Abstract
This chapter deals with differences among fungi to solve specific metabolic problems. Although metabolic studies have mainly been performed on Ascomycetes, it is shown that even closely related species developed different solutions to cope with specific nutritional conditions. Especially, fungal morphology (yeast versus hyphae), the natural nutritional niches, gene loss and acquisition and organismal interaction led to a very large variety of metabolic pathways. To exemplify these variations, an emphasis is given on the degradation of the toxic metabolic intermediate propionyl-CoA, the difference in utilisation of gluconeogenic nutrient sources among yeasts and filamentous fungi, the ability of using histidine as a nitrogen source and the biosynthesis of the amino acid lysine that also provides the essential precursor alpha-aminoadipate for synthesis of penicillins and cephalosporins.
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References
Abdeljalil S et al (2013) Improvement of cellulase and xylanase production by solid-state fermentation of Stachybotrys microspora. Biotechnol Appl Biochem. doi: 10.1002/bab.1195
Alam S, Shah HU, Magan N (2010) Effect of calcium propionate and water activity on growth and aflatoxins production by Aspergillus flavus. J Food Sci 75:M61–M64
Alifano P et al (1996) Histidine biosynthetic pathway and genes: structure, regulation, and evolution. Microbiol Rev 60:44–69
Aschenbach JR, Kristensen NB, Donkin SS, Hammon HM, Penner GB (2010) Gluconeogenesis in dairy cows: the secret of making sweet milk from sour dough. IUBMB Life 62:869–877
Bajmoczi M, Sneve M, Eide DJ, Drewes LR (1998) TAT1 encodes a low-affinity histidine transporter in Saccharomyces cerevisiae. Biochem Biophys Res Commun 243:205–209
Balestrini R, Bonfante P (2014) Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism. Front Plant Sci 5:237
Ballhausen D, Mittaz L, Boulat O, Bonafe L, Braissant O (2009) Evidence for catabolic pathway of propionate metabolism in CNS: expression pattern of methylmalonyl-CoA mutase and propionyl-CoA carboxylase alpha-subunit in developing and adult rat brain. Neuroscience 164:578–587
Baudin A, Ozier-Kalogeropoulos O, Denouel A, Lacroute F, Cullin C (1993) A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res 21:3329–3330
Berger H et al (2008) Dissecting individual steps of nitrogen transcription factor cooperation in the Aspergillus nidulans nitrate cluster. Mol Microbiol 69:1385–1398
Betzel C et al (2001) Structure of a serine protease proteinase K from Tritirachium album limber at 0.98 A resolution. Biochemistry 40:3080–3088
Bigner DR, Goff JP, Faust MA, Tyler HD, Horst RL (1997) Comparison of oral sodium compounds for the correction of acidosis. J Dairy Sci 80:2162–2166
Brock M (2009) Fungal metabolism in host niches. Curr Opin Microbiol 12:371–376
Brock M, Buckel W (2004) On the mechanism of action of the antifungal agent propionate. Eur J Biochem 271:3227–3241
Brock M, Fischer R, Linder D, Buckel W (2000) Methylcitrate synthase from Aspergillus nidulans: implications for propionate as an antifungal agent. Mol Microbiol 35:961–973
Brock M, Darley D, Textor S, Buckel W (2001) 2-Methylisocitrate lyases from the bacterium Escherichia coli and the filamentous fungus Aspergillus nidulans: characterization and comparison of both enzymes. Eur J Biochem 268:3577–3586
Brock M, Maerker C, Schutz A, Volker U, Buckel W (2002) Oxidation of propionate to pyruvate in Escherichia coli. Involvement of methylcitrate dehydratase and aconitase. Eur J Biochem 269:6184–6194
