Pressure adaptation is linked to thermal adaptation in salt-saturated marine habitats

Environmental Microbiology

Volumn 17, Issue 2, 2015, Pages 332-345

  Alcaide, María ^a   Stogios, Peter J ^b   Lafraya, Álvaro ^a,j   Tchigvintsev, Anatoli ^b   Flick, Robert ^b   Bargiela, Rafael ^a   Chernikova, Tatyana N ^c   Reva, Oleg N ^d   Hai, Tran ^c   Leggewie, Christian C ^e   Katzke, Nadine ^f   La Cono, Violetta ^g   Matesanz, Ruth ^h   Jebbar, Mohamed ⁱ   Jaeger, Karl Erich ^f   Yakimov, Michail M ^g   Yakunin, Alexander F ^b   Golyshin, Peter N ^c   Golyshina, Olga V ^c   Savchenko, Alexei ^b   Ferrer, Manuel ^a   more..

^a CSIC   (Spain)

^b UNIVERSITY OF TORONTO   (Canada)

^c BANGOR UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF PRETORIA   (South Africa)

^e Evocatal GmbH   (Germany)

^f FORSCHUNGSZENTRUM JÜLICH   (Germany)

^g CNR   (Italy)

^h CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

ⁱ UNIVERSITÉ DE BRETAGNE OCCIDENTALE   (France)

^j INSA   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

INORGANIC SALT; SEA WATER;

ACCLIMATIZATION; ADAPTATION; AQUATIC SPECIES; BACTERIUM; ECOSYSTEM; ENZYMOLOGY; HYDROSTATIC PRESSURE; LAKE; MEDITERRANEAN SEA; MICROBIOLOGY; SALINITY;

ACCLIMATIZATION; ADAPTATION, PHYSIOLOGICAL; AQUATIC ORGANISMS; BACTERIA; ECOSYSTEM; HYDROSTATIC PRESSURE; LAKES; MEDITERRANEAN SEA; SALINITY; SALTS; SEAWATER;

EID: 84923648530     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12660     Document Type: Article

References (61)

