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

PLoS One. 2015 Jul 10;10(7):e0131313. doi: 10.1371/journal.pone.0131313. eCollection 2015.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Desiccation / methods
  • Gene Dosage
  • Gene Transfer, Horizontal*
  • Glucosyltransferases / classification
  • Glucosyltransferases / genetics*
  • Glucosyltransferases / metabolism
  • Helminth Proteins / genetics*
  • Helminth Proteins / metabolism
  • Metabolic Networks and Pathways
  • Phosphoric Monoester Hydrolases / genetics
  • Phosphoric Monoester Hydrolases / metabolism
  • Phylogeny
  • Reverse Transcriptase Polymerase Chain Reaction
  • Rotifera / enzymology
  • Rotifera / genetics*
  • Transcriptional Activation
  • Trehalase / genetics*
  • Trehalase / metabolism
  • Trehalose / metabolism
  • Up-Regulation*

Substances

  • Helminth Proteins
  • Trehalose
  • Glucosyltransferases
  • trehalose-6-phosphate synthase
  • trehalose-phosphatase
  • Phosphoric Monoester Hydrolases
  • Trehalase

Grants and funding

This work was supported by UNamur through an assistant PhD grant allocated to BH and a starting grant allocated to KVD and by the Belgian National Fund for Scientific Research (Fonds National pour la Recherche Scientifique - FNRS) through a PhD FRIA (Fonds pour la formation à la Recherche dans l'Industrie et dans l'Agriculture) thesis grant allocated to XL and an FRFC (Fonds de la Recherche Fondamentale Collective) grant 2.4.655.09.F and a CDR research grant DAMAGE (19597258) allocated to KVD.