The eukaryotic enzyme Bds1 is an alkyl but not an aryl sulfohydrolase

Abstract

The eukaryotic enzyme Bds1 in Saccharomyces cerevisiae is a metallo-β-lactamase-related enzyme evolutionarily originating from bacterial horizontal gene transfer that serves an unknown biological role. Previously, Bds1 was reported to be an alkyl and aryl sulfatase. However, we demonstrate here that Bds1 acts on primary alkyl sulfates (of 6–12 carbon atoms) but not the aryl sulfates p-nitrophenyl sulfate and p-nitrocatechol sulfate. The apparent catalytic rate constant for hydrolysis of the substrate 1-hexyl sulfate by Bds1 is over 100 times lower than that of the reaction catalyzed by its bacterial homolog SdsA1. We show that Bds1 shares a catalytic mechanism with SdsA1 in which the carbon atom of the sulfate ester is the subject of nucleophilic attack, rather than the sulfur atom, resulting in C–O bond lysis. In contrast to SdsA1 and another bacterial homolog with selectivity for secondary alkyl sulfates named Pisa1, Bds1 does not show any substantial activity towards secondary alkyl sulfates. Neither Bds1 nor SdsA1 have any significant activity towards a branched primary alkyl sulfate, primary and secondary steroid sulfates, or phosphate diesters. Therefore, the enzymes homologous to SdsA1 that have been identified and characterized thus far vary in their selectivity towards primary and secondary alkyl sulfates but do not exhibit aryl sulfatase activity.

Structural and Mechanistic Analysis of the Choline Sulfatase from Sinorhizobium melliloti: A Class I Sulfatase Specific for an Alkyl Sulfate Ester

“…The similarity of Sm CS to ASs (in terms of overall structure as well as the catalytic residues) supports the case for for S–O attack and is also consistent with the effect mutations in residues that are conserved between Sm CS and ASs (i.e., all mutants expect E386L, Δ12 and Δ23 as shown in Table 2 ) have on Sm CS-catalyzed conversion of choline- O -sulfate. By contrast, alkylsulfatases known to utilize C–O cleavage do not catalyze the hydrolysis of 4-nitrophenyl sulfate [69] , underlining the diagnostic value of this reaction.…”

Assimilation of alternative sulfur sources in fungi

“…3 Overview of reaction mechanisms for desulfurization of sulfate esters in fungi. Metal ion requirements for each enzyme family are indicated (Hogan et al 1999 ; Korban et al 2017 ; Waddell et al 2017 ) …”

“…The S. cerevisiae Bds1 protein is currently the only fungal enzyme belonging to this family to have been characterized through genetic and biochemical means (Hall et al 2005 ; Waddell et al 2017 ). Bds1 specifically desulfurizes unbranched primary aliphatic sulfate esters, which is thought to occur by hydrolysis of the C–O bond through a nucleophilic attack by an exchangeable water molecule on the carbon atom with subsequent incorporation of the water-derived oxygen atom into the resulting alcohol (Waddell et al 2017 ). The BDS1 gene appears to have been acquired by a fairly recent ancestor of S. cerevisiae through horizontal gene transfer from proteobacteria (Hall et al 2005 ).…”

MaAts, an Alkylsulfatase, Contributes to Fungal Tolerances against UV-B Irradiation and Heat-Shock in Metarhizium acridum

“…In eukaryon, research related to alkylsulfatase is limited. Alkylsulfatases from Saccharomyces cerevisiae surprisingly degrade certain ary-sulfates, and this strain could utilize SDS regarded as a sulfur source to grow [ 44 , 45 , 46 ]. However, the functions of the type III sulfatases in filamentous fungi are still a mystery.…”