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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.


Maximum-likelihood phylogenetic tree based on the amino acid sequences available for trehalose-6 phosphate synthase (TPS) domains.The tree displayed was generated using RaxML with 1000 rapid bootstrap according to the model WAG+I+G+. Numbers above the branches are bootstrap support percentages and posterior probability of 1 obtained with MrBayes (See M&M). When the node was not recovered in the Bayesian tree, the bootstrap value was replaced by “-“. Bootstrap support values above 70% for MetaPIGA and NJ are indicated by lines respectively drawn above and below the ML bootstrap values and posterior probabilities*. Color code: green (plant), red (metazoans), black (bacteria and archeae), cyan (protists) and brown (fungi).
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pone.0131313.g003: Maximum-likelihood phylogenetic tree based on the amino acid sequences available for trehalose-6 phosphate synthase (TPS) domains.The tree displayed was generated using RaxML with 1000 rapid bootstrap according to the model WAG+I+G+. Numbers above the branches are bootstrap support percentages and posterior probability of 1 obtained with MrBayes (See M&M). When the node was not recovered in the Bayesian tree, the bootstrap value was replaced by “-“. Bootstrap support values above 70% for MetaPIGA and NJ are indicated by lines respectively drawn above and below the ML bootstrap values and posterior probabilities*. Color code: green (plant), red (metazoans), black (bacteria and archeae), cyan (protists) and brown (fungi).

Mentions: Tree topologies obtained by RaxML, Mr Bayes, Neighbor-Joining and MetaPIGA confirmed that the TPS sequences were grouped into two major branches as previously described by Avonce et al. [33] (Fig 3): the first group contains sequences from fungi, plants and some protists, whereas the second group consists of metazoans and bacteria. The TPS sequences of A. vaga were part of the clade of plant and fungal TPS proteins (strongly supported by bootstrap branch supports of 100-97-84 for RaxML, NJ, and MetaPIGA respectively, and by a posterior probability of 1 using Mr Bayes). The two A. vaga AvTpsA and AvTpsA’ sequences clustered with the protist TPS sequence of P. brassicae (bootstrap supports of 95-76-62, posterior probability of 1) and formed a sister clade to the plant Class I TPS proteins (bootstrap supports of 100-97-87, posterior probability of 1) confirming their non-metazoan origin. Most of these sequences have biochemically proven TPS enzymatic activity, except AtTPS2-AtTPS4 [71]. The position of ΨAvTpsB and ΨAvTpsB’ within the tree was not resolved as the phylogenetic trees were not congruent or branch support was insufficient. In contrast, the TPS sequences of monogonont rotifers (Brachionus manjavacas and Brachionus calyciflorus) grouped outside the plant and fungal clade and were associated with other metazoans (bootstrap support values 100-100-99, posterior probability 1). As previously described in [33], the nematode sequences did not cluster with those of other metazoans.


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)

Maximum-likelihood phylogenetic tree based on the amino acid sequences available for trehalose-6 phosphate synthase (TPS) domains.The tree displayed was generated using RaxML with 1000 rapid bootstrap according to the model WAG+I+G+. Numbers above the branches are bootstrap support percentages and posterior probability of 1 obtained with MrBayes (See M&M). When the node was not recovered in the Bayesian tree, the bootstrap value was replaced by “-“. Bootstrap support values above 70% for MetaPIGA and NJ are indicated by lines respectively drawn above and below the ML bootstrap values and posterior probabilities*. Color code: green (plant), red (metazoans), black (bacteria and archeae), cyan (protists) and brown (fungi).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0131313.g003: Maximum-likelihood phylogenetic tree based on the amino acid sequences available for trehalose-6 phosphate synthase (TPS) domains.The tree displayed was generated using RaxML with 1000 rapid bootstrap according to the model WAG+I+G+. Numbers above the branches are bootstrap support percentages and posterior probability of 1 obtained with MrBayes (See M&M). When the node was not recovered in the Bayesian tree, the bootstrap value was replaced by “-“. Bootstrap support values above 70% for MetaPIGA and NJ are indicated by lines respectively drawn above and below the ML bootstrap values and posterior probabilities*. Color code: green (plant), red (metazoans), black (bacteria and archeae), cyan (protists) and brown (fungi).
Mentions: Tree topologies obtained by RaxML, Mr Bayes, Neighbor-Joining and MetaPIGA confirmed that the TPS sequences were grouped into two major branches as previously described by Avonce et al. [33] (Fig 3): the first group contains sequences from fungi, plants and some protists, whereas the second group consists of metazoans and bacteria. The TPS sequences of A. vaga were part of the clade of plant and fungal TPS proteins (strongly supported by bootstrap branch supports of 100-97-84 for RaxML, NJ, and MetaPIGA respectively, and by a posterior probability of 1 using Mr Bayes). The two A. vaga AvTpsA and AvTpsA’ sequences clustered with the protist TPS sequence of P. brassicae (bootstrap supports of 95-76-62, posterior probability of 1) and formed a sister clade to the plant Class I TPS proteins (bootstrap supports of 100-97-87, posterior probability of 1) confirming their non-metazoan origin. Most of these sequences have biochemically proven TPS enzymatic activity, except AtTPS2-AtTPS4 [71]. The position of ΨAvTpsB and ΨAvTpsB’ within the tree was not resolved as the phylogenetic trees were not congruent or branch support was insufficient. In contrast, the TPS sequences of monogonont rotifers (Brachionus manjavacas and Brachionus calyciflorus) grouped outside the plant and fungal clade and were associated with other metazoans (bootstrap support values 100-100-99, posterior probability 1). As previously described in [33], the nematode sequences did not cluster with those of other metazoans.

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.