Skip to main content

12 Regulation of Sulfur Metabolism in Filamentous Fungi

  • Chapter
  • First Online:
Biochemistry and Molecular Biology

Part of the book series: The Mycota ((MYCOTA,volume III))

Abstract

Filamentous fungi provide a useful model for understanding the mechanisms of how organisms adjust to nutrient availability in order to avoid deficiencies of needed macro- and microelements. In particular, sulfur represents an essential low-abundance element that is found in a wide variety of compounds and macromolecules that are necessary for routine cellular functions. A particular focus will be on how filamentous fungi use a complex regulatory network to monitor the cellular sulfur status and respond with appropriate acquisition and/or metabolic remodeling strategies to achieve relatively stable levels. The emphasis here will be on the sulfur regulatory system of Neurospora crassa with included discussion of other fungal species.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adiga PR, Sastry KS, Sarma PS (1962) Amino acid relationships in cysteine toxicity in Neurospora crassa. Gen Microbiol 29:149–155

    Article  CAS  Google Scholar 

  • Amich J, Schafferer L, Haas H, Krappmann S (2013) Regulation of sulphur assimilation is essential for virulence and affects iron homeostasis of the human-pathogenic mould Aspergillus fumigatus. PLoS Pathog 9, e1003573

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Anderson ME, Meister A (1987) Intracellular delivery of cysteine. Methods Enzymol 143:313–325

    Article  CAS  PubMed  Google Scholar 

  • Apodaca G, McKerrow JH (1989) Regulation of Trichophyton rubrum proteolytic activity. Infect Immun 57:3081–3090

    PubMed Central  CAS  PubMed  Google Scholar 

  • Autry AR, Fitzgerald JW (1990) Sulfonate S: a major form of forest soil organic sulfur. Biol Fertil Soils 10:50–56

    CAS  Google Scholar 

  • Bai C, Sen P, Hofmann K, Ma L, Goebl M, Harper JW, Elledge SJ (1996) SKP 1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86:263–274

    Article  CAS  PubMed  Google Scholar 

  • Baudouin-Cornu P, Surdin-Kerjan Y, Marliere P, Thomas D (2001) Molecular evolution of protein atomic composition. Science 293:297–300

    Article  CAS  PubMed  Google Scholar 

  • Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, Seiler S, Bell-Pederson D, Paietta JV, Plesofsky N, Plamann M, Goodrich-Tanrikulu M, Schulte U, Mannhaupt G, Nargang FE, Radford A, Selitrennikoff C, Galagan JE, Dunlap JC, Loros JJ, Catcheside D, Inoue H, Aramayo R, Polymenis M, Selker EU, Sachs MS, Marzluf GA, Paulsen I, Davis R, Ebbole DJ, Zelter A, Kalkman ER, O’Rourke R, Bowring F, Yeadon J, Ishii C, Suzuki K, Sakai W, Pratt R (2004) Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68:1–108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brzywczy J, Kacprzak MM, Paszewski A (2011) Novel mutations reveal two important regions in Aspergillus nidulans transcriptional activator MetR. Fungal Genet Biol 48:104–112

    Article  CAS  PubMed  Google Scholar 

  • Burton EG, Metzenberg RL (1972) Novel mutation causing derepression of several enzymes of sulfur metabolism of several enzymes of sulfur metabolism in Neurospora crassa. J Bacteriol 109:140–151

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bykowski T, van der Ploeg JR, Iwanicka-Nowicka R, Hryniewicz MM (2002) The switch from inorganic sulphur assimilation in Escherichia coli: adenosine 5’-phosphosulphate (APS) as a signaling molecule for sulphate excess. Mol Microbiol 43:1347–1358

    Article  CAS  PubMed  Google Scholar 

  • Carrillo E, Ben-Ari G, Wildenhain J, Tyers M, Grammentz D, Lee TA (2012) Characterizing the roles of Met31 and Met32 in coordinating Met4-activated transcription in the absence of Met30. Mol Biol Cell 23:1928–1942

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Coulter KR, Marzluf GA (1998) Functional analysis of different regions of the positive-acting CYS3 regulatory protein of Neurospora crassa. Curr Genet 33:395–405

    Article  CAS  PubMed  Google Scholar 

  • Craig KL, Tyers M (1999) The F-Box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog Biophys Mol Biol 72:299–328

    Article  CAS  PubMed  Google Scholar 

  • Davies JP, Yildiz FH, Grossman AR (1999) SACl, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15:2150–2159

    Google Scholar 

  • Davis RH (2000) Neurospora. Contributions of a model organism. Oxford Press, Oxford

