Cargando…

Examination of gammarid transcriptomes reveals a widespread occurrence of key metabolic genes from epibiont bdelloid rotifers in freshwater species

Previous data revealed the unexpected presence of genes encoding for long-chain polyunsaturated fatty acid (LC-PUFA) biosynthetic enzymes in transcriptomes from freshwater gammarids but not in marine species, even though closely related species were compared. This study aimed to clarify the origin a...

Descripción completa

Detalles Bibliográficos
Autores principales: Ribes-Navarro, Alberto, Kabeya, Naoki, Castro, L. Filipe C., Gomes-dos-Santos, André, Fonseca, Miguel M., Alberts-Hubatsch, Hilke, Hontoria, Francisco, Navarro, Juan C., Monroig, Óscar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10597677/
https://www.ncbi.nlm.nih.gov/pubmed/37875161
http://dx.doi.org/10.1098/rsob.230196
_version_ 1785125394558484480
author Ribes-Navarro, Alberto
Kabeya, Naoki
Castro, L. Filipe C.
Gomes-dos-Santos, André
Fonseca, Miguel M.
Alberts-Hubatsch, Hilke
Hontoria, Francisco
Navarro, Juan C.
Monroig, Óscar
author_facet Ribes-Navarro, Alberto
Kabeya, Naoki
Castro, L. Filipe C.
Gomes-dos-Santos, André
Fonseca, Miguel M.
Alberts-Hubatsch, Hilke
Hontoria, Francisco
Navarro, Juan C.
Monroig, Óscar
author_sort Ribes-Navarro, Alberto
collection PubMed
description Previous data revealed the unexpected presence of genes encoding for long-chain polyunsaturated fatty acid (LC-PUFA) biosynthetic enzymes in transcriptomes from freshwater gammarids but not in marine species, even though closely related species were compared. This study aimed to clarify the origin and occurrence of selected LC-PUFA biosynthesis gene markers across all published gammarid transcriptomes. Through systematic searches, we confirmed the widespread occurrence of sequences from seven elongases and desaturases involved in LC-PUFA biosynthesis, in transcriptomes from freshwater gammarids but not marine species, and clarified that such occurrence is independent from the gammarid species and geographical origin. The phylogenetic analysis established that the retrieved elongase and desaturase sequences were closely related to bdelloid rotifers, confirming that multiple transcriptomes from freshwater gammarids contain contaminating rotifers' genetic material. Using the Adineta steineri genome, we investigated the genomic location and exon–intron organization of the elongase and desaturase genes, establishing they are all genome-anchored and, importantly, identifying instances of horizontal gene transfer. Finally, we provide compelling evidence demonstrating Bdelloidea desaturases and elongases enable these organisms to perform all the reactions for de novo biosynthesis of PUFA and, from them, LC-PUFA, an advantageous trait when considering the low abundance of these essential nutrients in freshwater environments.
format Online
Article
Text
id pubmed-10597677
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher The Royal Society
record_format MEDLINE/PubMed
spelling pubmed-105976772023-10-25 Examination of gammarid transcriptomes reveals a widespread occurrence of key metabolic genes from epibiont bdelloid rotifers in freshwater species Ribes-Navarro, Alberto Kabeya, Naoki Castro, L. Filipe C. Gomes-dos-Santos, André Fonseca, Miguel M. Alberts-Hubatsch, Hilke Hontoria, Francisco Navarro, Juan C. Monroig, Óscar Open Biol Research Previous data revealed the unexpected presence of genes encoding for long-chain polyunsaturated fatty acid (LC-PUFA) biosynthetic enzymes in transcriptomes from freshwater gammarids but not in marine species, even though closely related species were compared. This study aimed to clarify the origin and occurrence of selected LC-PUFA biosynthesis gene markers across all published gammarid transcriptomes. Through systematic searches, we confirmed the widespread occurrence of sequences from seven elongases and desaturases involved in LC-PUFA biosynthesis, in