Brunke S et al (2014) Histidine degradation via an aminotransferase increases the nutritional flexibility of Candida glabrata. Eukaryot Cell 13:758–765
Buchholz K, Collins J (2013) The roots--a short history of industrial microbiology and biotechnology. Appl Microbiol Biotechnol 97:3747–3762
Bulfer SL, Brunzelle JS, Trievel RC (2013) Crystal structure of Saccharomyces cerevisiae Aro8, a putative alpha-aminoadipate aminotransferase. Protein Sci 22:1417–1424
Chi Z, Chi Z, Liu G, Wang F, Ju L, Zhang T (2009) Saccharomycopsis fibuligera and its applications in biotechnology. Biotechnol Adv 27:423–431
Chittori S, Simanshu DK, Savithri HS, Murthy MR (2010) Preliminary X-ray crystallographic analysis of 2-methylcitrate synthase from Salmonella typhimurium. Acta Crystallogr Sect F: Struct Biol Cryst Commun 66:467–470
Coblentz WK, Coffey KP, Young AN, Bertram MG (2013) Storage characteristics, nutritive value, energy content, and in vivo digestibility of moist, large rectangular bales of alfalfa-orchardgrass hay treated with a propionic acid-based preservative. J Dairy Sci 96:2521–2535
Creighton DJ, Murthy NSRK (1990) Stereospecificity in enzymatic reactions. In: Sigman DS, Boyer PD (eds) The enzymes, 3rd edn. Academic, San Diego
Crittenden PD, Davis JC, Hawksworth DL, Campbell FS (1995) Attempted isolation and success in culturing of a broad spectrum of lichen forming and lichenicolous fungi. New Phytol 130:267–297
Cruz AH et al (2011) Phosphorylation is the major mechanism regulating isocitrate lyase activity in Paracoccidioides brasiliensis yeast cells. FEBS J 278:2318–2332
Cuomo CA et al (2012) Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res 22:2478–2488
Davis MA, Askin MC, Hynes MJ (2005) Amino acid catabolism by an areA-regulated gene encoding an L-amino acid oxidase with broad substrate specificity in Aspergillus nidulans. Appl Environ Microbiol 71:3551–3555
De Lucas JR, Gregory S, Turner G (1994a) Analysis of the regulation of the Aspergillus nidulans acuD gene, encoding isocitrate lyase, by construction of a hybrid promoter. Mol Gen Genet 243:654–659
De Lucas JR, Valenciano S, Laborda F, Turner G (1994b) Glucose-induced inactivation of isocitrate lyase in Aspergillus nidulans. Arch Microbiol 162:409–413
De Vit MJ, Waddle JA, Johnston M (1997) Regulated nuclear translocation of the Mig1 glucose repressor. Mol Biol Cell 8:1603–1618
Domin N, Wilson D, Brock M (2009) Methylcitrate cycle activation during adaptation of Fusarium solani and Fusarium verticillioides to propionyl-CoA-generating carbon sources. Microbiology 155:3903–3912
Dunn MF, Ramirez-Trujillo JA, Hernandez-Lucas I (2009) Major roles of isocitrate lyase and malate synthase in bacterial and fungal pathogenesis. Microbiology 155:3166–3175
Emmanuel B, Kennelly JJ (1984) Effect of propionic acid on ketogenesis in lactating sheep fed restricted rations or deprived of food. J Dairy Sci 67:344–350
Fazius F, Shelest E, Gebhardt P, Brock M (2012) The fungal alpha-aminoadipate pathway for lysine biosynthesis requires two enzymes of the aconitase family for the isomerization of homocitrate to homoisocitrate. Mol Microbiol 86:1508–1530
Fazius F, Zaehle C, Brock M (2013) Lysine biosynthesis in microbes: relevance as drug target and prospects for beta-lactam antibiotics production. Appl Microbiol Biotechnol 97:3763–3772
Fellbaum CR et al (2014) Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol 203:646–656