    Google Scholar 

  • Davis RH, Perkins DD (2002) Neurospora: a model of model microbes. Nat Rev Genet 3:397–403

    Article  CAS  PubMed  Google Scholar 

  • Fauchon M, Lagniel G, Aude J-C, Lombardis L, Soularue P, Petat C, Marguerie G, Senenac A, Werner M, Labarre J (2002) Sulfur sparing in the yeast proteome in response to sulfur demand. Mol Cell 9:713–723

    Article  CAS  PubMed  Google Scholar 

  • Ferreira MED, Marques ED, Malavazi I, Torres I, Restrepo A, Numes LR, deOliveira RC, Goldman MHS, Goldman GH (2006) Transcriptome analysis and molecular studies on sulfur metabolism in the human pathogenic fungus Paracoccidioides brasiliensis. Mol Gen Genomics 276:450–463

    Article  CAS  Google Scholar 

  • Gonzalez-Ballester D, Pollock SV, Pootakham W, Grossman AR (2008) The central role of a SNRK2 kinase in sulfur deprivation responses. Plant Physiol 147:216–227

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goodwin PH, Li J, Jin SM (2000) Evidence for sulfate derepression of an arylsulfatase gene of Colletotrichum gloeosporioides f. sp malvae during infection of round-leaved mallow, Malva pusilla. Physiol Mol Plant Pathol 57:169–176

    Article  CAS  Google Scholar 

  • Hansen J, Johannesen PF (2000) Cysteine is essential for transcriptional regulation of the sulfur assimilation genes in Saccharomyces cerevisiae. Mol Gen Genet 263:535–542

    Article  CAS  PubMed  Google Scholar 

  • Hanson MA, Marzluf GA (1975) Control of the synthesis of a single enzyme by multiple regulatory circuits in Neurospora crassa. Proc Natl Acad Sci USA 72:1240–1244

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Holland SL, Avery SV (2011) Chromate toxicity and the role of sulfur. Metallomics 3:1119–1123

    Article  CAS  PubMed  Google Scholar 

  • Jacobson ES, Metzenberg RL (1977) Control of arylsulfatase in a serine auxotroph of Neurospora. J Bacteriol 130:1397–1398

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jonkers W, Rep M (2009) Lessons from fungal F-box proteins. Eukaryot Cell 8:677–695

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kipreos ET, Pagano M (2000) The F-box protein family. Genome Biol 1:3002.1–3002.7

    Article  Google Scholar 

  • Kumar A, Paietta JV (1995) The sulfur controller-2 negative regulatory gene of Neurospora crassa encodes a protein with β-transducin repeats. Proc Natl Acad Sci U S A 92:3343–3347

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kumar A, Paietta JV (1998) An additional role for the F-box motif: gene regulation within the Neurospora crassa sulfur control network. Proc Natl Acad Sci USA 95:2417–2422

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kuras L, Cherest H, Surdin-Kerjan Y, Thomas D (1996) A heteromeric complex containing the centromere binding factor 1 and two basic leucine zipper factors, met4 and me28, mediates the transcription activation of yeast sulfur metabolism. EMBO J 15:2519–2529

    PubMed Central  CAS  PubMed  Google Scholar 

  • Laxman S, Sutter BM, Wu X, Kumar S, Guo X, Trudgian DC, Mirzaei H, Tu BP (2013) Sulfur amino acids regulated translational capacity and metabolic homeostasis through modulation of tRNA thiolation. Cell 154:416–429

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leustak T, Martin MN, Bick J-A, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51:141–146

    Article  Google Scholar 

  • Li Q, Marzluf GA (1996) Determination of the Neurospora crassa CYS3 sulfur regulatory protein consensus DNA-binding site: amino acid substitutions in the CYS3 bZIP domain that alter DNA-binding specificity. Curr Genet 30:298–304

    Article  CAS  PubMed  Google Scholar 

  • Linder T (2012) Genomics of alternative sulfur utilization in ascomycetous yeasts. Microbiology 158:2585–2597

    Article  CAS  PubMed  Google Scholar 

  • Lochowska A, Iwanicka-Nowicka R, Plochocka D, Hryniewica MM (2001) Functional dissection of the LysR-type CysB transcriptional regulator. Regions important for DNA binding, inducer response, oligomerization, and positive control. J Biol Chem 276:2098–2107

    Article  CAS  PubMed  Google Scholar 

  • Marzluf GA (1970) Genetic and metabolic controls for sulfate metabolism in Neurospora crassa: isolation and study of chromate-resistant and sulfate transport negative mutants. J Bacteriol 102:716–721

