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.

Hyperthermal-driven mass extinctions: killing models during the Permian–Triassic mass extinction

“…They then recover in minutes or hours when exposed to water. Rotifers, tardigrades and most other desiccation-resistant animals and plants possess the disaccharide sugar trehalose [ 55 ], as in certain insects.…”

No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini

“…Functional horizontal gene transfer (fHGT) can bring to a recipient genome new biochemical capacities and contrasts with gradualist evolution of endogenous genes to new function. The bdelloid rotifers Adineta vaga (28) and Adineta ricciae (29) have high levels of fHGT (∼8%), and this has been associated with both their survival as phylogenetically ancient asexuals and their ability to undergo cryptobiosis (28)(29)(30)(31)(32). Different kinds of evidence are required to support claims of doaHGT compared with fHGT.…”

Trehalose metabolism genes render rice white tip nematode, Aphelenchoides besseyi (Nematoda: Aphelenchoididae) resistant to anaerobic environment

“…In most eukaryotes, trehalose is catalysed by three trehalose metabolism enzymes. Trehalose-6-phosphate synthase (TPS) ( Vandesteene et al, 2010 ; Li et al, 2011 ; Sengupta et al, 2011a , b ; Delorge et al, 2015 ) and trehalose-6-phosphate phosphatase (TPP) ( Ponnu et al, 2011 ; Vandesteene et al, 2012 ; Lahiri et al, 2014 ; Yadav et al, 2014 ) are responsible for trehalose synthesis ( Avonce et al, 2010 ); trehalase (TRE) catalyses the hydrolysis of trehalose ( Pellerone et al, 2003 ; Hespeels et al, 2015 ), and regulates the concentration of sugars ( Alabran et al, 1983 ; Behm, 1997 ). It has been reported that trehalose hydrolysis is catalysed by two types of TRE, acid TRE (AT; Dmitryjuk and Zółtowska, 2003 ) and neutral TRE (NT; Londesborough and Varimo, 1984 ).…”

“…A correlation between regulation of trehalose synthesis and survivability of the organism under thermal stress has been established in Candida utilis ( Lahiri et al, 2014 ). However, so far no TPP genes have been identified in A. besseyi or other nematodes ( Pellerone et al, 2003 ; Hespeels et al, 2015 ). For these reasons, the study reported here was restricted to the transcript levels of TRE and TPS genes and the trehalose levels and activity of AT or NT to investigate the trehalose metabolism of A. besseyi under anaerobic conditions.…”