Feller A, Ramos F, Pierard A, Dubois E (1999) In Saccharomyces cerevisae, feedback inhibition of homocitrate synthase isoenzymes by lysine modulates the activation of LYS gene expression by Lys14p. Eur J Biochem 261:163–170
Free SJ (2013) Fungal cell wall organization and biosynthesis. Adv Genet 81:33–82
Gangloff SP, Marguet D, Lauquin GJ (1990) Molecular cloning of the yeast mitochondrial aconitase gene (ACO1) and evidence of a synergistic regulation of expression by glucose plus glutamate. Mol Cell Biol 10:3551–3561
Garcia I, Gonzalez R, Gomez D, Scazzocchio C (2004) Chromatin rearrangements in the prnD-prnB bidirectional promoter: dependence on transcription factors. Eukaryot Cell 3:144–156
Garvey GS, Rocco CJ, Escalante-Semerena JC, Rayment I (2007) The three-dimensional crystal structure of the PrpF protein of Shewanella oneidensis complexed with trans-aconitate: insights into its biological function. Protein Sci 16:1274–1284
Gonzalez R, Gavrias V, Gomez D, Scazzocchio C, Cubero B (1997) The integration of nitrogen and carbon catabolite repression in Aspergillus nidulans requires the GATA factor AreA and an additional positive-acting element, ADA. EMBO J 16:2937–2944
Graybill ER, Rouhier MF, Kirby CE, Hawes JW (2007) Functional comparison of citrate synthase isoforms from S. cerevisiae. Arch Biochem Biophys 465:26–37
Grimek TL, Escalante-Semerena JC (2004) The acnD genes of Shewenella oneidensis and Vibrio cholerae encode a new Fe/S-dependent 2-methylcitrate dehydratase enzyme that requires prpF function in vivo. J Bacteriol 186:454–462
Gropp K, Schild L, Schindler S, Hube B, Zipfel PF, Skerka C (2009) The yeast Candida albicans evades human complement attack by secretion of aspartic proteases. Mol Immunol 47:465–475
Halarnkar PP, Blomquist GJ (1989) Comparative aspects of propionate metabolism. Comp Biochem Physiol B 92:227–231
Hazelwood LA, Daran JM, van Maris AJ, Pronk JT, Dickinson JR (2008) The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl Environ Microbiol 74:2259–2266
Hers HG, Hue L (1983) Gluconeogenesis and related aspects of glycolysis. Annu Rev Biochem 52:617–653
Hori C et al (2013) Genomewide analysis of polysaccharides degrading enzymes in 11 white- and brown-rot Polyporales provides insight into mechanisms of wood decay. Mycologia 105:1412–1427
Horie A et al (2009) Discovery of proteinaceous N-modification in lysine biosynthesis of Thermus thermophilus. Nat Chem Biol 5:673–679
Horswill AR, Escalante-Semerena JC (2001) In vitro conversion of propionate to pyruvate by Salmonella enterica enzymes: 2-methylcitrate dehydratase (PrpD) and aconitase enzymes catalyze the conversion of 2-methylcitrate to 2-methylisocitrate. Biochemistry 40:4703–4713
Hudson AO et al (2005) Biosynthesis of lysine in plants: evidence for a variant of the known bacterial pathways. Biochim Biophys Acta 1721:27–36
Hutton CA, Perugini MA, Gerrard JA (2007) Inhibition of lysine biosynthesis: an evolving antibiotic strategy. Mol Biosyst 3:458–465
Hynes MJ, Murray SL (2010) ATP-citrate lyase is required for production of cytosolic acetyl coenzyme A and development in Aspergillus nidulans. Eukaryot Cell 9:1039–1048
Irvin SD, Bhattacharjee JK (1998) A unique fungal lysine biosynthesis enzyme shares a common ancestor with tricarboxylic acid cycle and leucine biosynthetic enzymes found in diverse organisms. J Mol Evol 46:401–408
