Two unexpected promiscuous activities of the iron-sulfur protein IspH in production of isoprene and isoamylene

Microbial Cell Factories

Volumn 15, Issue 1, 2016, Pages

  Ge, Deyong ^a,b,c   Xue, Yanfen ^a   Ma, Yanhe ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c ANHUI UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

(E) 4 Hydroxy 3 methyl 2 butenyl diphosphate (HMBPP); 2 Methyl 2 butene; 3 Methyl 1 butene; Bacillus; Dimethylallyl diphosphate (DMAPP); Isoprene; Isoprene synthase; IspH; IspS

Indexed keywords

ALKENE DERIVATIVE; ASPARAGINE; FERREDOXIN; FERREDOXIN NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE REDUCTASE; GLUTAMIC ACID; GLUTAMINE; HISTIDINE; IRON SULFUR PROTEIN; ISOAMYLENE; ISOPRENE; PROTEIN ISPH; RECOMBINANT PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; 1,3 BUTADIENE DERIVATIVE; 3,3-DIMETHYLALLYL PYROPHOSPHATE; 4-HYDROXY-3-METHYL-2-BUTENYL DIPHOSPHATE; BACTERIAL PROTEIN; HEMITERPENE; ORGANOPHOSPHATE; ORGANOPHOSPHORUS COMPOUND; OXIDOREDUCTASE; PENTANE;

ARTICLE; BACILLUS; BACILLUS SUBTILIS; BACTERIAL STRAIN; CATALYSIS; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVITY; ESCHERICHIA COLI; IN VITRO STUDY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SITE DIRECTED MUTAGENESIS; WILD TYPE; BIOSYNTHESIS; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; ISOMERISM; MASS FRAGMENTOGRAPHY; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS;

BACILLUS; BACTERIAL PROTEINS; BUTADIENES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FERREDOXINS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HEMITERPENES; IRON-SULFUR PROTEINS; ISOMERISM; MUTAGENESIS, SITE-DIRECTED; ORGANOPHOSPHATES; ORGANOPHOSPHORUS COMPOUNDS; OXIDOREDUCTASES; PENTANES; RECOMBINANT PROTEINS;

EID: 84968831715     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-016-0476-9     Document Type: Article

References (40)

