certik Milan, Shimizu Sakayu, Biosynthesis and regulation of microbial polyunsaturated fatty acid production, 10.1016/s1389-1723(99)80001-2
  17. Chatterjee I. B., Evolution and the Biosynthesis of Ascorbic Acid, 10.1126/science.182.4118.1271
  18. Chodok Pichit, Eiamsa-ard Pradinunt, Cove David J., Quatrano Ralph S., Kaewsuwan Sireewan, Identification and functional characterization of two Δ12-fatty acid desaturases associated with essential linoleic acid biosynthesis in Physcomitrella patens, 10.1007/s10295-013-1285-3
  19. Chuang Lu-Te, Leonard Amanda E., Liu Jim-Wen, Mukerji Pradip, Bray Tammy M., Huang Yung-Sheng, Inhibitory effect of conjugated linoleic acid on linoleic acid elongation in transformed yeast with human elongase, 10.1007/s11745-001-0819-0
  20. Covello P. S., Reed D. W., Functional Expression of the Extraplastidial Arabidopsis thaliana Oleate Desaturase Gene (FAD2) in Saccharomyces cerevisiae, 10.1104/pp.111.1.223
  21. Cripps Colleen, Blomquist Gary J., de Renobales Mertxe, De novo biosynthesis of linoleic acid in insects, 10.1016/0005-2760(86)90046-9
  22. De Renobales Mertxe, Ryan Robert O., Heisler Charles R., McLean Donald L., Blomquist Gary J., Linoleic acid biosynthesis in the pea aphid,Acyrthosiphon pisum (Harris), 10.1002/arch.940030209
  23. de Veth M.J., Bauman D.E., Koch W., Mann G.E., Pfeiffer A.M., Butler W.R., Efficacy of conjugated linoleic acid for improving reproduction: A multi-study analysis in early-lactation dairy cows, 10.3168/jds.2008-1845
  24. Destephano Don B., Brady U.Eugene, Prostaglandin and prostaglandin synthetase in the cricket, Acheta domesticus, 10.1016/0022-1910(77)90019-1
  25. Domenichiello Anthony F., Kitson Alex P., Chen Chuck T., Trépanier Marc-Olivier, Stavro P. Mark, Bazinet Richard P., The effect of linoleic acid on the whole body synthesis rates of polyunsaturated fatty acids from α-linolenic acid and linoleic acid in free-living rats, 10.1016/j.jnutbio.2015.11.016
  26. Douglas A. E., Nutritional Interactions in Insect-Microbial Symbioses: Aphids and Their Symbiotic BacteriaBuchnera, 10.1146/annurev.ento.43.1.17
  27. Dwyer Lawrence A., Blomquist Gary J., Nelson John H., George Pomonis J., A 13C-NMR study of the biosynthesis of 3-methylpentacosane in the American cockroach, 10.1016/0005-2760(81)90181-8
  28. Eder, K., Schleser, S., Becker, K., & Körting, R. (2003). Conjugated linoleic acids lower the release of eicosanoids and nitric oxide from human aortic endothelial cells. The Journal of Nutrition, 133, 4083–4089.
  29. Eleftherianos Ioannis, Atri Jaishri, Accetta Julia, Castillo Julio C., Endosymbiotic bacteria in insects: guardians of the immune system?, 10.3389/fphys.2013.00046
  30. Ellers Jacintha, Toby Kiers E., Currie Cameron R., McDonald Bradon R., Visser Bertanne, Ecological interactions drive evolutionary loss of traits, 10.1111/j.1461-0248.2012.01830.x
  31. El-Yassimi Abdelghani, Hichami Aziz, Besnard Philippe, Khan Naim Akhtar, Linoleic Acid Induces Calcium Signaling, Src Kinase Phosphorylation, and Neurotransmitter Release in Mouse CD36-positive Gustatory Cells, 10.1074/jbc.m707478200
  32. Farmer Edward E., Fatty acid signalling in plants and their associated microorganisms, 10.1007/bf00016483
  33. Fromm Herbert J., Hargrove Mark, Essentials of Biochemistry, ISBN:9783642196232, 10.1007/978-3-642-19624-9
  34. Gostinčar Cene, Turk Martina, Plemenitaš Ana, Gunde-Cimerman Nina, The expressions of Δ9-, Δ12-desaturases and an elongase by the extremely halotolerant black yeastHortaea werneckiiare salt dependent, 10.1111/j.1567-1364.2009.00481.x
  35. Grosso Giuseppe, Micek Agnieszka, Marventano Stefano, Castellano Sabrina, Mistretta Antonio, Pajak Andrzej, Galvano Fabio, Dietary n-3 PUFA, fish consumption and depression: A systematic review and meta-analysis of observational studies, 10.1016/j.jad.2016.08.011