Jacobsen ID, Lüttich A, Kurzai O, Hube B, Brock M (2014) In vivo imaging of disseminated murine Candida albicans infection reveals unexpected host sites of fungal persistence during antifungal therapy. J Antimicrob Chemother 69(10):2785–96
Jiang W, Nakayama Y, Sequeira JM, Quadros EV (2013) Mapping the functional domains of TCblR/CD320, the receptor for cellular uptake of transcobalamin-bound cobalamin. FASEB J 27:2988–2994
Kanamasa S, Dwiarti L, Okabe M, Park EY (2008) Cloning and functional characterization of the cis-aconitic acid decarboxylase (CAD) gene from Aspergillus terreus. Appl Microbiol Biotechnol 80:223–229
Klement T, Buchs J (2013) Itaconic acid – a biotechnological process in change. Bioresour Technol 135:422–431
Kmetzsch L et al (2011) The GATA-type transcriptional activator Gat1 regulates nitrogen uptake and metabolism in the human pathogen Cryptococcus neoformans. Fungal Genet Biol 48:192–199
Kobayashi K, Hattori T, Honda Y, Kirimura K (2013) Gene identification and functional analysis of methylcitrate synthase in citric acid-producing Aspergillus niger WU-2223L. Biosci Biotechnol Biochem 77:1492–1498
Kulis-Horn RK, Persicke M, Kalinowski J (2014) Histidine biosynthesis, its regulation and biotechnological application in Corynebacterium glutamicum. Microb Biotechnol 7:5–25
Kumar VP, West AH, Cook PF (2012) Supporting role of lysine 13 and glutamate 16 in the acid-base mechanism of saccharopine dehydrogenase from Saccharomyces cerevisiae. Arch Biochem Biophys 522:57–61
Lauble H, Stout CD (1995) Steric and conformational features of the aconitase mechanism. Proteins 22:1–11
Ledley FD, Crane AM, Klish KT, May GS (1991) Is there methylmalonyl CoA mutase in Aspergillus nidulans? Biochem Biophys Res Commun 177:1076–1081
Lin Y, West AH, Cook PF (2009) Site-directed mutagenesis as a probe of the acid-base catalytic mechanism of homoisocitrate dehydrogenase from Saccharomyces cerevisiae. Biochemistry 48:7305–7312
Liu S, Lu Z, Han Y, Melamud E, Dunaway-Mariano D, Herzberg O (2005) Crystal structures of 2-methylisocitrate lyase in complex with product and with isocitrate inhibitor provide insight into lyase substrate specificity, catalysis and evolution. Biochemistry 44:2949–2962
Lopez-Rituerto E, Avenoza A, Busto JH, Peregrina JM (2013) NMR study of histidine metabolism during alcoholic and malolactic fermentations of wine and their influence on histamine production. J Agric Food Chem 61:9464–9469
Maerker C, Rohde M, Brakhage AA, Brock M (2005) Methylcitrate synthase from Aspergillus fumigatus. Propionyl-CoA affects polyketide synthesis, growth and morphology of conidia. FEBS J 272:3615–3630
Marin S et al (1999) Control of growth and fumonisin B1 production by Fusarium verticillioides and Fusarium proliferatum isolates in moist maize with propionate preservatives. Food Addit Contam 16:555–563
Müller S, Fleck CB, Wilson D, Hummert C, Hube B, Brock M (2011) Gene acquisition, duplication and metabolic specification: the evolution of fungal methylisocitrate lyases. Environ Microbiol 13:1534–1548
Nehls U, Grunze N, Willmann M, Reich M, Kuster H (2007) Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. Phytochemistry 68:82–91
Nevoigt E (2008) Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol Mol Biol Rev 72:379–412
Nierman WC, May G, Kim HS, Anderson MJ, Chen D, Denning DW (2005) What the Aspergillus genomes have told us. Med Mycol 43(Suppl 1):S3–S5
Nishida H, Nishiyama M (2012) Evolution of lysine biosynthesis in the phylum Deinococcus-Thermus. Int J Evol Biol 2012:745931