    PubMed Central  CAS  PubMed  Google Scholar 

  • Marzluf GA (1994) Genetics and molecular genetics of sulfur assimilation in the fungi. Adv Genet 31:187–206

    Article  CAS  PubMed  Google Scholar 

  • Marzluf GA (1997) Molecular genetics of sulfur assimilation in filamentous fungi and yeast. Annu Rev Microbiol 51:73–96

    Article  CAS  PubMed  Google Scholar 

  • McGuire WG, Marzluf GA (1974) Developmental regulation of choline sulfatase and arylsulfatase in Neurospora crassa. Arch Biochim Biophys 161:360–368

    Article  CAS  Google Scholar 

  • McIsaac RS, Petti AA, Bussemaker HJ, Botstein D (2012) Perturbation-based analysis and modeling of combinatorial regulation in the yeast sulfur assimilation pathway. Mol Biol Cell 23:2993–3007

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Natorff R, Balinska M, Paszewski A (1993) At least four regulatory genes control sulphur metabolite repression in Aspergillus nidulans. Mol Gen Genet 238:185–192

    CAS  PubMed  Google Scholar 

  • Natorff R, Piotrowska M, Paszewski A (1998) The Aspergillus nidulans sulphur regulatory gene sconB encodes a protein with WD40 repeats and an F-box. Mol Gen Genet 257:255–263

    Article  CAS  PubMed  Google Scholar 

  • Natorff R, Sienko M, Brzywczy J, Paszewski A (2003) The Aspergillus nidulans metR gene encodes a bZIP protein which activates transcription of sulphur metabolism genes. Mol Microbiol 49:1081–1094

    Article  CAS  PubMed  Google Scholar 

  • Ono B, Kijima K, Ishii N, Kawato T, Matsuda A, Paszewski A, Shinoda S (1996) Regulation of sulphate assimilation in Saccharomyces cerevisiae. Yeast 12:1153–1162

    Article  CAS  PubMed  Google Scholar 

  • Ono B, Hazu T, Yoshida S, Kawato T, Shinoda S, Brzvwczy J, Paszewski A (1999) Cysteine biosynthesis in Saccharomyces cerevisiae: a new outlook on pathway and regulation. Yeast 15:1365–1375

    Article  CAS  PubMed  Google Scholar 

  • Paietta JV (1989) Molecular cloning and regulatory analysis of the arylsulfatase structural gene of Neurospora crassa. Mol Cell Biol 9:3630–3637

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paietta JV (1990) Molecular cloning and analysis of the scon-2 negative regulatory gene of Neurospora crassa. Mol Cell Biol 10:5207–5214

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paietta JV (1992) Production of the CYS3 regulator, a bZIP DNA-binding protein is sufficient to induce sulfur gene expression in Neurospora crassa. Mol Cell Biol 12:1568–1577

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paietta JV (1995) Analysis of CYS3 regulator function in Neurospora crassa by modification of leucine zipper dimerization specificity. Nucleic Acids Res 23:1044–1049

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paietta JV (2000) Regulation of sulfur metabolism in Neurospora crassa. Fungal Genet Newslett 47S:8

    Google Scholar 

  • Paietta JV (2004) Regulation of sulfur metabolism in mycelial fungi. In: Esser K (ed) The Mycota III. Biochemistry and molecular biology (2nd edn). [Brambl R, Marzluf GA (eds)]. Springer, Berlin, pp. 369–383

    Google Scholar 

  • Paietta JV (2008) DNA-binding specificity of the CYS3 transcription factor of Neurospora crassa defined by binding-site selection. Fungal Genet Biol 45:1166–1171

    Article  CAS  PubMed  Google Scholar 

  • Paietta JV (2010) Sulfur, phosphorus and iron metabolism. In: Borkovich KA, Ebbole DJ (eds) Cellular and molecular biology of filamentous fungi. ASM Press, Washington, DC, pp 359–375

    Chapter  Google Scholar 

  • Paietta JV, Akins RA, Lambowitz AM, Marzluf GA (1987) Molecular cloning and characterization of the cys-3 regulatory gene of Neurospora crassa. Mol Cell Biol 7:2506–2511

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pall ML, Robertson CK (1988) Growth-regulation by GTP: regulation of nucleotide pools in Neurospora by nitrogen and sulfur control systems. J Biol Chem 263:11168–11174