  36. Harizi H., Gualde N., The impact of eicosanoids on the crosstalk between innate and adaptive immunity: the key roles of dendritic cells, 10.1111/j.1399-0039.2005.00394.x
  37. Hashimoto Kosuke, Yoshizawa Akiyasu C., Okuda Shujiro, Kuma Keiichi, Goto Susumu, Kanehisa Minoru, The repertoire of desaturases and elongases reveals fatty acid variations in 56 eukaryotic genomes, 10.1194/jlr.m700377-jlr200
  38. Hazel J R, Thermal Adaptation in Biological Membranes: Is Homeoviscous Adaptation the Explanation?, 10.1146/annurev.ph.57.030195.000315
  39. Helliwell Katherine E., Wheeler Glen L., Smith Alison G., Widespread decay of vitamin-related pathways: coincidence or consequence?, 10.1016/j.tig.2013.03.003
  40. Horrobin David F., The membrane phospholipid hypothesis as a biochemical basis for the neurodevelopmental concept of schizophrenia, 10.1016/s0920-9964(97)00151-5
  41. Hulbert A. J., Turner N., Storlien L. H., Else P. L., Dietary fats and membrane function: implications for metabolism and disease, 10.1017/s1464793104006578
  42. Iskandarov Umidjon, Khozin-Goldberg Inna, Cohen Zvi, Identification and Characterization of Δ12, Δ6, and Δ5 Desaturases from the Green Microalga Parietochloris incisa, 10.1007/s11745-010-3421-4
  43. Jenkins Nathaniel D.M., Buckner Samuel L., Baker Robert B., Bergstrom Haley C., Cochrane Kristen C., Weir Joseph P., Housh Terry J., Cramer Joel T., Effects of 6 Weeks of Aerobic Exercise Combined With Conjugated Linoleic Acid on the Physical Working Capacity at Fatigue Threshold : , 10.1519/jsc.0000000000000513
  44. Jurenka Russell A., de Renobales Mertxe, Blomquist Gary J., De novo biosynthesis of polyunsaturated fatty acids in the cockroach Periplaneta americana, 10.1016/0003-9861(87)90309-2
  45. Kainou Kumiko, Kamisaka Yasushi, Kimura Kazuyoshi, Uemura Hiroshi, Isolation of Δ12 and ω3-fatty acid desaturase genes from the yeastKluyveromyces lactis and their heterologous expression to produce linoleic and α-linolenic acids inSaccharomyces cerevisiae, 10.1002/yea.1378
  46. Kalmijn S., Feskens E. J. M., Launer L J., Kromhout D., Polyunsaturated Fatty Acids, Antioxidants, and Cognitive Function in Very Old Men, 10.1093/oxfordjournals.aje.a009029
  47. Kaye Yuval, Grundman Omer, Leu Stefan, Zarka Aliza, Zorin Boris, Didi-Cohen Shoshana, Khozin-Goldberg Inna, Boussiba Sammy, Metabolic engineering toward enhanced LC-PUFA biosynthesis in Nannochloropsis oceanica : Overexpression of endogenous Δ12 desaturase driven by stress-inducible promoter leads to enhanced deposition of polyunsaturated fatty acids in TAG, 10.1016/j.algal.2015.05.003
  48. Kennedy David, B Vitamins and the Brain: Mechanisms, Dose and Efficacy—A Review, 10.3390/nu8020068
  49. Kuwahara Yasumasa, Chemical ecology of astigmatid mites, Advances in Insect Chemical Ecology ISBN:9780511542664 p.76-109, 10.1017/cbo9780511542664.004
  50. Los Dmitry A., Murata Norio, Structure and expression of fatty acid desaturases, 10.1016/s0005-2760(98)00091-5
  51. Louloudes Spiro J., Kaplanis J. N., Robbins W. E., Monroe R. E., Lipogenesis from C14-Acetate by the American Cockroach1, 10.1093/aesa/54.1.99
  52. Lu Yandu, Chi Xiaoyuan, Yang Qingli, Li Zhaoxin, Liu Shaofang, Gan Qinhua, Qin Song, Molecular cloning and stress-dependent expression of a gene encoding Δ12-fatty acid desaturase in the Antarctic microalga Chlorella vulgaris NJ-7, 10.1007/s00792-009-0275-x
  53. Macartney, A., Maresca, B., & Cossins, A. R. (1994). Acyl-CoA desaturases and the adaptive regulation of membrane lipid composition. Temperature adaptation of biological membranes. London: Portland Press.