Otzen C, Bardl B, Jacobsen ID, Nett M, Brock M (2014) Candida albicans utilizes a modified beta-oxidation pathway for the degradation of toxic propionyl-CoA. J Biol Chem 289:8151–8169
Papagianni M (2007) Advances in citric acid fermentation by Aspergillus niger: biochemical aspects, membrane transport and modeling. Biotechnol Adv 25:244–263
Peraza-Reyes L, Berteaux-Lecellier V (2013) Peroxisomes and sexual development in fungi. Front Physiol 4:244
Pink DB et al (2011) Lysine alpha-ketoglutarate reductase, but not saccharopine dehydrogenase, is subject to substrate inhibition in pig liver. Nutr Res 31:544–554
Polkinghorne MA, Hynes MJ (1982) L-histidine utilization in Aspergillus nidulans. J Bacteriol 149:931–940
Pronk JT, van der Linden-Beuman A, Verduyn C, Scheffers WA, van Dijken JP (1994) Propionate metabolism in Saccharomyces cerevisiae: implications for the metabolon hypothesis. Microbiology 140(Pt 4):717–722
Quezada H et al (2011) The Lys20 homocitrate synthase isoform exerts most of the flux control over the lysine synthesis pathway in Saccharomyces cerevisiae. Mol Microbiol 82:578–590
Schöbel F, Jacobsen ID, Brock M (2010) Evaluation of lysine biosynthesis as an antifungal drug target: biochemical characterization of Aspergillus fumigatus homocitrate synthase and virulence studies. Eukaryot Cell 9:878–893
Sekito T, Chardwiriyapreecha S, Sugimoto N, Ishimoto M, Kawano-Kawada M, Kakinuma Y (2014) Vacuolar transporter Avt4 is involved in excretion of basic amino acids from the vacuoles of Saccharomyces cerevisiae. Biosci Biotechnol Biochem 78:969–975
Soontorngun N et al (2012) Genome-wide location analysis reveals an important overlap between the targets of the yeast transcriptional regulators Rds2 and Adr1. Biochem Biophys Res Commun 423:632–637
Steiger MG, Blumhoff ML, Mattanovich D, Sauer M (2013) Biochemistry of microbial itaconic acid production. Front Microbiol 4:23
Stocker-Wörgötter E (2008) Metabolic diversity of lichen-forming ascomycetous fungi: culturing, polyketide and shikimate metabolite production, and PKS genes. Nat Prod Rep 25:188–200
Strauss J, Horvath HK, Abdallah BM, Kindermann J, Mach RL, Kubicek CP (1999) The function of CreA, the carbon catabolite repressor of Aspergillus nidulans, is regulated at the transcriptional and post-transcriptional level. Mol Microbiol 32:169–178
Suzuki Y, Murray SL, Wong KH, Davis MA, Hynes MJ (2012) Reprogramming of carbon metabolism by the transcriptional activators AcuK and AcuM in Aspergillus nidulans. Mol Microbiol 84:942–964
Tabuchi T, Hara S (1974) Production of 2-methylisocitric acid from n-paraffins by mutants of Candida lipolytica. Agric Biol Chem 38:1105–1106
Tabuchi T, Uchiyama H (1975) Methylcitrate condensing and methylisocitrate cleaving enzymes; evidence for the pathway of oxidation of propionyl-CoA to pyruvate via C7-tricarboxylic acids. Agric Biol Chem 39:2035–2042
Takahashi-Iniguez T, Garcia-Hernandez E, Arreguin-Espinosa R, Flores ME (2012) Role of vitamin B12 on methylmalonyl-CoA mutase activity. J Zhejiang Univ Sci B 13:423–437
Tao Y, Marzluf GA (1999) The NIT2 nitrogen regulatory protein of Neurospora: expression and stability of nit-2 mRNA and protein. Curr Genet 36:153–158
Textor S et al (1997) Propionate oxidation in Escherichia coli: evidence for operation of a methylcitrate cycle in bacteria. Arch Microbiol 168:428–436
Tiwari P, Misra BN, Sangwan NS (2013) beta-Glucosidases from the fungus Trichoderma: an efficient cellulase machinery in biotechnological applications. Biomed Res Int 2013:203735
