Proteome profiling of heat, oxidative, and salt stress responses in Thermococcus kodakarensis KOD1

Frontiers in Microbiology

Volumn 6, Issue JUN, 2015, Pages

  Jia, Baolei ^a,b   Liu, Jinliang ^c   Van Duyet, Le ^b   Sun, Ying ^c   Xuan, Yuan H ^d   Cheong, Gang Won ^b  

^a Chung Ang University   (South Korea)

^b Gyeongsang National University   (South Korea)

^c JILIN UNIVERSITY   (China)

^d SHENYANG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Archaea; Metabolic pathway; Proteome; Stress responses; Thermococcus

Indexed keywords

PROTEOME;

ARTICLE; CARBOHYDRATE METABOLISM; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; GENE ONTOLOGY; HEAT STRESS; ISOELECTRIC FOCUSING; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SALT STRESS; SIGNAL TRANSDUCTION; THERMOCOCCUS KODAKARENSIS; UPREGULATION;

THERMOCOCCUS; THERMOCOCCUS KODAKARENSIS;

EID: 84936988526     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00605     Document Type: Article

References (43)

1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. doi: 10.1093/nar/25.17.3389
2. Atomi, H., Fukui, T., Kanai, T., Morikawa, M., and Imanaka, T. (2004). Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. KOD1. Archaea 1, 263-267. doi: 10.1155/2004/204953
3. Borges, N., Matsumi, R., Imanaka, T., Atomi, H., and Santos, H. (2010). Thermococcus kodakarensis mutants deficient in di-myo-inositol phosphate use aspartate to cope with heat stress. J. Bacteriol. 192, 191-197. doi: 10.1128/jb.01115-09
4. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254. doi: 10.1016/0003-2697(76)90527-3
5. Brasen, C., Esser, D., Rauch, B., and Siebers, B. (2014). Carbohydrate metabolism in Archaea: current insights into unusual enzymes and pathways and their regulation. Microbiol. Mol. Biol. Rev. 78, 89-175. doi: 10.1128/mmbr.00041-13
6. Chong, P. K., and Wright, P. C. (2005). Identification and characterization of the Sulfolobus solfataricus P2 proteome. J. Proteome Res. 4, 1789-1798. doi: 10.1021/pr0501214
7. Conesa, A., and Gotz, S. (2008). Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int. J. Plant Genomics 2008, 619832. doi: 10.1155/2008/619832
8. Danno, A., Fukuda, W., Yoshida, M., Aki, R., Tanaka, T., Kanai, T., et al. (2008). Expression profiles and physiological roles of two types of prefoldins from the hyperthermophilic archaeon Thermococcus kodakaraensis. J. Mol. Biol. 382, 298-311. doi: 10.1016/j.jmb.2008.07.032
9. Edgcomb, V., Molyneaux, S., Böer, S., Wirsen, C., Saito, M., Atkins, M., et al. (2007). Survival and growth of two heterotrophic hydrothermal vent archaea, Pyrococcus strain GB-D and Thermococcus fumicolans, under low pH and high sulfide concentrations in combination with high temperature and pressure regimes. Extremophiles 11, 329-342. doi: 10.1007/s00792-006-0043-0
10. Esteves, A. M., Chandrayan, S. K., Mcternan, P. M., Borges, N., Adams, M. W., and Santos, H. (2014). Mannosylglycerate and di-myo-inositol phosphate have interchangeable roles during adaptation of Pyrococcus furiosus to heat stress. Appl. Environ. Microbiol. 80, 4226-4233. doi: 10.1128/aem.00559-14
11. Feder, M. E., and Hofmann, G. E. (1999). Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61, 243-282. doi: 10.1146/annurev.physiol.61.1.243
12. Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M., Simonovic, M., Roth, A., et al. (2013). STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41, D808-D815. doi: 10.1093/nar/gks1094
