Structural Adaptations of Octaheme Nitrite Reductases from Haloalkaliphilic Thioalkalivibrio Bacteria to Alkaline PH and High Salinity

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2017 May 17

PMID 28510595

Citations 4

Authors

Anna Popinako

Mikhail Antonov

Alexey Tikhonov

Tamara Tikhonova

Vladimir Popov

Affiliations

Soon will be listed here.

Abstract

Bacteria Tv. nitratireducens and Tv. paradoxus from soda lakes grow optimally in sodium carbonate/NaCl brines at pH range from 9.5 to 10 and salinity from 0.5 to 1.5 M Na+. Octaheme nitrite reductases (ONRs) from haloalkaliphilic bacteria of genus Thioalkalivibrio are stable and active in a wide range of pH (up to 11) and salinity (up to 1 M NaCl). To establish adaptation mechanisms of ONRs from haloalkaliphilic bacteria a comparative analysis of amino acid sequences and structures of ONRs from haloalkaliphilic bacteria and their homologues from non-halophilic neutrophilic bacteria was performed. The following adaptation strategies were observed: (1) strategies specific for halophilic and alkaliphilic proteins (an increase in the number of aspartate and glutamate residues and a decrease in the number of lysine residues on the protein surface), (2) strategies specific for halophilic proteins (an increase in the arginine content and a decrease in the number of hydrophobic residues on the solvent-accessible protein surface), (3) strategies specific for alkaliphilic proteins (an increase in the area of intersubunit hydrophobic contacts). Unique adaptation mechanism inherent in the ONRs from bacteria of genus Thioalkalivibrio was revealed (an increase in the core in the number of tryptophan and phenylalanine residues, and an increase in the number of small side chain residues, such as alanine and valine, in the core).

Citing Articles

Living in trinity of extremes: Genomic and proteomic signatures of halophilic, thermophilic, and pH adaptation.

Amangeldina A, Tan Z, Berezovsky I Curr Res Struct Biol. 2024; 7:100129.

PMID: 38327713 PMC: 10847869. DOI: 10.1016/j.crstbi.2024.100129.

Trichlorobacter ammonificans, a dedicated acetate-dependent ammonifier with a novel module for dissimilatory nitrate reduction to ammonia.

Sorokin D, Tikhonova T, Koch H, van den Berg E, Hinderks R, Pabst M ISME J. 2023; 17(10):1639-1648.

PMID: 37443340 PMC: 10504241. DOI: 10.1038/s41396-023-01473-2.

Bioinformatic analysis of subfamily-specific regions in 3D-structures of homologs to study functional diversity and conformational plasticity in protein superfamilies.

Timonina D, Sharapova Y, Svedas V, Suplatov D Comput Struct Biotechnol J. 2021; 19:1302-1311.

PMID: 33738079 PMC: 7933735. DOI: 10.1016/j.csbj.2021.02.005.

Zebra2: advanced and easy-to-use web-server for bioinformatic analysis of subfamily-specific and conserved positions in diverse protein superfamilies.

Suplatov D, Sharapova Y, Geraseva E, Svedas V Nucleic Acids Res. 2020; 48(W1):W65-W71.

PMID: 32313959 PMC: 7319439. DOI: 10.1093/nar/gkaa276.

References

Shifman J, Gibney B, Sharp R, Dutton P . Heme redox potential control in de novo designed four-alpha-helix bundle proteins. Biochemistry. 2000; 39(48):14813-21. DOI: 10.1021/bi000927b. View

Polyakov K, Boyko K, Tikhonova T, Slutsky A, Antipov A, Zvyagilskaya R . High-resolution structural analysis of a novel octaheme cytochrome c nitrite reductase from the haloalkaliphilic bacterium Thioalkalivibrio nitratireducens. J Mol Biol. 2009; 389(5):846-62. DOI: 10.1016/j.jmb.2009.04.037. View

Waterhouse A, Procter J, Martin D, Clamp M, Barton G . Jalview Version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009; 25(9):1189-91. PMC: 2672624. DOI: 10.1093/bioinformatics/btp033. View

Notredame C, Higgins D, Heringa J . T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol. 2000; 302(1):205-17. DOI: 10.1006/jmbi.2000.4042. View

Salomon-Ferrer R, Gotz A, Poole D, Le Grand S, Walker R . Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit Solvent Particle Mesh Ewald. J Chem Theory Comput. 2015; 9(9):3878-88. DOI: 10.1021/ct400314y. View

Poidevin L, MacNeill S . Biochemical characterisation of LigN, an NAD+-dependent DNA ligase from the halophilic euryarchaeon Haloferax volcanii that displays maximal in vitro activity at high salt concentrations. BMC Mol Biol. 2006; 7:44. PMC: 1684257. DOI: 10.1186/1471-2199-7-44. View

KYTE J, Doolittle R . A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982; 157(1):105-32. DOI: 10.1016/0022-2836(82)90515-0. View

Edgar R . MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 2004; 5:113. PMC: 517706. DOI: 10.1186/1471-2105-5-113. View

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S . MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28(10):2731-9. PMC: 3203626. DOI: 10.1093/molbev/msr121. View

10.

OLeary N, Wright M, Brister J, Ciufo S, Haddad D, McVeigh R . Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 2015; 44(D1):D733-45. PMC: 4702849. DOI: 10.1093/nar/gkv1189. View

11.

Madern D, Camacho M, Rodriguez-Arnedo A, Bonete M, Zaccai G . Salt-dependent studies of NADP-dependent isocitrate dehydrogenase from the halophilic archaeon Haloferax volcanii. Extremophiles. 2004; 8(5):377-84. DOI: 10.1007/s00792-004-0398-z. View

12.

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

13.

Mevarech M, Frolow F, Gloss L . Halophilic enzymes: proteins with a grain of salt. Biophys Chem. 2000; 86(2-3):155-64. DOI: 10.1016/s0301-4622(00)00126-5. View

14.

Pettersen E, Goddard T, Huang C, Couch G, Greenblatt D, Meng E . UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem. 2004; 25(13):1605-12. DOI: 10.1002/jcc.20084. View

15.

Petersen T, Brunak S, von Heijne G, Nielsen H . SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011; 8(10):785-6. DOI: 10.1038/nmeth.1701. View

16.

Winn M, Ballard C, Cowtan K, Dodson E, Emsley P, Evans P . Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr. 2011; 67(Pt 4):235-42. PMC: 3069738. DOI: 10.1107/S0907444910045749. View

17.

Zweig M, Campbell G . Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine. Clin Chem. 1993; 39(4):561-77. View

18.

Tikhonova T, Tikhonov A, Trofimov A, Polyakov K, Boyko K, Cherkashin E . Comparative structural and functional analysis of two octaheme nitrite reductases from closely related Thioalkalivibrio species. FEBS J. 2012; 279(21):4052-61. DOI: 10.1111/j.1742-4658.2012.08811.x. View

19.

Dubnovitsky A, Kapetaniou E, Papageorgiou A . Enzyme adaptation to alkaline pH: atomic resolution (1.08 A) structure of phosphoserine aminotransferase from Bacillus alcalophilus. Protein Sci. 2004; 14(1):97-110. PMC: 2253317. DOI: 10.1110/ps.041029805. View

20.

Filimonenkov A, Zvyagilskaya R, Tikhonova T, Popov V . Isolation and characterization of nitrate reductase from the halophilic sulfur-oxidizing bacterium Thioalkalivibrio nitratireducens. Biochemistry (Mosc). 2010; 75(6):744-51. DOI: 10.1134/s000629791006009x. View