Acid trehalase in yeasts and filamentous fungi: Localization, regulation and physiological function

Abstract

Yeasts and filamentous fungi are endowed with two different trehalose-hydrolysing activities, termed acid and neutral trehalases according to their optimal pH for enzymatic activity. A wealth of information already exists on fungal neutral trehalases, while data on localization, regulation and function of fungal acid trehalases have remained elusive. The gene encoding the latter enzyme has now been isolated from two yeast species and two filamentous fungi, and sequences encoding putative acid trehalase can be retrieved from available public sequences. Despite weak similarities between amino acids sequences, this type of trehalase potentially harbours either a transmembrane segment or a signal peptide at the N-terminal sequence, as deduced from domain prediction algorithms. This feature, together with the demonstration that acid trehalase from yeasts and filamentous fungi is localized at the cell surface, is consistent with its main role in the utilisation of exogenous trehalose as a carbon source. The growth on this disaccharide is in fact pretty effective in most fungi except in Saccharomyces cerevisiae. This yeast species actually exhibits a "Kluyver effect" on trehalose. Moreover, an oscillatory behaviour reminiscent of what is observed in aerobic glucose-limited continuous cultures at low dilution rate is also observed in batch growth on trehalose. Finally, the S. cerevisiae acid trehalase may also participate in the catabolism of endogenous trehalose by a mechanism that likely requires the export of the disaccharide, its extracellular hydrolysis, and the subsequent uptake of the glucose released. Based on these recent findings, we suggest to rename "acid" and "neutral" trehalases as "extracellular" and "cytosolic" trehalases, which is more adequate to describe their localization and function in the fungal cell.

Developmental Cell Fate and Virulence Are Linked to Trehalose Homeostasis in Cryptococcus neoformans

“…The presence of NTH2 is consistent with the fact that fungi often harbor both cytosolic and secreted trehalases with characteristic features: cytosolic trehalases usually contain a calcium binding domain and a single trehalase domain, while secreted trehalases harbor a secretion signal and two trehalase domains (52,53). Through their predicted functional domains and features, NTH1 and NTH2 appear to be the only two genes encoding trehalase activity in the C. neoformans genome; NTH1 is a predicted cytosolic trehalase, and NTH2 is a predicted secreted trehalase (Fig.…”

The Saccharomyces cerevisiae vacuolar acid trehalase is targeted at the cell surface for its physiological function

“…Because the sequenced BY4741 strain is mal-negative, the assimilation of exogenous trehalose can rely only on the Ath1-dependent pathway [14]. Moreover, this model is consistent with what has been shown for fungal and plant acid trehalases, which are all localized at the cell surface or cell wall [22,29,30]. In addition to these data, other results support this model.…”

Physiological implication of intracellular trehalose and mannitol changes in response of entomopathogenic fungus Beauveria bassiana to thermal stress

“…Trehalose is known to be associated with eukaryotic tolerance to a variety of environmental stresses (Fillinger et al 2001;Elbein et al 2003;Parrou et al 2005). However, neither trehalose accumulation nor trehalase activity in fungal cells has been related to the tolerance of the fungal biocontrol agents to the thermal stress (Jorge et al 1997) although factors affecting trehalose accumulation in conidia of three entomopathogenic fungi have been well elucidated Magan 1994, 1996).…”