transcriptomes from freshwater gammarids but not marine species, and clarified that such occurrence is independent from the gammarid species and geographical origin. The phylogenetic analysis established that the retrieved elongase and desaturase sequences were closely related to bdelloid rotifers, confirming that multiple transcriptomes from freshwater gammarids contain contaminating rotifers' genetic material. Using the Adineta steineri genome, we investigated the genomic location and exon–intron organization of the elongase and desaturase genes, establishing they are all genome-anchored and, importantly, identifying instances of horizontal gene transfer. Finally, we provide compelling evidence demonstrating Bdelloidea desaturases and elongases enable these organisms to perform all the reactions for de novo biosynthesis of PUFA and, from them, LC-PUFA, an advantageous trait when considering the low abundance of these essential nutrients in freshwater environments. The Royal Society 2023-10-25 /pmc/articles/PMC10597677/ /pubmed/37875161 http://dx.doi.org/10.1098/rsob.230196 Text en © 2023 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Research
Ribes-Navarro, Alberto
Kabeya, Naoki
Castro, L. Filipe C.
Gomes-dos-Santos, André
Fonseca, Miguel M.
Alberts-Hubatsch, Hilke
Hontoria, Francisco
Navarro, Juan C.
Monroig, Óscar
Examination of gammarid transcriptomes reveals a widespread occurrence of key metabolic genes from epibiont bdelloid rotifers in freshwater species
title Examination of gammarid transcriptomes reveals a widespread occurrence of key metabolic genes from epibiont bdelloid rotifers in freshwater species
title_full Examination of gammarid transcriptomes reveals a widespread occurrence of key metabolic genes from epibiont bdelloid rotifers in freshwater species
title_fullStr Examination of gammarid transcriptomes reveals a widespread occurrence of key metabolic genes from epibiont bdelloid rotifers in freshwater species
title_full_unstemmed Examination of gammarid transcriptomes reveals a widespread occurrence of key metabolic genes from epibiont bdelloid rotifers in freshwater species
title_short Examination of gammarid transcriptomes reveals a widespread occurrence of key metabolic genes from epibiont bdelloid rotifers in freshwater species
title_sort examination of gammarid transcriptomes reveals a widespread occurrence of key metabolic genes from epibiont bdelloid rotifers in freshwater species
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10597677/
https://www.ncbi.nlm.nih.gov/pubmed/37875161
http://dx.doi.org/10.1098/rsob.230196
work_keys_str_mv AT ribesnavarroalberto examinationofgammaridtranscriptomesrevealsawidespreadoccurrenceofkeymetabolicgenesfromepibiontbdelloidrotifersinfreshwaterspecies
AT kabeyanaoki examinationofgammaridtranscriptomesrevealsawidespreadoccurrenceofkeymetabolicgenesfromepibiontbdelloidrotifersinfreshwaterspecies
AT castrolfilipec examinationofgammaridtranscriptomesrevealsawidespreadoccurrenceofkeymetabolicgenesfromepibiontbdelloidrotifersinfreshwaterspecies
AT gomesdossantosandre examinationofgammaridtranscriptomesrevealsawidespreadoccurrenceofkeymetabolicgenesfromepibiontbdelloidrotifersinfreshwaterspecies
AT fonsecamiguelm examinationofgammaridtranscriptomesrevealsawidespreadoccurrenceofkeymetabolicgenesfromepibiontbdelloidrotifersinfreshwaterspecies
AT albertshubatschhilke examinationofgammaridtranscriptomesrevealsawidespreadoccurrenceofkeymetabolicgenesfromepibiontbdelloidrotifersinfreshwaterspecies
AT hontoriafrancisco examinationofgammaridtranscriptomesrevealsawidespreadoccurrenceofkeymetabolicgenesfromepibiontbdelloidrotifersinfreshwaterspecies
AT navarrojuanc examinationofgammaridtranscriptomesrevealsawidespreadoccurrenceofkeymetabolicgenesfromepibiontbdelloidrotifersinfreshwaterspecies
AT monroigoscar examinationofgammaridtranscriptomesrevealsawidespreadoccurrenceofkeymetabolicgenesfromepibiontbdelloidrotifersinfreshwaterspecies