1. Akondi, K.B., and Lakshmi, V.V. (2013) Emerging trends in genomic approaches for microbial bioprospecting. OMICS 17: 61-70.
2. Albuquerque, D.M., Lopes, J.B., Segundo, L.F., Brandão, T.M., Ribeiro, M.N., Ramos, L., etal. (2012) Dehydrated brewery residue for pigs in the growth phase under high temperature conditions. Rev Bras Zool 41: 1784-1788.
3. Alcaide, M., Tornes, J., Stogios, P.J., Xu, X., Gertler, C., Di Leo, R., etal. (2013) Single residues dictate the co-evolution of dual esterases - MCP hydrolases from the α/β hydrolase family. Biochem J 454: 157-166.
4. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
5. Antunes, A., Eder, W., Fareleira, P., Santos, H., and Huber, R. (2003) Salinisphaera shabanensis gen. nov., sp. nov., a novel, moderately halophilic bacterium from the brine-seawater interface of the Shaban Deep, Red Sea. Extremophiles 7: 29-34.
6. Antunes, A., França, L., Rainey, F.A., Huber, R., Nobre, M.F., Edwards, K.J., and da Costa, M.S. (2007) Marinobacter salsuginis sp. nov., isolated from the brine-seawater interface of the Shaban Deep, Red Sea. Int J Syst Evol Microbiol 57: 1035-1040.
7. Antunes, A., Taborda, M., Huber, R., Moissl, C., Nobre, M.F., and da Costa, M.S. (2008) Halorhabdus tiamatea sp. nov., a non-pigmented, extremely halophilic archaeon from a deep-sea, hypersaline anoxic basin of the Red Sea, and emended description of the genus Halorhabdus. Int J Syst Evol Microbiol 58: 215-220.
8. Antunes, A., Rainey, F.A., Wanner, G., Taborda, M., Pätzold, J., Nobre, M.F., etal. (2008) A new lineage of halophilic, wall-less, contractile bacteria from a brine-filled deep of the Red Sea. J Bacteriol 190: 3580-3587.
9. Antunes, A., Alam, I., El Dorry, H., Siam, R., Robertson, A., Bajic, V.B., and Stingl, U. (2011) Genome sequence of Haloplasma contractile, an unusual contractile bacterium from a deep-sea anoxic brine lake. J Bacteriol 193: 4551-4552.
10. Cantarel, B.L., Coutinho, P.M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37: D233-D238.
11. Chamot-Rooke, N., Rabaute, A., and Kreemer, C. (2005) Western Mediterranean Ridge mud belt correlates with active shear strain at the prism-backstop geological contact. Geology 33: 861-864.
12. Combet, C., Jambon, M., Deléage, G., and Geourjon, C. (2002) Geno3D: automatic comparative molecular modelling of protein. Bioinformatics 18: 213-214.
13. Creamer, T.P., Srinivasan, R., and Rose, G.D. (1997) Modeling unfolded states of proteins and peptides. II. Backbone solvent accessibility. Biochemistry 36: 2832-2835.
14. Daffonchio, D., Borin, S., Brusa, T., Brusetti, L., van der Wielen, P.W., Bolhuis, H., etal. (2006) Biodeep scientific party. Stratified prokaryote network in the oxic-anoxic transition of a deep-sea halocline. Nature 440: 203-207.
15. De Corte, D., Sintes, E., Yokokawa, T., Reinthaler, T., and Herndl, G.J. (2012) Links between viruses and prokaryotes throughout the water column along a North Atlantic latitudinal transect. ISME J 6: 1566-1577.
16. De Lange, G.J., and Ten Haven, H.L. (1983) Recent sapropel formations in the eastern Mediterranean. Nature 305: 797-798.
17. De Vos, D., Xu, Y., Hulpiau, P., Vergauwen, B., and Van Beeumen, J.J. (2007) Structural investigation of cold activity and regulation of aspartate carbamoyltransferase from the extreme psychrophilic bacterium Moritella profunda. J Mol Biol 365: 379-395.
18. Del Pozo, M.V., Fernández-Arrojo, L., Gil-Martínez, J., Montesinos, A., Chernikova, T.N., Nechitaylo, T.Y., etal. (2012) Microbial β-glucosidases from cow rumen metagenome enhance the saccharification of lignocellulose in combination with commercial cellulase cocktail. Biotechnol Biofuels 5: 73.
19. Delgado-García, M., Valdivia-Urdiales, B., Aguilar-González, C.N., Contreras-Esquivel, J.C., and Rodríguez-Herrera, R. (2012) Halophilic hydrolases as a new tool for the biotechnological industries. J Sci Food Agric 92: 2575-2780.
