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

Author:

Ribes-Navarro Alberto1ORCID,Kabeya Naoki2ORCID,Castro L. Filipe C.34ORCID,Gomes-dos-Santos André3ORCID,Fonseca Miguel M.3ORCID,Alberts-Hubatsch Hilke5ORCID,Hontoria Francisco1ORCID,Navarro Juan C.1ORCID,Monroig Óscar1ORCID

Affiliation:

1. Instituto de Acuicultura Torre de la Sal (IATS), CSIC, 12595 Ribera de Cabanes, Castellón, Spain

2. Department of Marine Biosciences, Tokyo University of Marine Science and Technology, Konan 4-5-7, Minato, Tokyo, Japan

3. CIMAR/CIIMAR—Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Avenida General Norton de Matos, S/N, 4450-208 Matosinhos, Portugal

4. Department of Biology, Faculty of Sciences, University of Porto (U. Porto), Rua do Campo Alegre S/N, 4169-007 Porto, Portugal

5. Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Bremerhaven, Germany

Abstract

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.

Funder

Agencia Estatal de Investigación

Bundesministerium für Bildung und Forschung

Fundação para a Ciência e a Tecnologia

Publisher

The Royal Society

Subject

General Biochemistry, Genetics and Molecular Biology,Immunology,General Neuroscience

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