  54. Malcicka Miriama, Ruther Joachim, Ellers Jacintha, De novo Synthesis of Linoleic Acid in Multiple Collembola Species, 10.1007/s10886-017-0878-0
  55. Mauldin Joe K., Rich Nely M., Cook David W., Amino acid synthesis from 14C-acetate by normally and abnormally faunated termites, Coptotermes formosanus, 10.1016/0020-1790(78)90046-x
  56. Mauldin Joe K., Smythe Richard V., Baxter Cyril C., Cellulose catabolism and lipid synthesis by the subterranean termite, Coptotermes formosanus, 10.1016/0020-1790(72)90055-8
  57. Millar Jocelyn G., Polyene hydrocarbons and epoxides: A Second Major Class of Lepidopteran Sex Attractant Pheromones, 10.1146/annurev.ento.45.1.575
  58. Murata N, Wada H, Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria, 10.1042/bj3080001
  59. Nugteren, D. H., Van Evert, W. C., Soeting, W. J., & Spuy, J. H. (1979). Effect of different amounts of linoleic acid in the diet on the excretion of urinary prostaglandin metabolites in the rat. Advances in Prostaglandin and Thromboxane Research, 8, 1793–1796.
  60. Ohta Yuriko, Nishikimi Morimitsu, Random nucleotide substitutions in primate nonfunctional gene for l-gulono-γ-lactone oxidase, the missing enzyme in l-ascorbic acid biosynthesis1The nucleotide sequences reported in this paper have been submitted to GenBank under accession Nos. AB025719, AB025786, and AB025787.1, 10.1016/s0304-4165(99)00123-3
  61. Oliver Kerry M., Degnan Patrick H., Burke Gaelen R., Moran Nancy A., Facultative Symbionts in Aphids and the Horizontal Transfer of Ecologically Important Traits, 10.1146/annurev-ento-112408-085305
  62. Palmquist Donald L., Lock Adam L., Shingfield Kevin J., Bauman Dale E., Biosynthesis of Conjugated Linoleic Acid in Ruminants and Humans, Advances in Food and Nutrition Research (2005) ISBN:9780120164509 p.179-217, 10.1016/s1043-4526(05)50006-8
  63. Pandey Vimal Chandra, Prakash Prem, Bajpai Omesh, Kumar Akhilesh, Singh Nandita, Phytodiversity on fly ash deposits: evaluation of naturally colonized species for sustainable phytorestoration, 10.1007/s11356-014-3517-0
  64. Park Wan Beom, Kim Nak-Hyun, Kim Kye-Hyung, Lee Seung Hwan, Nam Won-Seok, Yoon Seo Hyun, Song Kyoung-Ho, Choe Pyoeng Gyun, Kim Nam Joong, Jang In-Jin, Oh Myoung-don, Yu Kyung-Sang, The Effect of Therapeutic Drug Monitoring on Safety and Efficacy of Voriconazole in Invasive Fungal Infections: A Randomized Controlled Trial, 10.1093/cid/cis599
  65. Peyou-Ndi Marlyse M., Watts Jennifer L., Browse John, Identification and Characterization of an Animal Δ12 Fatty Acid Desaturase Gene by Heterologous Expression in Saccharomyces cerevisiae, 10.1006/abbi.2000.1733
  66. Qi Baoxiu, Fraser Tom, Mugford Sam, Dobson Gary, Sayanova Olga, Butler Justine, Napier Johnathan A, Stobart A Keith, Lazarus Colin M, Production of very long chain polyunsaturated omega-3 and omega-6 fatty acids in plants, 10.1038/nbt972
  67. JIN Rong, LIU Nai-yong, LIU Yan, DONG Shuang-lin, A larval specific OBP able to bind the major female sex pheromone component in Spodoptera exigua (Hübner), 10.1016/s2095-3119(14)60849-2
  68. Rule Geoffrey S., Roelofs Wendell L., Biosynthesis of sex pheromone components from linolenic acid in arctiid moths, 10.1002/arch.940120203
  69. Sampath Harini, Ntambi James M., POLYUNSATURATED FATTY ACID REGULATION OF GENES OF LIPID METABOLISM, 10.1146/annurev.nutr.25.051804.101917
  70. Shimizu Nobuhiro, Naito Michiya, Mori Naoki, Kuwahara Yasumasa, De novo biosynthesis of linoleic acid and its conversion to the hydrocarbon (Z,Z)-6,9-heptadecadiene in the astigmatid mite, Carpoglyphus lactis: Incorporation experiments with 13C-labeled glucose, 10.1016/j.ibmb.2013.11.006
  71. Sinclair, A. J., Begg, D., Mathai, M., & Weisinger, R. S. (2007). Omega 3 fatty acids and the brain: Review of studies in depression. Asia Pacific Journal of Clinical Nutrition, 16, 391–397.
