title: Against All Odds: Trehalose-6-Phosphate Synthase and Trehalase Genes in the Bdelloid Rotifer Adineta vaga Were Acquired by Horizontal Gene Transfer and Are Upregulated during Desiccation.
abstract: The disaccharide sugar trehalose is essential for desiccation resistance in most metazoans that survive dryness; however, neither trehalose nor the enzymes involved in its metabolism have ever been detected in bdelloid rotifers despite their extreme resistance to desiccation. Here we screened the genome of the bdelloid rotifer Adineta vaga for genes involved in trehalose metabolism. We discovered a total of four putative trehalose-6-phosphate synthase (TPS) and seven putative trehalase (TRE) gene copies in the genome of this ameiotic organism; however, no trehalose-6-phosphate phosphatase (TPP) gene or domain was detected. The four TPS copies of A. vaga appear more closely related to plant and fungi proteins, as well as to some protists, whereas the seven TRE copies fall in bacterial clades. Therefore, A. vaga likely acquired its trehalose biosynthesis and hydrolysis genes by horizontal gene transfers. Nearly all residues important for substrate binding in the predicted TPS domains are highly conserved, supporting the hypothesis that several copies of the genes might be functional. Besides, RNAseq library screening showed that trehalase genes were highly expressed compared to TPS genes, explaining probably why trehalose had not been detected in previous studies of bdelloids. A strong overexpression of their TPS genes was observed when bdelloids enter desiccation, suggesting a possible signaling role of trehalose-6-phosphate or trehalose in this process.
authors.affiliation: LEGE laboratory, URBE, Department of Biology, University of Namur, Namur, Belgium.
authors.forename: Boris
authors.initials: B
authors.lastname: Hespeels
authors.affiliation: LEGE laboratory, URBE, Department of Biology, University of Namur, Namur, Belgium.
authors.forename: Xiang
authors.initials: X
authors.lastname: Li
authors.affiliation: Department of Genetics, Evolution and Environment, University College London, London, United Kingdom.
authors.forename: Jean-François
authors.initials: JF
authors.lastname: Flot
authors.affiliation: LEGE laboratory, URBE, Department of Biology, University of Namur, Namur, Belgium.
authors.forename: Lise-Marie
authors.initials: LM
authors.lastname: Pigneur
authors.affiliation: Research Unit for Molecular Physiology, Cell and Tissue Laboratory, Namur, Belgium.
authors.forename: Jeremy
authors.initials: J
authors.lastname: Malaisse
authors.affiliation: CEA-Institut de Génomique, GENOSCOPE, Centre National de Séquençage, Evry, France.
authors.forename: Corinne
authors.initials: C
authors.lastname: Da Silva
authors.affiliation: LEGE laboratory, URBE, Department of Biology, University of Namur, Namur, Belgium; naXys, Namur Center for Complex Systems, University of Namur, Namur, Belgium.
authors.forename: Karine
authors.initials: K
authors.lastname: Van Doninck
mesh_terms: D000818:Animals; D003890:Desiccation / Q000379:methods; D018628:Gene Dosage; D022761:Gene Transfer, Horizontal; D005964:Glucosyltransferases / Q000145:classification / Q000235:genetics* / Q000378:metabolism; D015801:Helminth Proteins / Q000235:genetics* / Q000378:metabolism; D053858:Metabolic Networks and Pathways; D010744:Phosphoric Monoester Hydrolases / Q000235:genetics / Q000378:metabolism; D010802:Phylogeny; D020133:Reverse Transcriptase Polymerase Chain Reaction; D012403:Rotifera / Q000201:enzymology / Q000235:genetics*; D015533:Transcriptional Activation; D014198:Trehalase / Q000235:genetics* / Q000378:metabolism; D014199:Trehalose / Q000378:metabolism; D015854:Up-Regulation
chemical_list: D015801:Helminth Proteins; D014199:Trehalose; D005964:Glucosyltransferases; C023180:trehalose-6-phosphate synthase; C023178:trehalose-phosphatase; D010744:Phosphoric Monoester Hydrolases; D014198:Trehalase