Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates
Background Provision of long-chain polyunsaturated fatty acids (LC-PUFA) in vertebrates occurs through the diet or via endogenous production from C18 precursors through consecutive elongations and desaturations. It has been postulated that the abundance of LC-PUFA in the marine environment has remar...
Published in: | BMC Evolutionary Biology |
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Main Authors: | , , , , , , , , |
Other Authors: | , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
BMC
2018
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Subjects: | |
Online Access: | http://hdl.handle.net/1893/28256 https://doi.org/10.1186/s12862-018-1271-5 http://dspace.stir.ac.uk/bitstream/1893/28256/1/LopezMarquesRetentionOfFattyAcylDesaturase.pdf |
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author | Lopes-Marques, Monica Kabeya, Naoki Qian, Yu Ruivo, Raquel Santos, Miguel Venkatesh, Byrappa Tocher, Douglas R Castro, L Filipe C Monroig, Oscar |
author2 | University of Porto University of Tokyo Institute of Aquaculture orcid:0000-0002-8603-9410 orcid:0000-0001-8712-0440 |
author_facet | Lopes-Marques, Monica Kabeya, Naoki Qian, Yu Ruivo, Raquel Santos, Miguel Venkatesh, Byrappa Tocher, Douglas R Castro, L Filipe C Monroig, Oscar |
author_sort | Lopes-Marques, Monica |
collection | University of Stirling: Stirling Digital Research Repository |
container_issue | 1 |
container_title | BMC Evolutionary Biology |
container_volume | 18 |
description | Background Provision of long-chain polyunsaturated fatty acids (LC-PUFA) in vertebrates occurs through the diet or via endogenous production from C18 precursors through consecutive elongations and desaturations. It has been postulated that the abundance of LC-PUFA in the marine environment has remarkably modulated the gene complement and function of Fads in marine teleosts. In vertebrates two fatty acyl desaturases, namely Fads1 and Fads2, encode ∆5 and ∆6 desaturases, respectively. To fully clarify the evolutionary history of LC-PUFA biosynthesis in vertebrates, we investigated the gene repertoire and function of Fads from species placed at key evolutionary nodes. Results We demonstrate that functional Fads1Δ5 and Fads2∆6 arose from a tandem gene duplication in the ancestor of vertebrates, since they are present in the Arctic lamprey. Additionally, we show that a similar condition was retained in ray-finned fish such as the Senegal bichir and spotted gar, with the identification of fads1 genes in these lineages. Functional characterisation of the isolated desaturases reveals the first case of a Fads1 enzyme with ∆5 desaturase activity in the Teleostei lineage, the Elopomorpha. In contrast, in Osteoglossomorpha genomes, while no fads1 was identified, two separate fads2 duplicates with ∆6 and ∆5 desaturase activities respectively were uncovered. Conclusions We conclude that, while the essential genetic components involved LC-PUFA biosynthesis evolved in the vertebrate ancestor, the full completion of the LC-PUFA biosynthesis pathway arose uniquely in gnathostomes. |
format | Article in Journal/Newspaper |
genre | Arctic |
genre_facet | Arctic |
geographic | Arctic Gar’ |
geographic_facet | Arctic Gar’ |
id | ftunivstirling:oai:dspace.stir.ac.uk:1893/28256 |
institution | Open Polar |
language | English |
long_lat | ENVELOPE(162.014,162.014,57.140,57.140) |
op_collection_id | ftunivstirling |
op_doi | https://doi.org/10.1186/s12862-018-1271-5 |
op_relation | Lopes-Marques M, Kabeya N, Qian Y, Ruivo R, Santos M, Venkatesh B, Tocher DR, Castro LFC & Monroig O (2018) Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates. BMC Evolutionary Biology , 18, Art. No.: 157. https://doi.org/10.1186/s12862-018-1271-5 157 http://hdl.handle.net/1893/28256 30340454 1041093 http://dspace.stir.ac.uk/bitstream/1893/28256/1/LopezMarquesRetentionOfFattyAcylDesaturase.pdf |
op_rights | © The Author(s). 2018 This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. http://creativecommons.org/licenses/by/4.0/ |
publishDate | 2018 |
publisher | BMC |
record_format | openpolar |
