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Unique Metabolic Responses to Hypoxia and Nitric Oxide by Filamentous Fungi

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Abstract

To understand fungal metabolism under stress is important for the industrial production of organic acids and enzymes from fungi, and also for traditional large-scale fermentation because inadequately controlled cultures impose stress on fungi that reduces performance efficiency. This chapter describes recent advances in studies of the hypoxic regulation of fungal metabolism. Transcriptome and proteome analyses of the model filamentous fungus Aspergillus nidulans have identified global metabolic changes in carbon source utilization and energy conservation under hypoxia. Insufficient nitrate reduction under hypoxia results in the generation of nitrite or reactive nitrogen species (RNS) that constitute a prevalent nitrogen source for filamentous fungi such as Aspergillus. Fungi have developed novel nitrate reduction mechanisms to survive under hypoxia that are likely to be industrially important because they can generate RNS during fermentation. This chapter also describes recent findings of heme biosynthesis and nitrosothionein that are involved in fungal responses to RNS and detoxification mechanisms.

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Abbreviations

GABA:

γ-Aminobutyric acid

GSNOR:

GSNO reductase

iNT:

Nitrosothionein

Nar:

Nitrate reductase

Nir:

Nitrite reductase

Nor:

NO reductase

PPP:

Pentose phosphate pathway

RNS:

Reactive nitrogen species

TCA:

Tricarboxylic acid TrxR, thioredoxin reductase

References

  • Barker BM, Kroll K, Vödisch M et al (2012) Transcriptomic and proteomic analyses of the Aspergillus fumigatus hypoxia response using an oxygen-controlled fermenter. BMC Genomics 13:62

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Benhar M, Forrester MT, Stamler JS (2009) Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat Rev Mol Cell Biol 10:721–732

    CAS  PubMed  Google Scholar 

  • Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115

    Article  PubMed  Google Scholar 

  • Bunn HF, Poyton RO (1996) Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev 76:839–885

    CAS  PubMed  Google Scholar 

  • Capdevila M, Atrian S (2011) Metallothionein protein evolution: a miniassay. J Biol Inorg Chem 16:977–989

    Article  CAS  PubMed  Google Scholar 

  • Datta PK, Lianos EA (2006) Nitric oxide induces metallothionein-1 gene expression in mesangial cells. Transl Res 148:180–187

    Article  CAS  PubMed  Google Scholar 

  • Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci U S A 99:16314–16318

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Diano A, Peeters J, Dynesen J et al (2009) Physiology of Aspergillus niger in oxygen-limited continuous cultures: influence of aeration, carbon source concentration and dilution rate. Biotechnol Bioeng 103:956–965

    Article  CAS  PubMed  Google Scholar 

  • Fujii T, Takaya N (2008) Denitrification by the fungus Fusarium oxysporum involves NADH-nitrate reductase. Biosci Biotechnol Biochem 72:412–420

    Article  CAS  PubMed  Google Scholar 

  • Gems D, Johnstone IL, Clutterbuck AJ (1991) An autonomously replicating plasmid transforms Aspergillus nidulans at high frequency. Gene 98:61–67

    Article  CAS  PubMed  Google Scholar 

  • Hall LA, Denning DW (1994) Oxygen requirements of Aspergillus species. J Med Microbiol 41:311–315

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Hausladen A, Zeng M et al (2001) A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410:490–494

    Article  CAS  PubMed  Google Scholar 

  • Masuo S, Terabayashi Y, Shimizu M et al (2010) Global gene expression analysis of Aspergillus nidulans reveals metabolic shift and transcription suppression under hypoxia. Mol Gen Genet 284:415–424

    Article  CAS  Google Scholar 

  • Nakahara K, Tanimoto T, Hatano K et al (1993) Cytochrome P-450 55A1 (P450dNIR) acts as nitric oxide reductase employing NADH as direct electron donor. J Biol Chem 268:8350–8355

    CAS  PubMed  Google Scholar 

  • Poole RK (2005) Nitric oxide and nitrosative stress tolerance in bacteria. Biochem Soc Trans 33:176–180

    Article  CAS  PubMed  Google Scholar 

  • Poyton R, Castello P, Ball K et al (2009) Mitochondria and hypoxic signaling. Ann N Y Acad Sci 1177:48–56

    Article  CAS  PubMed  Google Scholar 

  • Shimizu M, Fujii T, Masuo S et al (2009) Proteomic analysis of Aspergillus nidulans cultured under hypoxic conditions. Proteomics 9:7–19

    Article  CAS  PubMed  Google Scholar 

  • Shimizu M, Fujii T, Masuo S et al (2010) Mechanism of de novo branched-chain amino acid synthesis as an alternative electron sink in hypoxic Aspergillus nidulans cells. Appl Environ Microbiol 76:1507–1515

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shoun H, Tanimoto T (1991) Denitrification by the fungus Fusarium oxysporum and involvement of cytochrome P-450 in respiratory nitrate reduction. J Biol Chem 266:11078–11082

    CAS  PubMed  Google Scholar 

  • Takasaki K, Shoun H, Yamaguchi M et al (2004) Fungal ammonia fermentation, a novel metabolic mechanism that couples the dissimilatory and assimilatory pathways of both nitrate and ethanol. J Biol Chem 279:12414–12420

    Article  CAS  PubMed  Google Scholar 

  • Takaya N (2009) Response to hypoxia, reduction of electron acceptors, and subsequent survival by filamentous fungi. Biosci Biotechnol Biochem 73:1–8

    Article  CAS  PubMed  Google Scholar 

  • Terabayashi Y, Shimizu M, Kitazume T et al (2012) Conserved and specific responses to hypoxia in Aspergillus oryzae and Aspergillus nidulans determined by comparative transcriptomics. Appl Microbiol Biotechnol 93:305–317

    Article  PubMed  Google Scholar 

  • Vašák M, Meloni G (2011) Chemistry and biology of mammalian metallothioneins. J Biol Inorg Chem 16:1067–1078

    Article  PubMed  Google Scholar 

  • Vödisch M, Scherlach K, Winkler R et al (2011) Analysis of the Aspergillus fumigatus proteome reveals metabolic changes and the activation of the pseurotin A biosynthesis gene cluster in response to hypoxia. J Proteome Res 10:2508–2524

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhou Z, Takaya N, Nakamura A et al (2002) Ammonia fermentation, a novel anoxic metabolism of nitrate by fungi. J Biol Chem 277:1892–1896

    Article  CAS  PubMed  Google Scholar 

  • Zhou S, Fushinobu S, Kim SW et al (2011) Functional analysis and subcellular location of two flavohemoglobins from Aspergillus oryzae. Fungal Genet Biol 48:200–207

    Article  CAS  PubMed  Google Scholar 

  • Zhou S, Narukami T, Nameki M et al (2012) Heme-biosynthetic porphobilinogen deaminase protects Aspergillus nidulans from nitrosative stress. Appl Environ Microbiol 78:103–109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhou S, Narukami T, Masuo S et al (2013) NO-inducible nitrosothionein mediates NO removal in tandem with thioredoxin. Nat Chem Biol 9:657–663

    Google Scholar 

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Correspondence to Naoki Takaya .

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Masuo, S., Takaya, N. (2015). Unique Metabolic Responses to Hypoxia and Nitric Oxide by Filamentous Fungi. In: Takagi, H., Kitagaki, H. (eds) Stress Biology of Yeasts and Fungi. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55248-2_9

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