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.

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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.

langue originaleAnglais
Numéro d'articlee0131313
journalPLoS ONE
Volume10
Numéro de publication7
Les DOIs
étatPublié - 10 juil. 2015

Empreinte digitale

Trehalase
trehalase
Gene transfer
Horizontal Gene Transfer
Desiccation
Rotifera
trehalose
Trehalose
Genes
genes
Metabolism
Genome
Plant Proteins
metabolism
genome
trehalose-6-phosphate synthase
alpha,alpha-trehalose-phosphate synthase (UDP-forming)
horizontal gene transfer
Adineta vaga
Disaccharides

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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.",
author = "Boris Hespeels and Xiang Li and Jean-Fran{\cc}ois Flot and Lise-Marie Pigneur and J{\'e}r{\'e}my Malaisse and {Da Silva}, Corine and {Van Doninck}, Karine",
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T1 - 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.

AU - Hespeels, Boris

AU - Li, Xiang

AU - Flot, Jean-François

AU - Pigneur, Lise-Marie

AU - Malaisse, Jérémy

AU - Da Silva, Corine

AU - Van Doninck, Karine

PY - 2015/7/10

Y1 - 2015/7/10

N2 - 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.

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