Molecular Interactions, Structural Transitions and Alterations in SoxB Protein Due to SoxYZ Interaction from Two Distinct β-Proteobacteria: An In silico Approach Towards the Thiosulfate Oxidation and Recycling of SoxY Protein

Sujay Ray1, Semanti Ghosh1, Angshuman Bagchi1
1Department of Biochemistry and Biophysics, University of Kalyani, Kalyani, Nadia, India

Tóm tắt

Microbial oxidation–reduction reactions utilizing the environmental thiosulfate ions and mediated mainly by the sox operon are very much essential to maintain the sulfur balance in the environment. Majority of the previously documented wet laboratory studies show genetics behind the functionality of Sox proteins encoded by the sox operon. However, the molecular details of the involvements of the essential SoxB, SoxY and SoxZ proteins in the beta-proteobacteria have not yet been elucidated. In this work, an attempt was made to analyze the interaction profiles of the aforementioned SoxB, SoxY and SoxZ proteins to predict their roles in biological sulfur oxidation process. In order to establish the possible roles of these Sox proteins, we built the homology models of these proteins from the two different beta-proteobacteria Dechloromonas aromatica and Thiobacillus denitrificans. We then used molecular docking and simulation studies to further analyze the interaction profiles of these sox proteins. Our analyses revealed that SoxB protein from T. denitrificans exhibited steadier and stronger interactions with SoxYZ protein complex. On the other hand, SoxB protein from D. aromatica was found to exhibit a spontaneous interaction with greater ΔG values and therefore was well documented to exhibit a dual role. This is the first research article to discern the molecular level of interaction profiles of SoxB with SoxYZ protein complex in the beta-proteobacteria D. aromatica and T. denitrificans during the oxidations of thiosulfate. It would further prompt the future investigation into the mutational impact on the sequential interaction pattern in sox operon.

