A phosphoketolase Mpk1 of bacterial origin is adaptively required for full virulence in the insect-pathogenic fungus Metarhizium anisopliae

Environmental Microbiology

Volumn 11, Issue 9, 2009, Pages 2351-2360

  Duan, Zhibing ^a   Shang, Yianfang ^a   Gao, Qiang ^a   Zheng, Peng ^a   Wang, Chengshu ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LYASE; PENTOSE; PHOSPHOKETOLASE; VIRULENCE FACTOR;

ADAPTATION; ANIMAL; ARTICLE; BACTERIAL GENE; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; INSECT; LEPIDOPTERA; METABOLISM; METARHIZIUM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PENTOSE PHOSPHATE CYCLE; PHYLOGENY;

ADAPTATION, PHYSIOLOGICAL; ALDEHYDE-LYASES; ANIMALS; BASE SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; INSECTS; MANDUCA; METARHIZIUM; MOLECULAR SEQUENCE DATA; PENTOSE PHOSPHATE PATHWAY; PENTOSES; PHYLOGENY; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); FUNGI; HEXAPODA; MANDUCA SEXTA; METARHIZIUM ANISOPLIAE;

EID: 69949111630     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2009.01961.x     Document Type: Article

References (40)

1. Becker, A., Schlöder, P., Steele, J.E. Wegener, G. (1996) The regulation of trehalose metabolism in insects. Experientia 52 : 433 439.
2. Carbone, A., Zinovyev, A. Kepes, F. (2003) Codon adaptation index as a measure of dominating codon bias. Bioinformatics 19 : 2005 2015.
3. van der Does, H.C., Lievens, B., Claes, L., Houterman, P.M., Cornelissen, B.J. Rep, M. (2008) The presence of a virulence locus discriminates Fusarium oxysporum isolates causing tomato wilt from other isolates. Environ Microbiol 10 : 1475 1485.
4. de Faria, M.R. Wraight, S.P. (2007) Mycoinsecticides and Mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43 : 237 256.
5. Galagan, J.E., Calvo, S.E., Cuomo, C., Ma, L.J., Wortman, J.R., Batzoglou, S., et al. (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438 : 1105 1115.
6. Hu, G. St Leger, R.J. (2002) Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. Appl Environ Microbiol 68 : 6383 6387.
7. James, T.Y., Kauff, F., Schoch, C.L., Matheny, P.B., Hofstetter, V., Cox, C.J., et al. (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443 : 818 822.
8. Keeling, P.J. Palmer, J.D. (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9 : 605 618.
9. Kershaw, M.J., Moorhouse, E.R., Bateman, R., Reynolds, S.E. Charnley, A.K. (1999) The role of destruxins in the pathogenicity of Metarhizium anisopliae for three species of insect. J Invertebr Pathol 74 : 213 223.
10. Khaldi, N. Wolfe, K.H. (2008) Elusive origins of the extra genes in Aspergillus oryzae. PLoS ONE 3 : e3036.
11. Meile, L., Rohr, L.M., Geissmann, T.A., Herensperger, M. Teuber, M. (2001) Characterization of the d-xylulose 5-phosphate/d-fructose 6-phosphate phosphoketolase gene (xfp) from Bifidobacterium lactis. J Bacteriol 183 : 2929 2936.
12. Mullins, D.E. (1985) Chemistry and physiology of the hemolymph. In Comparative Physiology, Biochemistry and Pharmacology, Vol. 3. Kerkut, G.A. Gilbert, L.I. (eds). New York : Pergamon, pp. 355 400.
13. Nguyen, N.H., Suh, S.O., Marshall, C.J. Blackwell, M. (2006) Morphological and ecological similarities: wood-boring beetles associated with novel xylose-fermenting yeasts, Spathaspora passalidarum gen. sp. nov. and Candida jeffriesii sp. nov. Mycol Res 110 : 1232 1241.
14. Ochman, H., Lerat, E. Daubin, V. (2005) Examining bacterial species under the specter of gene transfer and exchange. Proc Natl Acad Sci USA 102 : 6595 6599.
15. Panagiotou, G., Kouskoumvekaki, I., Jonsdottir, S.O. Olsson, L. (2007) Monitoring novel metabolic pathways using metabolomics and machine learning: induction of the phosphoketolase pathway in Aspergillus nidulans cultivations. Metabolomics 3 : 503 516.
16. Panagiotou, G., Andersen, M.R., Grotkjaer, T., Regueira, T.B., Hofmann, G., Nielsen, J. Olsson, L. (2008) Systems analysis unfolds the relationship between the phosphoketolase pathway and growth in Aspergillus nidulans. PLoS ONE 3 : e3847.
17. Panagiotou, G., Andersen, M.R., Grotkjaer, T., Regueira, T.B., Hofmann, G., Nielsen, J. Olsson, L. (2009) Studies on the production of fungal polyketides in Aspergillus nidulans using systems biology tools. Appl Environ Microbiol 75 : 2212 2220.
