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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.

Hespeels B, Li X, Flot JF, Pigneur LM, Malaisse J, Da Silva C, Van Doninck K - PLoS ONE (2015)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: LEGE laboratory, URBE, Department of Biology, University of Namur, Namur, Belgium.

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.

No MeSH data available.


Annotation of the scaffolds containing (a) TPS and (b) TRE genes in Adineta vaga.Color-filled rectangles represent genes, numbers refer to the list at the bottom of the figure. Genes were colored in green or red if AI<45 or AI≥45, respectively. The genes annotated automatically in the A. vaga genome are surrounded with continuous lines, whereas discontinued lines surround additional genes detected during manual curation. The gene orientation is indicated by the position above (forward direction) or below (reverse direction) the line.
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pone.0131313.g001: Annotation of the scaffolds containing (a) TPS and (b) TRE genes in Adineta vaga.Color-filled rectangles represent genes, numbers refer to the list at the bottom of the figure. Genes were colored in green or red if AI<45 or AI≥45, respectively. The genes annotated automatically in the A. vaga genome are surrounded with continuous lines, whereas discontinued lines surround additional genes detected during manual curation. The gene orientation is indicated by the position above (forward direction) or below (reverse direction) the line.

Mentions: The TBLASTN search results for A. vaga homologues of trehalose phosphate synthase (TPS) from a wide range of species (bacteria, fungi, plants and metazoans) yielded significant E-values (< 10−10) for four predicted genes belonging to three different scaffolds (av51, av255 and av681) in the A. vaga genomic dataset. Indeed, A. vaga was previously reported to be an ancient degenerate tetraploid [39], hence finding more than two copies of a given gene was not surprising. Two TPS genes were found on a palindromic, highly colinear allelic region [39] of scaffold av51, and were annotated AvTpsA and AvTpsA’ (Fig 1A). The surrounding region of the TPS copies on scaffolds av255 and av681 were also highly colinear and therefore probably allelic [39]: these two copies were annotated as AvTpsB and AvTpsB’ (Fig 1A). One copy (AvTpsB) was characterized by the insertion of an A at position 223 (in comparison with AvTpsB’) generating a stop codon in the translated protein. In AvTpsB’, the substitution of a C by a T at position 766 also resulted in a stop codon and a truncated protein sequence. We scrutinized the corresponding cDNA sequencing dataset and found no evidence for RNA editing (see below), suggesting that these two copies might be pseudogenes and we therefore prefixed their names with the Greek letter Ψ (Fig 1A). In downstream phylogenetic analyses, we restored both genes to their presumable full length by deleting the A in position 223 of ΨAvTpsB and by replacing the T in position 766 of ΨAvTpsB’ by a C.


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.

Hespeels B, Li X, Flot JF, Pigneur LM, Malaisse J, Da Silva C, Van Doninck K - PLoS ONE (2015)

Annotation of the scaffolds containing (a) TPS and (b) TRE genes in Adineta vaga.Color-filled rectangles represent genes, numbers refer to the list at the bottom of the figure. Genes were colored in green or red if AI<45 or AI≥45, respectively. The genes annotated automatically in the A. vaga genome are surrounded with continuous lines, whereas discontinued lines surround additional genes detected during manual curation. The gene orientation is indicated by the position above (forward direction) or below (reverse direction) the line.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4498783&req=5

pone.0131313.g001: Annotation of the scaffolds containing (a) TPS and (b) TRE genes in Adineta vaga.Color-filled rectangles represent genes, numbers refer to the list at the bottom of the figure. Genes were colored in green or red if AI<45 or AI≥45, respectively. The genes annotated automatically in the A. vaga genome are surrounded with continuous lines, whereas discontinued lines surround additional genes detected during manual curation. The gene orientation is indicated by the position above (forward direction) or below (reverse direction) the line.
Mentions: The TBLASTN search results for A. vaga homologues of trehalose phosphate synthase (TPS) from a wide range of species (bacteria, fungi, plants and metazoans) yielded significant E-values (< 10−10) for four predicted genes belonging to three different scaffolds (av51, av255 and av681) in the A. vaga genomic dataset. Indeed, A. vaga was previously reported to be an ancient degenerate tetraploid [39], hence finding more than two copies of a given gene was not surprising. Two TPS genes were found on a palindromic, highly colinear allelic region [39] of scaffold av51, and were annotated AvTpsA and AvTpsA’ (Fig 1A). The surrounding region of the TPS copies on scaffolds av255 and av681 were also highly colinear and therefore probably allelic [39]: these two copies were annotated as AvTpsB and AvTpsB’ (Fig 1A). One copy (AvTpsB) was characterized by the insertion of an A at position 223 (in comparison with AvTpsB’) generating a stop codon in the translated protein. In AvTpsB’, the substitution of a C by a T at position 766 also resulted in a stop codon and a truncated protein sequence. We scrutinized the corresponding cDNA sequencing dataset and found no evidence for RNA editing (see below), suggesting that these two copies might be pseudogenes and we therefore prefixed their names with the Greek letter Ψ (Fig 1A). In downstream phylogenetic analyses, we restored both genes to their presumable full length by deleting the A in position 223 of ΨAvTpsB and by replacing the T in position 766 of ΨAvTpsB’ by a C.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: LEGE laboratory, URBE, Department of Biology, University of Namur, Namur, Belgium.

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.

No MeSH data available.