    CAS  PubMed  Google Scholar 

  • Paszewski A, Natorff R, Piotrowska M, Brywczy J, Sienko M, Grynberg M, Pizzinini E, Turner G (2000) Regulation of sulfur amino acid biosynthesis in Aspergillus nidulans: physiological and genetic aspects. In: Brunhold C, Rennenberg H, De Kok LJ, Stulen I, Davidian J-C (eds) Sulfur nutrition and sulfur assimilation in higher plants. Paul Haupt, Bern, pp 93–105

    Google Scholar 

  • Patton EE, Willems AR, Tyers M (1998) Combinatorial control in ubiquitin-dependent proteolysis: don’t skp the F-box hypothesis. Trends Genet 14:236–243

    Article  CAS  PubMed  Google Scholar 

  • Piotrowska M, Natorff R, Paszewski A (2000) sconC, a gene involved in the regulation of sulphur metabolism in Aspergillus nidulans, belongs to the SKP1 gene family. Mol Gen Genet 264:276–282

    Article  CAS  PubMed  Google Scholar 

  • Reveal BS, Paietta JV (2012) Analysis of the sulfur-regulated control of the cystathionine γ-lyase gene of Neurospora crassa. BMC Res Notes 5:339

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reveal BS, Paietta JV (2013) Sulfur-regulated control of the met-2+ gene of Neurospora crassa encoding cystathionine β-lyase. BMC Res Notes 6:259

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Scheibel T, Bell S, Walke S (1997) S. cerevisiae and sulfur: a unique way to deal with the environment. FASEB J 11:917–921

    CAS  PubMed  Google Scholar 

  • Scott WA, Metzenberg RL (1970) Location of arylsulfatase in conidia and young mycelia of Neurospora crassa. J Bacteriol 104:1254–1265

    PubMed Central  CAS  PubMed  Google Scholar 

  • Shuler JL (1993) Analysis of the DNA binding of the Neurospora crassa CYS3 sulfur regulatory protein to the ars-1 + and cys-3 + promoters and determination of the consensus binding site sequence. PhD Thesis. Wright State University, Dayton

    Google Scholar 

  • Sizemore ST, Paietta JV (2002) Cloning and characterization of scon-3 +: a new member of the Neurospora crassa sulfur regulatory system. Eukaryot Cell 1:875–883

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Skowyra D, Craig KL, Tyers M, Elledge SJ, Harper JW (1997) F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209–219

    Article  CAS  PubMed  Google Scholar 

  • Sohn MJ, Yoo SJ, Oh DB, Kwon O, Lee SY, Sibirny AA, Kang HA (2014) Novel cysteine-centered sulfur metabolic pathway in the thermotolerant methyltrophic yeast Hansenula polymorpha. PLoS One 24, e100725

    Article  Google Scholar 

  • Tao Y, Marzluf GA (1998) Synthesis and differential turnover of the CYS3 regulatory protein of Neurospora crassa are subject to sulfur control. J Bacteriol 180:478–482

    PubMed Central  CAS  PubMed  Google Scholar 

  • Thomas D, Surdin-Kerjan Y (1997) Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 61:503–532

    PubMed Central  CAS  PubMed  Google Scholar 

  • Thomas D, Kuras L, Barbey R, Cherest H, Blaiseau P-L, Surdin-Kerjan Y (1995) Met30p, a yeast transcriptional inhibitor that responds to S-adenosylmethionine, is an essential protein with WD40 repeats. Mol Cell Biol 15:6526–6534

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Uthman A, Dockal M, Soltz-Szots J, Tschachler E (2005) Fluconazole upregulates sconc expression and inhibits sulphur metabolism in Microsporum canis. Fungal Genet Biol 42:719–725

    Article  CAS  PubMed  Google Scholar 

  • Van de Kamp M, Schuurs TA, Vos A, van der Lende TR, Konings WN, Driessen AJM (2000) Sulfur regulation of the sulfate transporter genes sutA and sutB in Penicillium chrysogenum. Appl Environ Microbiol 66:4536–4538

    Article  PubMed Central  PubMed  Google Scholar 

  • Zheng N, Schulman BA, Song L, Miller JJ, Jeffrey PD, Wang P, Chu C, Koepp DM, Elledge SM, Pagano M, Conaway RC, Conaway JW, Harper JW, Pavletich NP (2002) Structure of the Cul l-Rbx l-Skp l-F boxskp2 SCF ubiquitin ligase complex. Nature 416:703–709

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John V. Paietta .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Paietta, J.V. (2016). 12 Regulation of Sulfur Metabolism in Filamentous Fungi. In: Hoffmeister, D. (eds) Biochemistry and Molecular Biology. The Mycota, vol III. Springer, Cham. https://doi.org/10.1007/978-3-319-27790-5_12

Download citation

Publish with us

Policies and ethics