Identification of a Stable Complex Between a [NiFe]-hydrogenase Catalytic Subunit and Its Maturation Protease

Overview

Journal FEBS Lett

Specialty Biochemistry

Date 2016 Dec 29

PMID 28029689

Citations 4

Authors

Marta Albareda

Grant Buchanan

Frank Sargent

Affiliations

Soon will be listed here.

Abstract

Salmonella enterica serovar Typhimurium has the ability to use molecular hydrogen as a respiratory electron donor. This is facilitated by three [NiFe]-hydrogenases termed Hyd-1, Hyd-2, and Hyd-5. Hyd-1 and Hyd-5 are homologous oxygen-tolerant [NiFe]-hydrogenases. A critical step in the biosynthesis of a [NiFe]-hydrogenase is the proteolytic processing of the catalytic subunit. In this work, the role of the maturation protease encoded within the Hyd-5 operon, HydD, was found to be partially complemented by the maturation protease encoded in the Hyd-1 operon, HyaD. In addition, both maturation proteases were shown to form stable complexes, in vivo and in vitro, with the catalytic subunit of Hyd-5. The protein-protein interactions were not detectable in a strain that could not make the enzyme metallocofactor.

Citing Articles

Activation of a [NiFe]-hydrogenase-4 isoenzyme by maturation proteases.

Finney A, Buchanan G, Palmer T, Coulthurst S, Sargent F Microbiology (Reading). 2020; 166(9):854-860.

PMID: 32731905 PMC: 7654741. DOI: 10.1099/mic.0.000963.

A membrane-bound [NiFe]-hydrogenase large subunit precursor whose C-terminal extension is not essential for cofactor incorporation but guarantees optimal maturation.

Hartmann S, Frielingsdorf S, Caserta G, Lenz O Microbiologyopen. 2020; 9(6):1197-1206.

PMID: 32180370 PMC: 7294309. DOI: 10.1002/mbo3.1029.

Molecular Hydrogen Metabolism: a Widespread Trait of Pathogenic Bacteria and Protists.

Benoit S, Maier R, Sawers R, Greening C Microbiol Mol Biol Rev. 2020; 84(1).

PMID: 31996394 PMC: 7167206. DOI: 10.1128/MMBR.00092-19.

Delimiting the Function of the C-Terminal Extension of the [NiFe]-Hydrogenase 2 Large Subunit Precursor.

Pinske C, Thomas C, Nutschan K, Sawers R Front Microbiol. 2019; 10:2223.

PMID: 31611859 PMC: 6769069. DOI: 10.3389/fmicb.2019.02223.

References

Vergnes A, Gouffi-Belhabich K, Blasco F, Giordano G, Magalon A . Involvement of the molybdenum cofactor biosynthetic machinery in the maturation of the Escherichia coli nitrate reductase A. J Biol Chem. 2004; 279(40):41398-403. DOI: 10.1074/jbc.M407087200. View

Ballantine S, Boxer D . Nickel-containing hydrogenase isoenzymes from anaerobically grown Escherichia coli K-12. J Bacteriol. 1985; 163(2):454-9. PMC: 219143. DOI: 10.1128/jb.163.2.454-459.1985. View

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

Zakian S, Lafitte D, Vergnes A, Pimentel C, Sebban-Kreuzer C, Toci R . Basis of recognition between the NarJ chaperone and the N-terminus of the NarG subunit from Escherichia coli nitrate reductase. FEBS J. 2010; 277(8):1886-95. DOI: 10.1111/j.1742-4658.2010.07611.x. View

Sauter M, Bohm R, Bock A . Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. Mol Microbiol. 1992; 6(11):1523-32. DOI: 10.1111/j.1365-2958.1992.tb00873.x. View

Magalon A, Bock A . Dissection of the maturation reactions of the [NiFe] hydrogenase 3 from Escherichia coli taking place after nickel incorporation. FEBS Lett. 2000; 473(2):254-8. DOI: 10.1016/s0014-5793(00)01542-8. View

