Abstract
Sulfate is a well-established sulfur source for fungi; however, in soils sulfonates and sulfate esters, especially choline sulfate, are often much more prominent. Here we show that Saccharomyces cerevisiae YIL166C(SOA1) encodes an inorganic sulfur (sulfate, sulfite and thiosulfate) transporter that also catalyses sulfonate and choline sulfate uptake. Phylogenetic analysis of fungal SOA1 orthologues and expression of 20 members in the sul1Δ sul2Δ soa1Δ strain, which is deficient in inorganic and organic sulfur compound uptake, reveals that these transporters have diverse substrate preferences for sulfur compounds. We further show that SOA2, a S. cerevisiae SOA1 paralogue found in S. uvarum, S. eubayanus and S. arboricola is likely to be an evolutionary remnant of the uncharacterized open reading frames YOL163W and YOL162W. Our work highlights the importance of sulfonates and choline sulfate as sulfur sources in the natural environment of S. cerevisiae and other fungi by identifying fungal transporters for these compounds.
Highlights
Sulfate is a well-established sulfur source for fungi; in soils sulfonates and sulfate esters, especially choline sulfate, are often much more prominent
We have recently shown that both Sul[1] and Sul[2] act as transporter receptors or transceptors for sulfate-induced activation of the protein kinase A (PKA) pathway in sulfur-starved S. cerevisiae cells[20], which prompted us to identify the remaining unknown inorganic sulfur carrier(s)
Phylogenetic analysis reveals that SOA1 belongs to an extensive family of poorly characterized fungal transporters of organic anions, of which some members were suggested to function as sulfonate transporters
Summary
Sulfate is a well-established sulfur source for fungi; in soils sulfonates and sulfate esters, especially choline sulfate, are often much more prominent. We show that Saccharomyces cerevisiae YIL166C(SOA1) encodes an inorganic sulfur (sulfate, sulfite and thiosulfate) transporter that catalyses sulfonate and choline sulfate uptake. Cerevisiae, inorganic sulfur uptake mainly occurs by the high-affinity sulfate H þ -symporters, Sul[1] and Sul[2], which belong to the SulP family and of which the expression is strongly enhanced under sulfur starvation conditions[15,16,17,18] They transport other sulfate esters and sulfite as well[19,20]. We show that the YIL166C gene product is the remaining inorganic sulfur transporter that is responsible for the uptake of sulfite and high levels of sulfate during growth of the sul1D sul2D strain with these compounds as the sole sulfur source. We show that the S. cerevisiae genes, YOL163W and YOL162W, are likely to be evolutionary leftovers from a second sulfonate transporter gene, which we named SOA2, and which is present in an intact form only in the most distantly related Saccharomyces species, whereas it is completely absent in more closely related Saccharomyces species
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