Response to sulfur in Schizosaccharomyces pombe

Abstract

Sulfur is an essential component of various biologically important molecules, including methionine, cysteine and glutathione, and it is also involved in coping with oxidative and heavy metal stress. Studies using model organisms, including budding yeast (Saccharomyces cerevisiae) and fission yeast (Schizosaccharomyces pombe), have contributed not only to understanding various cellular processes but also to understanding the utilization and response mechanisms of each nutrient, including sulfur. Although fission yeast can use sulfate as a sulfur source, its sulfur metabolism pathway is slightly different from that of budding yeast because it does not have a trans-sulfuration pathway. In recent years, it has been found that sulfur starvation causes various cellular responses in S. pombe, including sporulation, cell cycle arrest at G2, chronological lifespan extension, autophagy induction and reduced translation. This MiniReview identifies two sulfate transporters in S. pombe, Sul1 (encoded by SPBC3H7.02) and Sul2 (encoded by SPAC869.05c), and summarizes the metabolic pathways of sulfur assimilation and cellular response to sulfur starvation. Understanding these responses, including metabolism and adaptation, will contribute to a better understanding of the various stress and nutrient starvation responses and chronological lifespan regulation caused by sulfur starvation.

Keywords: Schizosaccharomyces pombe; sul1 +; sul2 +; fission yeast; sulfate; sulfur.

Figure 1.

Sulfur metabolism in budding yeast Saccharomyces cerevisiae and in fission yeast Schizosaccharomyces pombe. Sulfate is used to synthesize cysteine (Cys), methionine (Met) and glutathione (GSH). In the reduction process, sulfate is converted to adenosine 5′-phosphosulfate (adenylyl sulfate; APS), 3′-phosphoadenosine-5′-phosphosulfate (3′-phosphoadenylyl sulfate; PAPS), sulfite (SO₃²⁻) and hydrogen sulfide (H₂S) or sulfide (S²⁻). Cys is used for the synthesis of GSH and Met via γ-Glutamyl-cysteine (γ-Glu-Cys).

Figure 2.

Sulfur metabolism in fission yeast, Schizosaccharomyces pombe. Sulfate taken up by sulfate transporters is used to synthesize cysteine (Cys), methionine (Met) and glutathione (GSH). In the reduction process, sulfate is converted to adenosine 5′-phosphosulfate (adenylyl sulfate; APS), 3′-phosphoadenosine-5′-phosphosulfate (3′-phosphoadenylyl sulfate; PAPS), sulfite (SO₃²⁻) and hydrogen sulfide (H₂S) or sulfide (S²⁻). Cys is used for the synthesis of GSH via γ-Glutamyl-cysteine (γ-Glu-Cys) and for the synthesis of Met via cystathionine and homocysteine. The SPBC3H7.02 protein is denoted as Sul1, and the SPAC869.05c protein is denoted as Sul2. The cystathionine β-lyase encoded by SPCC11E10.01 is referred to here as Cbl1. The at least doubled expression after 3 or 6 h of sulfur starvation is marked with a green circle on the left or right side of each factor, respectively (Ohtsuka et al. 2017). The expression that was suppressed to less than half after 3 or 6 h of sulfur starvation is marked with a red circle on the left or right side of each factor, respectively (Ohtsuka et al. 2017). It has been confirmed that Cys11 and Hmt2 is localized in the mitochondria (Vande Weghe and Ow ; Matsuyama et al. 2006). The broken line indicates expectations. The details of each process are described in the text.

Figure 3.

Schizosaccharomyces pombe responds to sulfur starvation, causing sporulation induction, G₂ arrest, autophagy induction, translational repression and chronological lifespan (CLS) extension.