1. Gelmont D, Stein RA, Mead JF. Isoprene-the main hydrocarbon in human breath. Biochem Biophys Res Commun. 1981;99:1456-60.
2. Monson RK, Fall R. Isoprene emission from aspen leaves: influence of environment and relation to photosynthesis and photorespiration. Plant Physiol. 1989;90:267-74.
3. Kuzma J, Nemecek-Marshall M, Pollock WH, Fall R. Bacteria produce the volatile hydrocarbon isoprene. Curr Microbiol. 1995;30:97-103.
4. Miller B, Oschinski C, Zimmer W. First isolation of an isoprene synthase gene from poplar and successful expression of the gene in Escherichia coli. Planta. 2001;213:483-7.
5. Sharkey TD, Yeh S, Wiberley AE, Falbel TG, Gong D, Fernandez DE. Evolution of the isoprene biosynthetic pathway in kudzu. Plant Physiol. 2005;137:700-12.
6. Koksal M, Zimmer I, Schnitzler JP, Christianson DW. Structure of isoprene synthase illuminates the chemical mechanism of teragram atmospheric carbon emission. J Mol Biol. 2010;402:363-73.
7. Sivy TL, Shirk MC, Fall R. Isoprene synthase activity parallels fluctuations of isoprene release during growth of Bacillus subtilis. Biochem Biophys Res Commun. 2002;294:71-5.
8. Rohmer M, Knani M, Simonin P, Sutter B, Sahm H. Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem J. 1993;295(Pt 2):517-24.
9. Paseshnichenko VA. A new alternative non-mevalonate pathway for isoprenoid biosynthesis in eubacteria and plants. Biochemistry (Mosc). 1998;63:139-48.
10. Rohmer M. The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat Prod Rep. 1999;16:565-74.
11. Zhao L, Chang WC, Xiao Y, Liu HW, Liu P. Methylerythritol phosphate pathway of isoprenoid biosynthesis. Annu Rev Biochem. 2013;82:497-530.
12. Rohdich F, Hecht S, Gartner K, Adam P, Krieger C, Amslinger S, Arigoni D, Bacher A, Eisenreich W. Studies on the nonmevalonate terpene biosynthetic pathway: metabolic role of IspH (LytB) protein. Proc Natl Acad Sci. 2002;99:1158-63.
13. Rohdich F, Zepeck F, Adam P, Hecht S, Kaiser J, Laupitz R, Grawert T, Amslinger S, Eisenreich W, Bacher A, Arigoni D. The deoxyxylulose phosphate pathway of isoprenoid biosynthesis: studies on the mechanisms of the reactions catalyzed by IspG and IspH protein. Proc Natl Acad Sci. 2003;100:1586-91.
14. Wolff M, Seemann M, Tse Sum Bui B, Frapart Y, Tritsch D, Garcia Estrabot A, Rodriguez-Concepcion M, Boronat A, Marquet A, Rohmer M. Isoprenoid biosynthesis via the methylerythritol phosphate pathway: the (E)-4-hydroxy-3-methylbut-2-enyl diphosphate reductase (LytB/IspH) from Escherichia coli is a [4Fe - 4S] protein. FEBS Lett. 2003;541:115-20.
15. Grawert T, Kaiser J, Zepeck F, Laupitz R, Hecht S, Amslinger S, Schramek N, Schleicher E, Weber S, Haslbeck M, et al. IspH protein of Escherichia coli: studies on iron-sulfur cluster implementation and catalysis. J Am Chem Soc. 2004;126:12847-55.
16. 2+ center with unusual coordination sphere in the LytB protein. J Am Chem Soc. 2009;131:13184-5.
17. Puan KJ, Wang H, Dairi T, Kuzuyama T, Morita CT. fldA is an essential gene required in the 2-C-methyl-D-erythritol 4-phosphate pathway for isoprenoid biosynthesis. FEBS Lett. 2005;579:3802-6.
18. Rohrich RC, Englert N, Troschke K, Reichenberg A, Hintz M, Seeber F, Balconi E, Aliverti A, Zanetti G, Kohler U, et al. Reconstitution of an apicoplast-localised electron transfer pathway involved in the isoprenoid biosynthesis of Plasmodium falciparum. FEBS Lett. 2005;579:6433-8.
19. Xiao Y, Chang WC, Liu HW, Liu P. Study of IspH, a key enzyme in the methylerythritol phosphate pathway using fluoro-substituted substrate analogues. Org Lett. 2011;13:5912-5.
20. Wang W, Wang K, Span I, Jauch J, Bacher A, Groll M, Oldfield E. Are free radicals involved in IspH catalysis? An EPR and crystallographic investigation. J Am Chem Soc. 2012;134:11225-34.
21. Span I, Wang K, Wang W, Zhang Y, Bacher A, Eisenreich W, Li K, Schulz C, Oldfield E, Groll M. Discovery of acetylene hydratase activity of the iron-sulphur protein IspH. Nat Commun. 2012;3:1042.
22. Rekittke I, Wiesner J, Rohrich R, Demmer U, Warkentin E, Xu W, Troschke K, Hintz M, No JH, Duin EC, et al. Structure of (E)-4-hydroxy-3-methyl-but-2-enyl diphosphate reductase, the terminal enzyme of the non-mevalonate pathway. J Am Chem Soc. 2008;130:17206-7.
23. Grawert T, Rohdich F, Span I, Bacher A, Eisenreich W, Eppinger J, Groll M. Structure of active IspH enzyme from Escherichia coli provides mechanistic insights into substrate reduction. Angew Chem Int Ed Engl. 2009;48:5756-9.
24. Wang W, Wang K, Liu YL, No JH, Li J, Nilges MJ, Oldfield E. Bioorganometallic mechanism of action, and inhibition, of IspH. Proc Natl Acad Sci. 2010;107:4522-7.
25. Span I, Grawert T, Bacher A, Eisenreich W, Groll M. Crystal structures of mutant IspH proteins reveal a rotation of the substrate's hydroxymethyl group during catalysis. J Mol Biol. 2012;416:1-9.
26. Grawert T, Span I, Eisenreich W, Rohdich F, Eppinger J, Bacher A, Groll M. Probing the reaction mechanism of IspH protein by x-ray structure analysis. Proc Natl Acad Sci. 2010;107:1077-81.
27. Fisher AJ, Rosenstiel TN, Shirk MC, Fall R. Nonradioactive assay for cellular dimethylallyl diphosphate. Anal Biochem. 2001;292:272-9.
28. Weise SE, Li Z, Sutter AE, Corrion A, Banerjee A, Sharkey TD. Measuring dimethylallyl diphosphate available for isoprene synthesis. Anal Biochem. 2013;435:27-34.
29. Jomaa H, Wiesner J, Sanderbrand S, Altincicek B, Weidemeyer C, Hintz M, Turbachova I, Eberl M, Zeidler J, Lichtenthaler HK, et al. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science. 1999;285:1573-6.
30. Wiesner J, Jomaa H. Isoprenoid biosynthesis of the apicoplast as drug target. Curr Drug Targets. 2007;8:3-13.
31. Heuston S, Begley M, Gahan CG, Hill C. Isoprenoid biosynthesis in bacterial pathogens. Microbiology. 2012;158:1389-401.
32. Lindberg P, Park S, Melis A. Engineering a platform for photosynthetic isoprene production in cyanobacteria, using Synechocystis as the model organism. Metab Eng. 2010;12:70-9.
33. Hong SY, Zurbriggen AS, Melis A. Isoprene hydrocarbons production upon heterologous transformation of Saccharomyces cerevisiae. J Appl Microbiol. 2012;113:52-65.
34. Yang J, Zhao G, Sun Y, Zheng Y, Jiang X, Liu W, Xian M. Bio-isoprene production using exogenous MVA pathway and isoprene synthase in Escherichia coli. Bioresour Technol. 2012;104:642-7.
35. Martin VJ, Pitera DJ, Withers ST, Newman JD, Keasling JD. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat Biotechnol. 2003;21:796-802.
36. Sivy TL, Fall R, Rosenstiel TN. Evidence of isoprenoid precursor toxicity in Bacillus subtilis. Biosci Biotechnol Biochem. 2011;75:2376-83.
37. Withers ST, Gottlieb SS, Lieu B, Newman JD, Keasling JD. Identification of isopentenol biosynthetic genes from Bacillus subtilis by a screening method based on isoprenoid precursor toxicity. Appl Environ Microbiol. 2007;73:6277-83.
38. Gao C, Xue Y, Ma Y. Protoplast transformation of recalcitrant alkaliphilic Bacillus sp. with methylated plasmid DNA and a developed hard agar regeneration medium. PLoS ONE. 2011;6:e28148.
39. Connelly MB, Young GM, Sloma A. Extracellular proteolytic activity plays a central role in swarming motility in Bacillus subtilis. J Bacteriol. 2004;186:4159-67.
40. Sullivan MA, Yasbin RE, Young FE. New shuttle vectors for Bacillus subtilis and Escherichia coli which allow rapid detection of inserted fragments. Gene. 1984;29:21-6.