  72. Stanley David, PROSTAGLANDINS AND OTHER EICOSANOIDS IN INSECTS: Biological Significance, 10.1146/annurev.ento.51.110104.151021
  73. Stanley William C., Khairallah Ramzi J., Dabkowski Erinne R., Update on lipids and mitochondrial function : impact of dietary n-3 polyunsaturated fatty acids, 10.1097/mco.0b013e32834fdaf7
  74. Stanley-Samuelson D. W., Jensen E., Nickerson K. W., Tiebel K., Ogg C. L., Howard R. W., Insect immune response to bacterial infection is mediated by eicosanoids., 10.1073/pnas.88.3.1064
  75. Stanley-Samuelson David W., Loher Werner, Blomquist Gary J., Biosynthesis of polyunsaturated fatty acids by the australian field cricket, Teleogryllus commodus, 10.1016/0020-1790(86)90052-1
  76. STANLEY-SAMUELSON DAVID W., PELOQUIN JOHN J., LOHER WERNER, Egg-laying in response to prostaglandin injections in the Australian field cricket, Teleogryllus commodus, 10.1111/j.1365-3032.1986.tb00408.x
  77. Thelen Jay J., Ohlrogge John B., Metabolic Engineering of Fatty Acid Biosynthesis in Plants, 10.1006/mben.2001.0204
  78. VANDERWEL DÉSIRÉE, OEHLSCHLAGER A. CAMERON, Biosynthesis of Pheromones and Endocrine Regulation of Pheromone Production in Coleoptera, Pheromone Biochemistry (1987) ISBN:9780125644853 p.175-215, 10.1016/b978-0-12-564485-3.50011-7
  79. Visser Bertanne, Ellers Jacintha, Lack of lipogenesis in parasitoids: A review of physiological mechanisms and evolutionary implications, 10.1016/j.jinsphys.2008.07.014
  80. Visser B., Le Lann C., den Blanken F. J., Harvey J. A., van Alphen J. J. M., Ellers J., Loss of lipid synthesis as an evolutionary consequence of a parasitic lifestyle, 10.1073/pnas.1001744107
  81. Wallis James G., Watts Jennifer L., Browse John, Polyunsaturated fatty acid synthesis: what will they think of next?, 10.1016/s0968-0004(02)02168-0
  82. Watts J. L., Browse J., Genetic dissection of polyunsaturated fatty acid synthesis in Caenorhabditis elegans, 10.1073/pnas.092064799
  83. Weber Hans, Fatty acid-derived signals in plants, 10.1016/s1360-1385(02)02250-1
  84. Weinert J., Blomquist G. J., Borgeson C. E., De novo biosynthesis of linoleic acid in two non-insect invertebrates: The land slug and the garden snail, 10.1007/bf01952610
  85. Wharton D.R.A., Lola J.E., Blood conditions and lysozyme action in the aposymbiotic cockroach, 10.1016/0022-1910(70)90161-7
  86. Yamaja Setty B.N., Ramaiah T.R., Isolation and identification of prostaglandins from the reproductive organs of male silkmoth, Bombyx mori L., 10.1016/0020-1790(79)90100-8
  87. Yan Zhang, Zhuo Liang, Mulan Jiang, Xia Wan, Yangmin Gon, Yinbo Zhang, Fenghong Huang, Clone and identification of bifunctional Δ12/Δ15 fatty acid desaturase LKFAD15 from Lipomyces kononenkoae, 10.1007/s10068-013-0116-7
  88. Zhou X.-R., Horne I., Damcevski K., Haritos V., Green A., Singh S., Isolation and functional characterization of two independently-evolved fatty acid Δ12-desaturase genes from insects, 10.1111/j.1365-2583.2008.00841.x
  89. Zhou Xue-Rong, Green Allan G., Singh Surinder P., Caenorhabditis elegansΔ12-Desaturase FAT-2 Is a Bifunctional Desaturase Able to Desaturate a Diverse Range of Fatty Acid Substrates at the Δ12 and Δ15 Positions, 10.1074/jbc.m111.266114
Bibliographic reference Malcicka, Miriama ; Visser, Bertanne ; Ellers, Jacintha. An Evolutionary Perspective on Linoleic Acid Synthesis in Animals. In: Evolutionary Biology, Vol. 11, p. 1-12 (2017)
Permanent URL http://hdl.handle.net/2078.1/193048