18. Posthuma, C.C., Bader, R., Engelmann, R., Postma, P.W., Hengstenberg, W. Pouwels, P.H. (2002) Expression of the xylulose 5-phosphate phosphoketolase gene, xpkA, from Lactobacillus pentosus MD363 is induced by sugars that are fermented via the phosphoketolase pathway and is repressed by glucose mediated by CcpA and the mannose phosphoenolpyruvate phosphotransferase system. Appl Environ Microbiol 68 : 831 837.
19. Sanchez, B., Noriega, L., Ruas-Madiedo, P., de los Reyes-Gavilán, C.G. Margolles, A. (2004) Acquired resistance to bile increases fructose-6-phosphate phosphoketolase activity in Bifidobacterium. FEMS Microbiol Lett 235 : 35 341.
20. Screen, S.E. St Leger, R.J. (2000) Cloning, expression, and substrate specificity of a fungal chymotrypsin. Evidence for lateral gene transfer from an actinomycete bacterium. J Biol Chem 275 : 6689 6694.
21. Sonderegger, M., Schümperli, M. Sauer, U. (2004) Metabolic engineering of a phosphoketolase pathway for pentose catabolism in Saccharomyces cerevisiae. Appl Environ Microbiol 70 : 2892 2897.
22. St Leger, R.J. (2008) Studies on adaptations of Metarhizium anisopliae to life in the soil. J Invertebr Pathol 98 : 271 276.
23. Suh, S.O., Marshall, C.J., McHugh, J.V. Blackwell, M. (2003) Wood ingestion by passalid beetles in the presence of xylose-fermenting gut yeasts. Mol Ecol 12 : 3137 3145.
24. Swofford, D. (2001) PAUP (Phylogenetic Analysis Using Parsimony) V.4.0 B8a. Sunderland, MA : Sinauer.
25. Tamura, K., Dudley, J., Nei, M. Kumar, S. (2007) Mega4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol Biol Evol 24 : 1596 1599.
26. Thompson, S.N. (1999) Blood sugar formation from dietary carbohydrate is facilitated by the pentose phosphate pathway in an insect Manduca sexta Linnaeus. Biochim Biophys Acta 1472 : 565 575.
27. Thompson, S.N. Borchardt, D.B. (2003) Glucogenic blood sugar formation in an insect Manduca sexta L. asymmetric synthesis of trehalose from 13C enriched pyruvate. Comp Biochem Physiol B Biochem Mol Biol 135 : 461 471.
28. Thompson, S.N., Borchardt, D.B. Wang, L.W. (2003) Dietary nutrient levels regulate protein and carbohydrate intake, gluconeogenic/glycolytic flux and blood trehalose level in the insect Manduca sexta L. J Comp Physiol [B] 173 : 149 163.
29. Thykaer, J. Nielsen, J. (2007) Evidence, through C13-labelling analysis, of phosphoketolase activity in fungi. Proc Biochem 42 : 1050 1055.
30. Walton, J.D. (2000) Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: an hypothesis. Fungal Genet Biol 30 : 167 171.
31. Wang, C.S. St Leger, R.J. (2006) A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proc Natl Acad Sci USA 103 : 6647 6652.
32. Wang, C.S. St Leger, R.J. (2007a) A scorpion neurotoxin increases the potency of a fungal insecticide. Nat Biotechnol 25 : 1455 1456.
33. Wang, C.S. St Leger, R.J. (2007b) The MAD1 adhesin of Metarhizium anisopliae links adhesion with blastospore production and virulence to insects, and the MAD2 adhesin enables attachment to plants. Eukaryot Cell 6 : 808 816.
34. Wang, C.S. St Leger, R.J. (2007c) The Metarhizium anisopliae perilipin homolog MPL1 regulates lipid metabolism, appressorial turgor pressure, and virulence. J Biol Chem 282 : 21110 21115.
35. Wang, C.S., Hu, G. St Leger, R.J. (2005) Differential gene expression by Metarhizium anisopliae growing in root exudate and host (Manduca sexta) cuticle or hemolymph reveals mechanisms of physiological adaptation. Fungal Genet Biol 42 : 704 718.
36. Wang, C.S., Duan, Z.B. St Leger, R.J. (2008) MOS1 osmosensor of Metarhizium anisopliae is required for adaptation to insect host hemolymph. Eukaryot Cell 7 : 302 309.
37. Wu, G., Culley, D.E. Zhang, W. (2005) Predicted highly expressed genes in the genomes of Streptomyces coelicolor and Streptomyces avermitilis and the implications for their metabolism. Microbiology 151 : 2175 2187.
38. Xia, Y.X., Gao, M., Clarkson, J. Charnley, A. (2002) Molecular cloning, characterisation, and expression of a neutral trehalase from the insect pathogenic fungus Metarhizium anisopliae. J Invertebr Pathol 80 : 127 137.
39. Zaunmuller, T., Eichert, M., Richter, H. Unden, G. (2006) Variations in the energy metabolism of biotechnologically relevant heterofermentative lactic acid bacteria during growth on sugars and organic acids. Appl Microbiol Biotechnol 72 : 421 429.
40. Zhao, H., Charnley, A.K., Wang, Z., Yin, Y., Li, Z., Li, Y., et al. (2006) Identification of an extracellular acid trehalase and its gene involved in fungal pathogenesis of Metarizium anisopliae. J Biochem 140 : 319 327.