Kumarevel T, Tanaka T, Bessho Y, Shinkai A, Yokoyama S . Crystal structure of hydrogenase maturating endopeptidase HycI from Escherichia coli. Biochem Biophys Res Commun. 2009; 389(2):310-4. DOI: 10.1016/j.bbrc.2009.08.135. View

Theodoratou E, Paschos A, Bock A . Analysis of the cleavage site specificity of the endopeptidase involved in the maturation of the large subunit of hydrogenase 3 from Escherichia coli. Arch Microbiol. 2000; 173(2):110-6. DOI: 10.1007/s002039900116. View

Zbell A, Maier S, Maier R . Salmonella enterica serovar Typhimurium NiFe uptake-type hydrogenases are differentially expressed in vivo. Infect Immun. 2008; 76(10):4445-54. PMC: 2546827. DOI: 10.1128/IAI.00741-08. View

10.

Fritsche E, Paschos A, Beisel H, Bock A, Huber R . Crystal structure of the hydrogenase maturating endopeptidase HYBD from Escherichia coli. J Mol Biol. 1999; 288(5):989-98. DOI: 10.1006/jmbi.1999.2719. View

11.

Yang F, Hu W, Xu H, Li C, Xia B, Jin C . Solution structure and backbone dynamics of an endopeptidase HycI from Escherichia coli: implications for mechanism of the [NiFe] hydrogenase maturation. J Biol Chem. 2006; 282(6):3856-63. DOI: 10.1074/jbc.M609263200. View

12.

Zbell A, Benoit S, Maier R . Differential expression of NiFe uptake-type hydrogenase genes in Salmonella enterica serovar Typhimurium. Microbiology (Reading). 2007; 153(Pt 10):3508-3516. DOI: 10.1099/mic.0.2007/009027-0. View

13.

Lukey M, Parkin A, Roessler M, Murphy B, Harmer J, Palmer T . How Escherichia coli is equipped to oxidize hydrogen under different redox conditions. J Biol Chem. 2009; 285(6):3928-3938. PMC: 2823535. DOI: 10.1074/jbc.M109.067751. View

14.

Ladant D, Karimova G . Genetic systems for analyzing protein-protein interactions in bacteria. Res Microbiol. 2000; 151(9):711-20. DOI: 10.1016/s0923-2508(00)01136-0. View

15.

Maier R, Olczak A, Maier S, Soni S, Gunn J . Respiratory hydrogen use by Salmonella enterica serovar Typhimurium is essential for virulence. Infect Immun. 2004; 72(11):6294-9. PMC: 523013. DOI: 10.1128/IAI.72.11.6294-6299.2004. View

16.

Bock A, King P, Blokesch M, Posewitz M . Maturation of hydrogenases. Adv Microb Physiol. 2006; 51:1-71. DOI: 10.1016/s0065-2911(06)51001-x. View

17.

Sawers R, Jamieson D, Higgins C, Boxer D . Characterization and physiological roles of membrane-bound hydrogenase isoenzymes from Salmonella typhimurium. J Bacteriol. 1986; 168(1):398-404. PMC: 213464. DOI: 10.1128/jb.168.1.398-404.1986. View

18.

Chalut C, Remy M, MASSON J . Disulfide bridges are not involved in penicillin-binding protein 1b dimerization in Escherichia coli. J Bacteriol. 1999; 181(9):2970-2. PMC: 93747. DOI: 10.1128/JB.181.9.2970-2972.1999. View

19.

Towbin H, Staehelin T, Gordon J . Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979; 76(9):4350-4. PMC: 411572. DOI: 10.1073/pnas.76.9.4350. View

20.

Hamilton C, Aldea M, Washburn B, Babitzke P, Kushner S . New method for generating deletions and gene replacements in Escherichia coli. J Bacteriol. 1989; 171(9):4617-22. PMC: 210259. DOI: 10.1128/jb.171.9.4617-4622.1989. View