YihQ is a Sulfoquinovosidase That Cleaves Sulfoquinovosyl Diacylglyceride Sulfolipids

Overview

Journal Nat Chem Biol

Specialties Biochemistry
Biology
Chemistry

Date 2016 Feb 16

PMID 26878550

Citations 28

Authors

Gaetano Speciale

Yi Jin

Gideon J Davies

Spencer J Williams

Ethan D Goddard-Borger

Affiliations

Soon will be listed here.

Abstract

Sulfoquinovose is produced by photosynthetic organisms at a rate of 10(10) tons per annum and is degraded by bacteria as a source of carbon and sulfur. We have identified Escherichia coli YihQ as the first dedicated sulfoquinovosidase and the gateway enzyme to sulfoglycolytic pathways. Structural and mutagenesis studies unveiled the sequence signatures for binding the distinguishing sulfonate residue and revealed that sulfoquinovoside degradation is widespread across the tree of life.

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References

Felux A, Spiteller D, Klebensberger J, Schleheck D . Entner-Doudoroff pathway for sulfoquinovose degradation in Pseudomonas putida SQ1. Proc Natl Acad Sci U S A. 2015; 112(31):E4298-305. PMC: 4534283. DOI: 10.1073/pnas.1507049112. View

Martelli H, Benson A . SULFOCARBOHYDRATE METABOLISM. I. BACTERIAL PRODUCTION AND UTILIZATION OF SULFOACETATE. Biochim Biophys Acta. 1964; 93:169-71. DOI: 10.1016/0304-4165(64)90272-7. View

McNicholas S, Potterton E, Wilson K, Noble M . Presenting your structures: the CCP4mg molecular-graphics software. Acta Crystallogr D Biol Crystallogr. 2011; 67(Pt 4):386-94. PMC: 3069754. DOI: 10.1107/S0907444911007281. View

Roy A, Hewlins M, Ellis A, Harwood J, White G . Glycolytic breakdown of sulfoquinovose in bacteria: a missing link in the sulfur cycle. Appl Environ Microbiol. 2003; 69(11):6434-41. PMC: 262304. DOI: 10.1128/AEM.69.11.6434-6441.2003. View

Denger K, Huhn T, Hollemeyer K, Schleheck D, Cook A . Sulfoquinovose degraded by pure cultures of bacteria with release of C3-organosulfonates: complete degradation in two-member communities. FEMS Microbiol Lett. 2011; 328(1):39-45. DOI: 10.1111/j.1574-6968.2011.02477.x. View

Speciale G, Thompson A, Davies G, Williams S . Dissecting conformational contributions to glycosidase catalysis and inhibition. Curr Opin Struct Biol. 2014; 28:1-13. PMC: 4220041. DOI: 10.1016/j.sbi.2014.06.003. View

Tagami T, Yamashita K, Okuyama M, Mori H, Yao M, Kimura A . Molecular basis for the recognition of long-chain substrates by plant α-glucosidases. J Biol Chem. 2013; 288(26):19296-303. PMC: 3696700. DOI: 10.1074/jbc.M113.465211. View

Studier F . Protein production by auto-induction in high density shaking cultures. Protein Expr Purif. 2005; 41(1):207-34. DOI: 10.1016/j.pep.2005.01.016. View

Sugimoto K, Sato N, Tsuzuki M . Utilization of a chloroplast membrane sulfolipid as a major internal sulfur source for protein synthesis in the early phase of sulfur starvation in Chlamydomonas reinhardtii. FEBS Lett. 2007; 581(23):4519-22. DOI: 10.1016/j.febslet.2007.08.035. View

10.

Okuyama M, Okuno A, Shimizu N, Mori H, Kimura A, Chiba S . Carboxyl group of residue Asp647 as possible proton donor in catalytic reaction of alpha-glucosidase from Schizosaccharomyces pombe. Eur J Biochem. 2001; 268(8):2270-80. DOI: 10.1046/j.1432-1327.2001.02104.x. View

11.

Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F . Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008; 36(Web Server issue):W465-9. PMC: 2447785. DOI: 10.1093/nar/gkn180. View

12.

Lee S, Yu S, Withers S . alpha-1,4-Glucan lyase performs a trans-elimination via a nucleophilic displacement followed by a syn-elimination. J Am Chem Soc. 2002; 124(18):4948-9. DOI: 10.1021/ja0255610. View

13.

Shimojima M . Biosynthesis and functions of the plant sulfolipid. Prog Lipid Res. 2011; 50(3):234-9. DOI: 10.1016/j.plipres.2011.02.003. View

14.

Denger K, Weiss M, Felux A, Schneider A, Mayer C, Spiteller D . Sulphoglycolysis in Escherichia coli K-12 closes a gap in the biogeochemical sulphur cycle. Nature. 2014; 507(7490):114-7. DOI: 10.1038/nature12947. View

15.

Lombard V, Ramulu H, Drula E, Coutinho P, Henrissat B . The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2013; 42(Database issue):D490-5. PMC: 3965031. DOI: 10.1093/nar/gkt1178. View

16.

Okuyama M, Mori H, Chiba S, Kimura A . Overexpression and characterization of two unknown proteins, YicI and YihQ, originated from Escherichia coli. Protein Expr Purif. 2004; 37(1):170-9. DOI: 10.1016/j.pep.2004.05.008. View

17.

Benning C . BIOSYNTHESIS AND FUNCTION OF THE SULFOLIPID SULFOQUINOVOSYL DIACYLGLYCEROL. Annu Rev Plant Physiol Plant Mol Biol. 2004; 49:53-75. DOI: 10.1146/annurev.arplant.49.1.53. View

18.

Quaroni A, Semenza G . Partial amino acid sequences around the essential carboxylate in the active sites of the intestinal sucrase-isomaltase complex. J Biol Chem. 1976; 251(11):3250-3. View

19.

. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr. 1994; 50(Pt 5):760-3. DOI: 10.1107/S0907444994003112. View

20.

Durham B, Sharma S, Luo H, Smith C, Amin S, Bender S . Cryptic carbon and sulfur cycling between surface ocean plankton. Proc Natl Acad Sci U S A. 2014; 112(2):453-7. PMC: 4299198. DOI: 10.1073/pnas.1413137112. View