13. Guan, Q., Guo, X., Han, T., Wei, M., Jin, M., Zeng, F., et al. (2013). Cloning, purification and biochemical characterisation of an organic solvent-, detergent-, and thermo-stable amylopullulanase from Thermococcus kodakarensis KOD1. Process. Biochem. 48, 878-884. doi: 10.1016/j.procbio.2013.04.007
14. Hileman, T. H., and Santangelo, T. J. (2012). Genetics techniques for Thermococcus kodakarensis. Front. Microbiol. 3:195. doi: 10.3389/fmicb.2012.00195
15. Izumi, M., Fujiwara, S., Takagi, M., Fukui, K., and Imanaka, T. (2001). Two kinds of archaeal chaperonin with different temperature dependency from a hyperthermophile. Biochem. Biophys. Res. Commun. 280, 581-587. doi: 10.1006/bbrc.2000.4154
16. Jenney, F. E., Verhagen, M. F. J. M., Cui, X., and Adams, M. W. W. (1999). Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286, 306-309. doi: 10.1126/science.286.5438.306
17. Jia, B., Lee, S., Pham, B., Liu, J., Pan, H., Zhang, S., et al. (2010). Oxidized NADH oxidase inhibits activity of an ATP/NAD kinase from a thermophilic archaeon. Protein J. 29, 609-616 doi: 10.1007/s10930-010-9284-y
18. Jiang, F., Zhang, Y., and Dusting, G. J. (2011). NADPH oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacol. Rev. 63, 218-242. doi: 10.1124/pr.110.002980
19. Kanehisa, M., and Goto, S. (2000). KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30. doi: 10.1093/nar/28.1.27
20. Kawakami, R., Sakuraba, H., Kamohara, S., Goda, S., Kawarabayasi, Y., and Ohshima, T. (2004). Oxidative stress response in an anaerobic hyperthermophilic archaeon: presence of a functional peroxiredoxin in Pyrococcus horikoshii. J. Biochem. 136, 541-547. doi: 10.1093/jb/mvh157
21. Kobori, H., Ogino, M., Orita, I., Nakamura, S., Imanaka, T., and Fukui, T. (2010). Characterization of NADH oxidase/NADPH polysulfide oxidoreductase and its unexpected participation in oxygen sensitivity in an anaerobic hyperthermophilic archaeon. J. Bacteriol. 192, 5192-5202. doi: 10.1128/jb.00235-10
22. Kondoh, H., Lleonart, M. E., Bernard, D., and Gil, J. (2007). Protection from oxidative stress by enhanced glycolysis; a possible mechanism of cellular immortalization. Histol. Histopathol. 22, 85-90.
23. Kültz, D. (2003). Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function. J. Exp. Biol. 206, 3119-3124. doi: 10.1242/jeb.00549
24. Kültz, D. (2005). Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67, 225-257. doi: 10.1146/annurev.physiol.67.040403.103635
25. Kwon, S., Kang, S., Park, S.-H., Kim, Y., Choi, J.-S., Lee, J.-H., et al. (2009). Proteomic characterization of the sulfur-reducing hyperthermophilic archaeon Thermococcus onnurineus NA1 by 2-DE/MS-MS. Extremophiles 13, 379-387. doi: 10.1007/s00792-008-0220-4
26. Lee, S., Jia, B., Liu, J., Pham, B. P., Kwak, J. M., Xuan, Y. H., et al. (2015). A 1-Cys peroxiredoxin from a thermophilic archaeon moonlights as a molecular chaperone to protect protein and DNA against stress-induced damage. PLoS ONE 10:e0125325. doi: 10.1371/journal.pone.0125325
27. Legrain, C., Villeret, V., Roovers, M., Tricot, C., Clantin, B., Van Beeumen, J., et al. (2001). "[20] Ornithine carbamoyltransferase from Pyrococcus furfosus," in Methods in Enzymology, eds R. M. K. Michael and W. W. Adams (Waltham, MA: Academic Press), 227-235.
28. Letunic, I., Doerks, T., and Bork, P. (2015). SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 43, D257-D260. doi: 10.1093/nar/gku949
