Identification of fungal oxaloacetate hydrolyase within the isocitrate lyase/PEP mutase enzyme superfamily using a sequence marker-based method
Henk-Jan Joosten
Laboratory of Microbiology, Wageningen University, 6703 HA Wageningen, The Netherlands
Henk-Jan Joosten and Ying Han contributed equally to this work.
Search for more papers by this authorYing Han
Department of Chemistry, University of New Mexico, Albuquerque, New Mexico 87131
Henk-Jan Joosten and Ying Han contributed equally to this work.
Search for more papers by this authorWeiling Niu
Department of Chemistry, University of New Mexico, Albuquerque, New Mexico 87131
Search for more papers by this authorJacques Vervoort
Laboratory Biochemistry, Wageningen University, 6703 HA Wageningen, The Netherlands
Search for more papers by this authorDebra Dunaway-Mariano
Department of Chemistry, University of New Mexico, Albuquerque, New Mexico 87131
Search for more papers by this authorCorresponding Author
Peter J. Schaap
Laboratory of Microbiology, Wageningen University, 6703 HA Wageningen, The Netherlands
Laboratory of Microbiology, Dreijenlaan 2, 6703 HA Wageningen, The Netherlands===Search for more papers by this authorHenk-Jan Joosten
Laboratory of Microbiology, Wageningen University, 6703 HA Wageningen, The Netherlands
Henk-Jan Joosten and Ying Han contributed equally to this work.
Search for more papers by this authorYing Han
Department of Chemistry, University of New Mexico, Albuquerque, New Mexico 87131
Henk-Jan Joosten and Ying Han contributed equally to this work.
Search for more papers by this authorWeiling Niu
Department of Chemistry, University of New Mexico, Albuquerque, New Mexico 87131
Search for more papers by this authorJacques Vervoort
Laboratory Biochemistry, Wageningen University, 6703 HA Wageningen, The Netherlands
Search for more papers by this authorDebra Dunaway-Mariano
Department of Chemistry, University of New Mexico, Albuquerque, New Mexico 87131
Search for more papers by this authorCorresponding Author
Peter J. Schaap
Laboratory of Microbiology, Wageningen University, 6703 HA Wageningen, The Netherlands
Laboratory of Microbiology, Dreijenlaan 2, 6703 HA Wageningen, The Netherlands===Search for more papers by this authorAbstract
Aspergillus niger produces oxalic acid through the hydrolysis of oxaloacetate, catalyzed by the cytoplasmic enzyme oxaloacetate acetylhydrolase (OAH). The A. niger genome encodes four additional open reading frames with strong sequence similarity to OAH yet only the oahA gene encodes OAH activity. OAH and OAH-like proteins form subclass of the isocitrate lyase/PEP mutase enzyme superfamily, which is ubiquitous present filamentous fungi. Analysis of function-specific residues using a superfamily-based approach revealed an active site serine as a possible sequence marker for OAH activity. We propose that presence of this serine in family members correlates with presence of OAH activity whereas its absence correlates with absence of OAH. This hypothesis was tested by carrying out a serine mutagenesis study with the OAH from the fungal oxalic acid producer Botrytis cinerea and the OAH active plant petal death protein as test systems. Proteins 2008. © 2007 Wiley-Liss, Inc.
Supporting Information
The Supplementary Material referred to in this article can be found online at http://www.interscience.wiley.com/jpages/0887-3585/suppmat .
| Filename | Description |
|---|---|
| jws-prot.216221.doc211.5 KB | Supporting Information file jws-prot.216221.doc |
| jws-prot.216222.pdf163.7 KB | Supporting Information file jws-prot.216222.pdf |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1 Dutton,Evans CS. Oxalate production by fungi: its role in pathogenicity and ecology in the soil enviroment. Can J Microbiol 1996; 42: 881–895.
- 2 Kirkland BH,Eisa A,Keyhani NO. Oxalic acid as a fungal acaracidal virulence factor. J Med Entomol 2005; 42: 346–351.
- 3 Maxwell DP,Bateman DF. Oxalic acid biosynthesis by Sclerotium rolfsii. Phytopathology 1968; 58: 1635–1642.
- 4 Godoy G,Steadman JR,Dickman B,Dam R. Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiol Mol Plant Pathol 1990; 37: 179–191.
- 5 Nakagawa Y,Shimazu K,Ebihara M,Nakagawa K. Aspergillus niger pneumonia with fatal pulmonary oxalosis. J Infect Chemother 1999; 5: 97–100.
- 6 Kubicek CP,Schreferl-Kunar G,Wohrer W,Rohr M. Evidence for a cytoplasmic pathway of oxalate biosynthesis in Aspergillus niger. Appl Environ Microbiol 1988; 54: 633–637.
- 7 Balmforth AJ,Thomson A. Isolation and characterization of glyoxylate dehydrogenase from the fungus Sclerotium rolfsii. Biochem J 1984; 218: 113–118.
- 8 Hammel KE,Mozuch MD,Jensen KA.Jr.,Kersten PJ. H2O2 recycling during oxidation of the arylglycerol beta-aryl ether lignin structure by lignin peroxidase and glyoxal oxidase. Biochemistry 1994; 33: 13349–13354.