spelling | ftunivstirling:oai:dspace.stir.ac.uk:1893/28256 2025-04-06T14:46:07+00:00 Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates Lopes-Marques, Monica Kabeya, Naoki Qian, Yu Ruivo, Raquel Santos, Miguel Venkatesh, Byrappa Tocher, Douglas R Castro, L Filipe C Monroig, Oscar University of Porto University of Tokyo Institute of Aquaculture orcid:0000-0002-8603-9410 orcid:0000-0001-8712-0440 2018-10-19 application/pdf http://hdl.handle.net/1893/28256 https://doi.org/10.1186/s12862-018-1271-5 http://dspace.stir.ac.uk/bitstream/1893/28256/1/LopezMarquesRetentionOfFattyAcylDesaturase.pdf en eng BMC Lopes-Marques M, Kabeya N, Qian Y, Ruivo R, Santos M, Venkatesh B, Tocher DR, Castro LFC & Monroig O (2018) Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates. BMC Evolutionary Biology , 18, Art. No.: 157. https://doi.org/10.1186/s12862-018-1271-5 157 http://hdl.handle.net/1893/28256 30340454 1041093 http://dspace.stir.ac.uk/bitstream/1893/28256/1/LopezMarquesRetentionOfFattyAcylDesaturase.pdf © The Author(s). 2018 This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. http://creativecommons.org/licenses/by/4.0/ Biosynthesis Fatty acyl desaturase Gene duplication Gene loss Long-chain polyunsaturated fatty acids Journal Article VoR - Version of Record 2018 ftunivstirling https://doi.org/10.1186/s12862-018-1271-5 2025-03-11T04:30:58Z Background Provision of long-chain polyunsaturated fatty acids (LC-PUFA) in vertebrates occurs through the diet or via endogenous production from C18 precursors through consecutive elongations and desaturations. It has been postulated that the abundance of LC-PUFA in the marine environment has remarkably modulated the gene complement and function of Fads in marine teleosts. In vertebrates two fatty acyl desaturases, namely Fads1 and Fads2, encode ∆5 and ∆6 desaturases, respectively. To fully clarify the evolutionary history of LC-PUFA biosynthesis in vertebrates, we investigated the gene repertoire and function of Fads from species placed at key evolutionary nodes. Results We demonstrate that functional Fads1Δ5 and Fads2∆6 arose from a tandem gene duplication in the ancestor of vertebrates, since they are present in the Arctic lamprey. Additionally, we show that a similar condition was retained in ray-finned fish such as the Senegal bichir and spotted gar, with the identification of fads1 genes in these lineages. Functional characterisation of the isolated desaturases reveals the first case of a Fads1 enzyme with ∆5 desaturase activity in the Teleostei lineage, the Elopomorpha. In contrast, in Osteoglossomorpha genomes, while no fads1 was identified, two separate fads2 duplicates with ∆6 and ∆5 desaturase activities respectively were uncovered. Conclusions We conclude that, while the essential genetic components involved LC-PUFA biosynthesis evolved in the vertebrate ancestor, the full completion of the LC-PUFA biosynthesis pathway arose uniquely in gnathostomes. Article in Journal/Newspaper Arctic University of Stirling: Stirling Digital Research Repository Arctic Gar’ ENVELOPE(162.014,162.014,57.140,57.140) BMC Evolutionary Biology 18 1 |
spellingShingle | Biosynthesis Fatty acyl desaturase Gene duplication Gene loss Long-chain polyunsaturated fatty acids Lopes-Marques, Monica Kabeya, Naoki Qian, Yu Ruivo, Raquel Santos, Miguel Venkatesh, Byrappa Tocher, Douglas R Castro, L Filipe C Monroig, Oscar Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates |
title | Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates |
title_full | Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates |
title_fullStr | Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates |
title_full_unstemmed | Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates |
title_short | Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates |
title_sort | retention of fatty acyl desaturase 1 (fads1) in elopomorpha and cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates |
topic | Biosynthesis Fatty acyl desaturase Gene duplication Gene loss Long-chain polyunsaturated fatty acids |
topic_facet | Biosynthesis Fatty acyl desaturase Gene duplication Gene loss Long-chain polyunsaturated fatty acids |
url | http://hdl.handle.net/1893/28256 https://doi.org/10.1186/s12862-018-1271-5 http://dspace.stir.ac.uk/bitstream/1893/28256/1/LopezMarquesRetentionOfFattyAcylDesaturase.pdf |