Todd RB et al (1997) The acetate regulatory gene facB of Aspergillus nidulans encodes a Zn(II)2Cys6 transcriptional activator. Mol Gen Genet 254:495–504
Todd RB, Andrianopoulos A, Davis MA, Hynes MJ (1998) FacB, the Aspergillus nidulans activator of acetate utilization genes, binds dissimilar DNA sequences. EMBO J 17:2042–2054
Trepanier M et al (2005) Dependence of arbuscular-mycorrhizal fungi on their plant host for palmitic acid synthesis. Appl Environ Microbiol 71:5341–5347
Tsai CS, Mitton KP, Johnson BF (1989) Acetate assimilation by the fission yeast, Schizosaccharomyces pombe. Biochem Cell Biol 67:464–467
Tsang AW, Horswill AR, Escalante-Semerena JC (1998) Studies of regulation of expression of the propionate (prpBCDE) operon provide insights into how Salmonella typhimurium LT2 integrates its 1,2-propanediol and propionate catabolic pathways. J Bacteriol 180:6511–6518
Tu T et al (2013) High-yield production of a low-temperature-active polygalacturonase for papaya juice clarification. Food Chem 141:2974–2981
Turcotte B, Liang XB, Robert F, Soontorngun N (2010) Transcriptional regulation of nonfermentable carbon utilization in budding yeast. FEMS Yeast Res 10:2–13
Tylicki A, Ziolkowska G, Bolkun A, Siemieniuk M, Czerniecki J, Nowakiewicz A (2008) Comparative study of the activity and kinetic properties of malate dehydrogenase and pyruvate decarboxylase from Candida albicans, Malassezia pachydermatis, and Saccharomyces cerevisiae. Can J Microbiol 54:734–741
Vashishtha AK, West AH, Cook PF (2009) Chemical mechanism of saccharopine reductase from Saccharomyces cerevisiae. Biochemistry 48:5899–5907
Watanabe N, James MN (2011) Structural insights for the substrate recognition mechanism of LL-diaminopimelate aminotransferase. Biochim Biophys Acta 1814:1528–1533
Wendisch VF (2014) Microbial production of amino acids and derived chemicals: synthetic biology approaches to strain development. Curr Opin Biotechnol 30C:51–58
White MF, Fothergill-Gilmore LA, Kelly SM, Price NC (1993) Substitution of His-181 by alanine in yeast phosphoglycerate mutase leads to cofactor-induced dissociation of the tetrameric structure. Biochem J 291(Pt 2):479–483
Woo JM, Yang KM, Kim SU, Blank LM, Park JB (2014) High temperature stimulates acetic acid accumulation and enhances the growth inhibition and ethanol production by Saccharomyces cerevisiae under fermenting conditions. Appl Microbiol Biotechnol 98:6085–6094
Wu G (2014) Dietary requirements of synthesizable amino acids by animals: a paradigm shift in protein nutrition. J Anim Sci Biotechnol 5:34
Xu H, Andi B, Qian J, West AH, Cook PF (2006) The alpha-aminoadipate pathway for lysine biosynthesis in fungi. Cell Biochem Biophys 46:43–64
Yan H, He P, Cheng HR, Shen A, Jiang N (2007) Cloning, sequencing and characterization of the alpha-aminoadipate reductase gene (LYS2) from Saccharomycopsis fibuligera. Yeast 24:189–199
Yike I (2011) Fungal proteases and their pathophysiological effects. Mycopathologia 171:299–323
Zhang YQ, Brock M, Keller NP (2004) Connection of propionyl-CoA metabolism to polyketide biosynthesis in Aspergillus nidulans. Genetics 168:785–794
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Brock, M., Geib, E. (2016). 14 Special Aspects of Fungal Catabolic and Anabolic Pathways. In: Hoffmeister, D. (eds) Biochemistry and Molecular Biology. The Mycota, vol III. Springer, Cham. https://doi.org/10.1007/978-3-319-27790-5_14
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