Tài liệu tham khảo

Ogawa T, Furusawa T, Shiga M, Seo D, Sakurai H, Inoue K (2010) Biochemical studies of a soxF-encoded monomeric flavoprotein purified from green sulfur bacterium Chlorobium tepidum that stimulates in Vitro thiosulfate oxidation. Biosci Biotechnol Biochem 74:771–780 Freidrich CG (1998) Physiology and genetics of sulfur- oxidizing bacteria. Adv Microb Physiol 39:235–289. doi:10.1016/S0065-2911(08)60018-1 Le Faou A et al (1990) Thiosulfate, polythionates and elemental sulfur assimilation and reduction in the bacterial world. FEMS Microbiol Rev 6:351–381. doi:10.1016/S0168-6445(05)80005-1 Appia-Ayme C et al (2001) Cytochrome complex essential for photosynthetic oxidation of both thiosulfate and sulfide in Rhodovulum sulfidophilum. J Bacteriol 183:6107–6118. doi:10.1128/JB.183.20.6107-6118.2001 Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67:2873–2882 Bagchi A, Ghosh TC (2006) Structural insight into the interactions of SoxV, SoxW and SoxS in the process of transport of reductants during sulfur oxidation by the novel global sulfur oxidation reaction cycle. Biophys Chem 119:7–13 Bagchi A (2005) Homology modeling of a transcriptional regulator SoxR of the lithotrophic sulfur oxidation (Sox) operon in α-proteobacteria. J Bio-molecular Struct Dyn 22:571–578 Bagchi A, Roy P (2005) Structural insight into SoxC and SoxD interaction and their role in electron transport process in the novel global sulfur cycle in Paracoccus pantotrophus. Biochem Biophys Res Commun 331:1107–1113. doi:10.1016/j.bbrc.2005.04.028 Rother D, Friedrich CG (2002) The cytochrome complex SoxXA of Paracoccus pantotrophus is produced in Escherichia coli and functional in the reconstituted sulfur-oxidizing enzyme system. Biochimica et Bio-physica Acta 1598:65–73 Hensen D et al (2006) Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Mol Microbiol 62:794–810. doi:10.1111/j.1365-2958.2006.05408.x Sano R et al (2010) Thiosulphate oxidation by a ther- mo-neutrophilic hydrogen-oxidizing bacterium, Hydrogenobacter thermophilus. Biosci Biotechnol Biochem 74:892–894. doi:10.1271/bbb.90948 Justin P, Kelly DP (1978) Growth kinetics of Thiobacillus denitrificans in anaerobic and aerobic chemostat culture. J Gen Microbiol 107:123–130 Justin P, Kelly DP (1978) Metabolic changes in Thiobacillus denitrificans accompanying the transition from aerobic to anaerobic growth in continuous chemostat culture. J Gen Microbiol 107:131–137 Kelly DP, Wood AP (2000) Confirmation of Thiobacillus denitrificans as a species of the genus Thiobacillus, in the β-subclass of the Proteobacteria, with strain NCIMB 9548 as the type strain. Int J Syst Evol Micr 50:547–550 Beller HR, Chain PS, Letain TE et al (2006) The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J Bacteriol 188:1473–1488 Kennan KS, Keith K, William SF, Helene F, Stephan T, Genevieve DB, Alla L (2009) Metabolic analysis of the soil microbe Dechloromonas aromatica str. RCB: indications of a surprisingly complex life-style and cryptic anaerobic pathways for aromatic degradation. BMC Genom 10:351 Ghosh W, Dam B (2009) Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol Rev 33:999–1043 Ray S, Bagchi A (2016) Insight into the Conformational Variations in SoxYZ Protein Complex from Two Different Members of the b-Proteobacterial Family Involved in Sulfur Oxidation. Interdiscip Sci Comput Life Sci. doi:10.1007/s12539-016-0153-z Xiang Z (2006) Advances in homology protein structure modeling. Curr Protein Pept Sci. 6 7(3):217–227. PMCID: PMC1839925 Webb B, Sali A (2014) Comparative protein structure modeling using modeller. Current protocols in bioinformatics. Wiley, Hoboken, pp 5.6.1–5.6.32 Marco B, Stefan B, Andrew W, Konstantin A, Gabriel S, Tobias S, Florian K, Tiziano GC, Martino B, Lorenza B, Torsten S (2014) SWISS-MODEL: modeling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42(W1):W252–W258 Fiser A, Sali A (2003) ModLoop: automated modeling of loops in protein structures. Bioinformatics 19(18):2500-1. PMID: 14668246 [PubMed—indexed for MEDLINE] Xu D, Zhang Y (2001) Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophys J 101:2525–2534. doi:10.1016/j.bpj.2011.10.024 Eisenberg D, Luthy R, Bowie JU (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol 277:396–404 Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemistry of protein structures. J Appl Cryst 26:283–291. doi:10.1107/S0021889892009944 Ramachandran GN, Sashisekharan V (1968) Conformation of polypeptides and proteins. Adv Protein Chem 23:283–438. doi:10.1016/S0065-3233(08)60402-7 Comeau SR, Gatchel DW, Vajda S, Camacho CJ (2004) ClusPro: an automated docking and discrimination method for the prediction of protein complexes. Bioinformatics 20(1):45–50 Kozakov D, Beglov D, Bohnuud T, Mottarella S, Xia B, Hall DR, Vajda S (2013) How good is automated protein docking? Proteins: structure. Funct Bioinform 81:2159–2166 Vakser IA (1995) Protein docking for low-resolution structures. Protein Eng 8:371–377 Chen R et al (2003) ZDOCK: an initial-stage protein docking algorithms. Proteins 51:82–87 Jian Z, Yu L, Yang Z (2011) Atomic-level protein structure refinement using fragment-guided molecular dynamics conformation sampling. Structure 19:1784–1795 Ramachandran S, Kota P, Ding F, Dokholyan NV (2011) PROTEINS: structure. Funct Bioinform 79:261–270 Tina KG, Bhadra R, Srinivasan N (2007) PIC: protein interactions calculator. Nucleic Acids Res 35:W473–W476 Baldwin RL (1996) How Hofmeister ion interactions affect protein stability. Biophys J 71(4):2056–2063 Gerstein M (1992) A resolution-sensitive procedure for comparing protein surfaces and its application to the comparison of antigen-combining sites. Acta Cryst A48:271–276 DeLano WL (2002) The PyMOL molecular graphics system. DeLano Scientific, San Carlos. doi:10.1093/nar/gki408 Tartaglia GG, Pawar AP, Campioni S, Dobson CM, Chiti F, Vendruscolo M (2008) Prediction of aggregation-prone regions in structured proteins. J Mol Biol 380:425–436 Zhou H, Zhou Y (2002) Distance-scaled, finite ideal-gas reference state improves structure-derived potentials of mean force for structure selection and stability prediction. Protein Sci 11:2714–2726 Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22(12):2577–2637 Mark B, David W (2003) Application of the random coil index to studying protein flexibility. J Biomol NMR 40(1):31–48 Ray S, Bagchi A (2013) Structural analysis of the mode of interactions of SoxB protein with SoxYZ complex from Allochromatium vinosum in the global sulfur oxidation cycle. Comput Mol Biol 3(1):1–5 Ray S, Banerjee A (2015) Molecular level biodegradation of phenol and its derivatives through dmp operon of Pseudomonas putida: a bio-molecular modeling and docking analysis. J Environ Sci 36:144–151