Characterization of a Family IV Esterase from Extremely Halophilic Archaeon Haloarcula Japonica

Overview

Journal Extremophiles

Publisher Springer

Date 2024 Dec 3

PMID 39625542

Authors

Hiromichi Kato

Shota Ambai

Fumiya Ikeda

Koji Abe

Satoshi Nakamura

Rie Yatsunami

Affiliations

Soon will be listed here.

Abstract

The novel esterase gene lipP1, which encodes HjEstP1, was discovered in the genome of the extremely halophilic archaeon Haloarcula japonica. A homology search and sequence alignment revealed that HjEstP1 is a member of family IV esterases with conserved GXSXG and HGGG motifs. lipP1 was expressed in its parental strain, and recombinant HjEstP1 was purified and characterized. Optimal pH and temperature of HjEstP1 were 6.0 and > 60 °C, respectively. HjEstP1 showed higher activity with increasing NaCl concentration, and optimal NaCl concentration was > 4.5 M. Furthermore, HjEstP1 preferentially hydrolyzed pNP and glycerol esters with short chain fatty acids. To our knowledge, this is the first report of an esterase from an extremely halophilic archaeon obtained via homologous expression.

References

Ollis D, Cheah E, Cygler M, Dijkstra B, Frolow F, Franken S . The alpha/beta hydrolase fold. Protein Eng. 1992; 5(3):197-211. DOI: 10.1093/protein/5.3.197. View

Madeira F, Pearce M, Tivey A, Basutkar P, Lee J, Edbali O . Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Res. 2022; 50(W1):W276-W279. PMC: 9252731. DOI: 10.1093/nar/gkac240. View

Bornscheuer U . Microbial carboxyl esterases: classification, properties and application in biocatalysis. FEMS Microbiol Rev. 2002; 26(1):73-81. DOI: 10.1111/j.1574-6976.2002.tb00599.x. View

Izotova L, Strongin A, Chekulaeva L, Sterkin V, Ostoslavskaya V, Lyublinskaya L . Purification and properties of serine protease from Halobacterium halobium. J Bacteriol. 1983; 155(2):826-30. PMC: 217755. DOI: 10.1128/jb.155.2.826-830.1983. View

Manco G, Adinolfi E, Pisani F, Ottolina G, Carrea G, Rossi M . Overexpression and properties of a new thermophilic and thermostable esterase from Bacillus acidocaldarius with sequence similarity to hormone-sensitive lipase subfamily. Biochem J. 1998; 332 ( Pt 1):203-12. PMC: 1219469. DOI: 10.1042/bj3320203. View

Arpigny J, Jaeger K . Bacterial lipolytic enzymes: classification and properties. Biochem J. 1999; 343 Pt 1:177-83. PMC: 1220539. View

Huo Y, Rong Z, Jian S, Xu C, Li J, Xu X . A Novel Halotolerant Thermoalkaliphilic Esterase from Marine Bacterium SW-135. Front Microbiol. 2017; 8:2315. PMC: 5702849. DOI: 10.3389/fmicb.2017.02315. View

Fukuchi S, Yoshimune K, Wakayama M, Moriguchi M, Nishikawa K . Unique amino acid composition of proteins in halophilic bacteria. J Mol Biol. 2003; 327(2):347-57. DOI: 10.1016/s0022-2836(03)00150-5. View

Rangel Pereira M, Maester T, Mercaldi G, Lemos E, Hyvonen M, Balan A . From a metagenomic source to a high-resolution structure of a novel alkaline esterase. Appl Microbiol Biotechnol. 2017; 101(12):4935-4949. DOI: 10.1007/s00253-017-8226-4. View

10.

Lu M, Daniel R . A Novel Carboxylesterase Derived from a Compost Metagenome Exhibiting High Stability and Activity towards High Salinity. Genes (Basel). 2021; 12(1). PMC: 7835964. DOI: 10.3390/genes12010122. View

11.

Muller-Santos M, de Souza E, de O Pedrosa F, Mitchell D, Longhi S, Carriere F . First evidence for the salt-dependent folding and activity of an esterase from the halophilic archaea Haloarcula marismortui. Biochim Biophys Acta. 2009; 1791(8):719-29. DOI: 10.1016/j.bbalip.2009.03.006. View

12.

Wang M, Ai L, Zhang M, Wang F, Wang C . Characterization of a novel halotolerant esterase from isolated from salt well mine. 3 Biotech. 2020; 10(10):430. PMC: 7490289. DOI: 10.1007/s13205-020-02420-0. View

13.

Wakai H, Nakamura S, Kawasaki H, Takada K, Mizutani S, Aono R . Cloning and sequencing of the gene encoding the cell surface glycoprotein of Haloarcula japonica strain TR-1. Extremophiles. 1997; 1(1):29-35. DOI: 10.1007/s007920050012. View

14.

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

15.

Park Y, Choi S, Lee H . A carboxylesterase from the thermoacidophilic archaeon Sulfolobus solfataricus P1; purification, characterization, and expression. Biochim Biophys Acta. 2006; 1760(5):820-8. DOI: 10.1016/j.bbagen.2006.01.009. View

16.

Manco G, Mandrich L, Rossi M . Residues at the active site of the esterase 2 from Alicyclobacillus acidocaldarius involved in substrate specificity and catalytic activity at high temperature. J Biol Chem. 2001; 276(40):37482-90. DOI: 10.1074/jbc.M103017200. View

17.

Miguel-Ruano V, Rivera I, Rajkovic J, Knapik K, Torrado A, Otero J . Biochemical and Structural Characterization of a novel thermophilic esterase EstD11 provide catalytic insights for the HSL family. Comput Struct Biotechnol J. 2021; 19:1214-1232. PMC: 7905190. DOI: 10.1016/j.csbj.2021.01.047. View

18.

De Santi C, Altermark B, Pierechod M, Ambrosino L, de Pascale D, Willassen N . Characterization of a cold-active and salt tolerant esterase identified by functional screening of Arctic metagenomic libraries. BMC Biochem. 2016; 17:1. PMC: 4717575. DOI: 10.1186/s12858-016-0057-x. View

19.

De Simone G, Galdiero S, Manco G, Lang D, Rossi M, Pedone C . A snapshot of a transition state analogue of a novel thermophilic esterase belonging to the subfamily of mammalian hormone-sensitive lipase. J Mol Biol. 2000; 303(5):761-71. DOI: 10.1006/jmbi.2000.4195. View

20.

Nagaoka S, Sugiyama N, Yatsunami R, Nakamura S . Characterization of 3-isopropylmalate dehydrogenase from extremely halophilic archaeon Haloarcula japonica. Biosci Biotechnol Biochem. 2021; 85(9):1986-1994. DOI: 10.1093/bbb/zbab122. View