20. Dolinsky, T.J., Nielsen, J.E., McCammon, J.A., and Baker, N.A. (2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res 32: W665-W667.
21. Dundas, J., Ouyang, Z., Tseng, J., Binkowski, A., Turpaz, Y., and Liang, J. (2006) CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res 34: W116-W118.
22. Eloe, E.A., Shulse, C.N., Fadrosh, D.W., Williamson, S.J., Allen, E.E., and Bartlett, D.H. (2011) Compositional differences in particle-associated and free-living microbial assemblages from an extreme deep-ocean environment. Environ Microbiol Rep 3: 449-458.
23. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62: 72-82.
24. Ferrer, M., Golyshina, O.V., Chernikova, T.N., Khachane, A.N., Martins Dos Santos, V.A., Yakimov, M.M., etal. (2005) Microbial enzymes mined from the Urania deep-sea hypersaline anoxic basin. Chem Biol 12: 895-904.
25. Ferrer, M., Werner, J., Chernikova, T.N., Bargiela, R., Fernández, L., La Cono, V., etal. (2012) Unveiling microbial life in the new deep-sea hypersaline Lake Thetis. Part II: a metagenomic study. Environ Microbiol 14: 268-281.
26. Hall, T.A. (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
27. 2-containing environments: chaotropicity defines the window. Environ Microbiol 9: 801-813.
28. Harrison, J.P., Gheeraert, N., Tsigelnitskiy, D., and Cockell, C.S. (2013) The limits for life under multiple extremes. Trends Microbiol 21: 204-212.
29. Kabsch, W. (2010) XDS. Acta Crystallogr D Biol Crystallogr 66: 125-132.
30. Kourist, R., Jochens, H., Bartsch, S., Kuipers, R., Padhi, S.K., Gall, M., etal. (2010) The alpha/beta-hydrolase fold 3DM database (ABHDB) as a tool for protein engineering. Chembiochem 11: 1635-1643.
31. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 60: 2256-2268.
32. La Cono, V., Smedile, F., Bortoluzzi, G., Arcadi, E., Maimone, G., Messina, E., etal. (2011) Unveiling microbial life in new deep-sea hypersaline Lake Thetis. Part I: prokaryotes and environmental settings. Environ Microbiol 13: 2250-2268.
33. Lai, K.K., Stogios, P.J., Vu, C., Xu, X., Cui, H., Molloy, S., etal. (2011) An inserted α/β subdomain shapes the catalytic pocket of Lactobacillus johnsonii cinnamoyl esterase. PLoS ONE 6: e23269.
34. Lukashin, A.V., and Borodovsky, M. (1998) GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26: 1107-1115.
35. Madern, D., Ebel, C., and Zaccai, G. (2000) Halophilic adaptation of enzymes. Extremophiles 4: 91-98.
36. Martínez-Martínez, M., Alcaide, M., Tchigvintsev, A., Reva, O., Polaina, J., Bargiela, R., etal. (2013) Biochemical diversity of carboxyl esterases and lipases from Lake Arreo (Spain): a metagenomic approach. Appl Environ Microbiol 79: 3553-3562.
37. MEDRIFF Consortium (1995) Three brine lakes discovered in the seafloor of the eastern Mediterranean. EOS Trans AGU 76: 313-318.
38. Menigaud, S., Mallet, L., Picord, G., Churlaud, C., Borrel, A., and Deschavanne, P. (2012) GOHTAM: a website for genomic origin of horizontal transfers, alignment and metagenomics. Bioinformatics 28: 1270-1271.
39. Michels, P.C., and Clark, D.S. (1997) Pressure-enhanced activity and stability of a hyperthermophilic protease from a deep-sea methanogen. Appl Environ Microbiol 63: 3985-3991.
40. Minor, W., Cymborowski, M., Otwinowski, Z., and Chruszcz, M. (2006) HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes. Acta Crystallogr D Biol Crystallogr 62: 859-866.
41. Nagata, T., Tamburini, C., Aristegui, J., Baltar, F., Bochdansky, A.B., Fonda-Umani, S., etal. (2010) Emerging concepts on microbial processes in the bathypelagic ocean - ecology, biogeochemistry and genomics. Deep Sea Res Part II Top Stud Oceanogr 57: 1519-1536.
42. Nechitaylo, T.Y., Timmis, K.N., and Golyshin, P.N. (2009) 'Candidatus Lumbricincola', a novel lineage of uncultured Mollicutes from earthworms of family Lumbricidae. Environ Microbiol 11: 1016-1026.