- 9 Yaver D,Cherry B,Murrell J. Polypeptides having oxaloacetate hydrolase activity and nucleic acids encoding same. US Patent 6,939,701, 2004.
- 10 Munir E,Yoon Gem JJ,Tokimatsu T,Hattori T,Shimada M. A physiological role for oxalic acid biosynthesis in the wood-rotting basidiomycete Fomitopsis palustris. Proc Natl Acad Sci USA 2001; 98: 11126–11130.
- 11 Akamatsu Y,Takahashi M,Shimada M. Influences of various factors on oxaloactase activity of the brown-rot fungus Tyromyces palustris. Mokuzia Gakkaishi 1993; 39: 352–356.
- 12 Ruijter GJ,van de Vondervoort PJ,Visser J. Oxalic acid production by Aspergillus niger: an oxalate-non-producing mutant produces citric acid at pH 5 and in the presence of manganese. J Microbiol 1999; 145: 2569–2576.
- 13 Pedersen H,Gem C,Nielsen J. Cloning and characterization of oah, the gene encoding oxaloacetate hydrolase in Aspergillus niger. J Mol Gen Genet 2000; 263: 281–286.
- 14 Pedersen H,Christensen B,Hjort C,Nielsen J. Construction and characterization of an oxalic acid nonproducing strain of Aspergillus niger. Metab Eng 2000; 2: 34–41.
- 15 Folkertsma S,van Noort P,Van Durme J,Joosten HJ,Bettler E,Fleuren W,Oliveira L,Horn F,de Vlieg J,Vriend G. A family-based approach reveals the function of residues in the nuclear receptor ligand-binding domain. J Mol Biol 2004; 341: 321–335.
- 16 Verhoeff K,Leeman M,Peer R,Posthuma L,Schot N,van Eijk GW. Changes in pH and the production of organic acids during colonisation of tomato petioles by Botrytis cinerea. J Phytopathol 1988; 122: 327–336.
- 17 Khabir A,Makni S,Ayadi L,Boudawara T,Frikha I,Sahnoun Y,Jlidi R. Pulmonary oxalosis with necrotizing pulmonary aspergillosis. Ann Pathol 2002; 22: 121–123.
- 18 Guimaraes RL,Stotz HU. Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiol 2004; 136: 3703–3711.
- 19 Kenealy WR,Dietrich DM. Growth and fermentation responses of Phanerochaete chrysosporium to O2 limitation. Enzyme Microb Technol 2004; 34: 490–498.
- 20 Lu Z,Feng X,Song L,Han Y,Kim A,Herzberg O,Woodson WR,Martin BM,Mariano PS,Dunaway-Mariano D. Diversity of function in the isocitrate lyase enzyme superfamily: the Dianthus caryophyllus petal death protein cleaves alpha-keto and alpha-hydroxycarboxylic acids. Biochemistry 2005; 44: 16365–16376.
- 21 Han Y,Joosten HJ,Niu W,Zhao Z,Mariano PS,McCalman MT,van Kan JAL,Schaap PJ,Dunaway-Mariano D. Oxaloacetate hydrolase: the CC bond lyase of oxalate secreting fungi. Submitted.
- 22 Andreeva A,Howorth D,Brenner SE,Hubbard TJ,Chothia C,Murzin AG. SCOP database in 2004: refinements integrate structure and sequence family data. Nucleic Acids Res 2004: 32; 226–229.
- 23 Vriend G. WHAT IF: a molecular modeling and drug design program. J Mol Graph 1990; 8: 52–56
- 24 Shulman AI,Larson C,Mangelsdorf DJ,Ranganathan R. Structural determinants of allosteric ligand activation in RXR heterodimers. Cell 2004; 116: 417–429.
- 25 Thompson JD,Higgins DG,Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22: 4673–4680.
- 26 Schmidt HA,Strimmer K,Vingron M,von Haeseler A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 2002; 18: 502–504.
- 27 Muller T,Vingron M. Modeling amino acid replacement. J Comput Biol 2000; 7: 761–776.
- 28 Howe K,Bateman A,Durbin R. QuickTree: building huge neighbour-joining trees of protein sequences. Bioinformatics 2002; 18: 1546–1547.
- 29 Page RD. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 1996; 12: 357–358.
- 30 Van Durme J,Horn F,Costagliola S,Vriend G,Vassart G. GRIS: Glycoprotein-hormone Receptor Information System. Mol Endocrinol 2006; 20: 2247–2255.
- 31 Teplyakov A,Liu S,Lu Z,Howard A,Dunaway-Mariano D,Herzberg O. Crystal structure of the petal death protein from carnation flower. Biochemistry 2005; 44: 16377–16384.
- 32
Oliveira L,Paiva CM,Vriend G.
Correlated mutation analyses on very large sequence families.
Chembiochem
2002;
3:
1010–1017.
10.1002/1439-7633(20021004)3:10<1010::AID-CBIC1010>3.0.CO;2-T CAS PubMed Web of Science® Google Scholar
Citing Literature