29. Logemann, E., and Hahlbrock, K. (2002). Crosstalk among stress responses in plants: pathogen defense overrides UV protection through an inversely regulated ACE/ACE type of light-responsive gene promoter unit. Proc. Natl. Acad. Sci. U.S.A. 99, 2428-2432. doi: 10.1073/pnas.042692199
30. Marteinsson, V. T., Moulin, P., Birrien, J., Gambacorta, A., Vernet, M., and Prieur, D. (1997). Physiological responses to stress conditions and barophilic behavior of the hyperthermophilic vent Archaeon Pyrococcus abyssi. Appl. Environ. Microbiol. 63, 1230-1236.
31. Matsuura, A., Yoon, J., Yoon, H.-J., Lee, H., and Suh, S. (2012). Crystal structure of pyridoxal biosynthesis lyase PdxS from Pyrococcus horikoshii. Mol. Cells 34, 407-412. doi: 10.1007/s10059-012-0198-8
32. Mooney, S., Leuendorf, J.-E., Hendrickson, C., and Hellmann, H. (2009). Vitamin B6: a long known compound of surprising complexity. Molecules 14, 329-351. doi: 10.3390/molecules14010329
33. Morikawa, M., Izawa, Y., Rashid, N., Hoaki, T., and Imanaka, T. (1994). Purification and characterization of a thermostable thiol protease from a newly isolated hyperthermophilic Pyrococcus sp. Appl. Environ. Microbiol. 60, 4559-4566.
34. Orita, I., Sato, T., Yurimoto, H., Kato, N., Atomi, H., Imanaka, T., et al. (2006). The ribulose monophosphate pathway substitutes for the missing pentose phosphate pathway in the archaeon Thermococcus kodakaraensis. J. Bacteriol. 188, 4698-4704. doi: 10.1128/JB.00492-06
35. Park, S.-C., Pham, B. P., Van Duyet, L., Jia, B., Lee, S., Yu, R., et al. (2008). Structural and functional characterization of osmotically inducible protein C (OsmC) from Thermococcus kodakaraensis KOD1. BBA-Proteins Proteom. Biochim. Biophys. Acta 1784, 783-788. doi: 10.1016/j.bbapap.2008.02.002
36. Reed, C. J., Lewis, H., Trejo, E., Winston, V., and Evilia, C. (2013). Protein adaptations in archaeal extremophiles. Archaea 2013, 14. doi: 10.1155/2013/373275
37. Roy, A., Kucukural, A., and Zhang, Y. (2010). I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725-738. doi: 10.1038/nprot.2010.5
38. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., et al. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504. doi: 10.1101/gr.1239303
39. Simmons, S. O., Fan, C.-Y., and Ramabhadran, R. (2009). Cellular stress response pathway system as a sentinel ensemble in toxicological screening. Toxicol. Sci. 111, 202-225. doi: 10.1093/toxsci/kfp140
40. Sun, Y., Lv, X., Li, Z., Wang, J., Jia, B., and Liu, J. (2015). Recombinant cyclodextrinase from Thermococcus kodakarensis KOD1: expression, purification, and enzymatic characterization. Archaea 2015:397924. doi: 10.1155/2015/397924
41. Thorgersen, M. P., Stirrett, K., Scott, R. A., and Adams, M. W. (2012). Mechanism of oxygen detoxification by the surprisingly oxygen-tolerant hyperthermophilic archaeon, Pyrococcus furiosus. Proc. Natl. Acad. Sci. U.S.A. 109, 18547-18552. doi: 10.1073/pnas.1208605109
42. Yokooji, Y., Sato, T., Fujiwara, S., Imanaka, T., and Atomi, H. (2013). Genetic examination of initial amino acid oxidation and glutamate catabolism in the hyperthermophilic archaeon Thermococcus kodakarensis. J. Bacteriol. 195, 1940-1948. doi: 10.1128/jb.01979-12
43. Yun, S. H., Lee, Y. G., Choi, C.-W., Lee, S.-Y., and Kim, S. I. (2014). Proteomic exploration of extremophiles. Curr. Biotechnol. 3, 87-99. doi: 10.2174/22115501113026660040