43. Pace, N., and Scholtz, J.M. (1997) Measuring the conformational stability of a protein, Chapter 12. In Protein Structure: A practical Approach. Creighton, T.E. (ed.). Heidelberg, Germany: IRL Press at Oxford University Press, pp. 299-322.
44. Pietra, F. (2012) On 3LEZ, a deep-sea halophilic protein with in vitro class-a β-lactamase activity: molecular-dynamics, docking, and reactivity simulations. Chem Biodivers 9: 2659-2684.
45. Puspita, I.D., Kamagata, Y., Tanaka, M., Asano, K., and Nakatsu, C.H. (2012) Are uncultivated bacteria really uncultivable? Microbes Environ 27: 356-366.
46. Reed, C.J., Lewis, H., Trejo, E., Winston, V., and Evilia, C. (2013) Protein adaptations in archaeal extremophiles. Archaea 2013: 373275.
47. Reyes-Duarte, D., Ferrer, M., and García-Arellano, H. (2012) Functional-based screening methods for lipases esterases and phospholipases in metagenomic libraries. In Lipases and Phospholipases: Methods and Protocols Methods in Molecular Biology, Vol. 861. Sandoval, G. (ed.). New York, NY, USA: © Springer Science+Business Media, pp. 101-113. doi:10.1007/978-1-61779-600-5_6.
48. Schlitzer, R. (2010) Ocean data view. SeaDataNet, Pan-European Infrastructure for Oceand & Marine Data Management, IFREMER/SISMER, Plouzane, France. URL http://odv.awi.de.
49. Schmid, F.Z. (1997) Optical spectroscopy to characterize protein conformation, Chapter 11. In Protein Structure: A Practical Approach. Creighton, T.E. (ed.). Oxford, UK: IRL Press, pp. 261-298.
50. Shin, D.S., Didonato, M., Barondeau, D.P., Hura, G.L., Hitomi, C., Berglund, J.A., etal. (2009) Superoxide dismutase from the eukaryotic thermophile Alvinella pompejana: structures, stability, mechanism, and insights into amyotrophic lateral sclerosis. J Mol Biol 385: 1534-1555.
51. Shirai, T., Hung, V.S., Morinaka, K., Kobayashi, T., and Ito, S. (2008) Crystal structure of GH13 alpha-glucosidase GSJ from one of the deepest sea bacteria. Proteins 73: 126-133.
52. Sineva, E.V., and Davydov, D.R. (2010) Cytochrome P450 from Photobacterium profundum SS9, a piezophilic bacterium, exhibits a tightened control of water access to the active site. Biochemistry 49: 10636-10646.
53. Smedile, F., Messina, E., La Cono, V., Tsoy, O., Monticelli, L.S., Borghini, M., etal. (2013) Metagenomic analysis of hadopelagic microbial assemblages thriving at the deepest part of Mediterranean Sea, Matapan-Vavilov Deep. Environ Microbiol 15: 167-182.
54. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
55. Wallmann, K., Suess, E., Westbrook, G.H., Winckler, G., and Cita, M.B. (1997) Salty brines on the Mediterranean Sea floor. Nature 387: 31-32.
56. Wang, H., Gong, Y., Xie, W., Xiao, W., Wang, J., Zheng, Y., etal. (2011) Identification and characterization of a novel thermostable gh-57 gene from metagenomic fosmid library of the Juan de Fuca Ridge hydrothemal vent. Appl Biochem Biotechnol 164: 1323-1338.
57. Werner, J., Ferrer, M., Michel, G., Mann, A.J., Huang, S., Juarez, S., etal. (2014) Halorhabdus tiamatea: proteogenomics and glycosidase activity measurements identify the first cultivated euryarchaeon from a deep-sea anoxic brine lake as potential polysaccharide degrader. Environ Microbiol 16: 2525-2537.
58. Xu, M., Xiao, X., and Wang, F. (2008) Isolation and characterization of alkane hydroxylases from a metagenomic library of Pacific deep-sea sediment. Extremophiles 12: 255-262.
59. Yakimov, M.M., Giuliano, L., Cappello, S., Denaro, R., and Golyshin, P.N. (2007) Microbial community of a hydrothermal mud vent underneath the deep-sea anoxic brine lake Urania (eastern Mediterranean). Orig Life Evol Biosph 37: 177-188.
60. Yakimov, M.M., La Cono, V., Slepak, V.Z., La Spada, G., Arcadi, E., Messina, E., etal. (2013) Microbial life in the Lake Medee, the largest deep-sea salt-saturated formation. Sci Rep 3: 3554.
61. Zeng, X., Birrien, J.L., Fouquet, Y., Cherkashov, G., Jebbar, M., Querellou, J., etal. (2009) Pyrococcus CH1, an obligate piezophilic hyperthermophile: extending the upper pressure-temperature limits for life. ISME J 3: 873-876.