Temperature-dependent global gene expression in the Antarctic archaeon Methanococcoides burtonii

Environmental Microbiology

Volumn 13, Issue 8, 2011, Pages 2018-2038

  Campanaro, S ^a   Williams, T J ^b   Burg, D W ^b,c   De Francisci, D ^b   Treu, L ^a   Lauro, F M ^b   Cavicchioli, R ^b  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c ANZAC Research Institute   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEAL PROTEIN;

ADAPTATION; ANTARCTICA; ARTICLE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHANOSARCINACEAE; OPERON; PROTEOMICS; TEMPERATURE;

ADAPTATION, PHYSIOLOGICAL; ANTARCTIC REGIONS; ARCHAEAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ARCHAEAL; METHANOSARCINACEAE; OPERON; PROTEOMICS; TEMPERATURE;

ARCHAEA; HALOBACTERIUM SALINARUM; METHANOCOCCOIDES BURTONII;

EID: 80051911251     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02367.x     Document Type: Article

References (72)

1. Adams, H.E., Crump, B.C., and Kling, G.W. (2010) Temperature controls on aquatic bacterial production and community dynamics in arctic lakes and streams. Environ Microbiol 12: 1319-1333.
2. Allen, M.A., Lauro, F.M., Williams, T.J., Burg, D., Siddiqui, K.S., De Francisci, D., etal. (2009) The genome sequence of the psychrophilic archaeon, Methanococcoides burtonii: the role of genome evolution in cold adaptation. ISME J 3: 1012-1035.
3. Allenby, N.E., O'Connor, N., Pragai, Z., Carter, N.M., Miethke, M., Engelmann, S., etal. (2004) Post-transcriptional regulation of the Bacillus subtilis pst operon encoding a phosphate-specific ABC transporter. Microbiology 150: 2619-2628.
4. Amato, P., Doyle, S., and Christner, B.C. (2009) Macromolecular synthesis by yeasts under frozen conditions. Environ Microbiol 11: 589-596.
5. Anantharaman, V., Koonin, E.V., and Aravind, L. (2001) TRAM, a predicted RNA-binding domain, common to tRNA uracil methylation and adenine thiolation enzymes. FEMS Microbiol Lett 197: 215-221.
6. Baranov, P.V., Kubarenko, A.V., Gurvich, O.L., Shamolina, T.A., and Brimacombe, R. (1999) The database of ribosomal cross-links: an update. Nucleic Acids Res 27: 184-185.
7. Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: signalP 3.0. J Mol Biol 340: 783-795.
8. Bergholz, P.W., Bakermans, C., and Tiedje, J.M. (2009) Psychrobacter arcticus 273-4 uses resource efficiency and molecular motion adaptations for subzero temperature growth. J Bacteriol 191: 2340-2352.
9. Broeze, R.J., Solomon, C.J., and Pope, D.H. (1978) Effects of low temperature on in vivo and in vitro protein synthesis in Escherichia coli and Pseudomonas fluorescens. J Bacteriol 134: 861-874.
10. Brouwer, R.W., Kuipers, O.P., and van Hijum, S.A. (2008) The relative value of operon predictions. Brief Bioinform 9: 367-375.
11. Budde, I., Steil, L., Scharf, C., Volker, U., and Bremer, E. (2006) Adaptation of Bacillus subtilis to growth at low temperature: a combined transcriptomic and proteomic appraisal. Microbiology 152: 831-853.
12. Burg, D.W., Lauro, F.M., Williams, T.J., Raftery, M.J., Guilhaus, M., and Cavicchioli, R. (2010) Analyzing the hydrophobic proteome of the antarctic archaeon Methanococcoides burtonii using differential solubility fractionation. J Proteome Res 9: 664-676.
13. Cavicchioli, R. (2006) Cold-adapted archaea. Nat Rev Microbiol 4: 331-343.
14. Coker, J.A., DasSarma, P., Kumar, J., Muller, J.A., and DasSarma, S. (2007) Transcriptional profiling of the model Archaeon Halobacterium sp. NRC-1: responses to changes in salinity and temperature. Saline Systems 3: 6.
15. Dalluge, J.J., Hamamoto, T., Horikoshi, K., Morita, R.Y., Stetter, K.O., and McCloskey, J.A. (1997) Posttranscriptional modification of tRNA in psychrophilic bacteria. J Bacteriol 179: 1918-1923.
16. Ermolaeva, M.D., Khalak, H.G., White, O., Smith, H.O., and Salzberg, S.L. (2000) Prediction of transcription terminators in bacterial genomes. J Mol Biol 301: 27-33.
17. Farnham, P.J. (2009) Insights from genomic profiling of transcription factors. Nat Rev Genet 10: 605-616.
18. Feller, G., and Gerday, C. (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1: 200-208.
19. Franzmann, P.D., Springer, N., Ludwig, W., Conway de Macario, E., and Rohde, M. (1992) A methanogenic archaeon from ace lake, antarctica: Methanococcoides burtonii sp. nov. Syst Appl Microbiol 15: 573-581.
20. 2-using methanogen from ace lake, antarctica. Int J Syst Bacteriol 47: 1068-1072.
21. Frols, S., Ajon, M., Wagner, M., Teichmann, D., Zolghadr, B., Folea, M., etal. (2008) UV-inducible cellular aggregation of the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by pili formation. Mol Microbiol 70: 938-952.
22. Goodchild, A., Raftery, M., Saunders, N.F., Guilhaus, M., and Cavicchioli, R. (2004a) Biology of the cold adapted archaeon, Methanococcoides burtonii determined by proteomics using liquid chromatography-tandem mass spectrometry. J Proteome Res 3: 1164-1176.
23. Goodchild, A., Saunders, N.F., Ertan, H., Raftery, M., Guilhaus, M., Curmi, P.M., and Cavicchioli, R. (2004b) A proteomic determination of cold adaptation in the antarctic archaeon, Methanococcoides burtonii. Mol Microbiol 53: 309-321.
24. Goodchild, A., Raftery, M., Saunders, N.F., Guilhaus, M., and Cavicchioli, R. (2005) Cold adaptation of the antarctic archaeon, Methanococcoides burtonii assessed by proteomics using ICAT. J Proteome Res 4: 473-480.
25. Grunden, A.M., and Shanmugam, K.T. (1997) Molybdate transport and regulation in bacteria. Arch Microbiol 168: 345-354.
26. Hochheimer, A., Linder, D., Thauer, R.K., and Hedderich, R. (1996) The molybdenum formylmethanofuran dehydrogenase operon and the tungsten formylmethanofuran dehydrogenase operon from Methanobacterium thermoautotrophicum: structures and transcriptional regulation. Eur J Biochem 242: 156-162.
27. Kall, L., Krogh, A., and Sonnhammer, E.L. (2007) Advantages of combined transmembrane topology and signal peptide prediction - the phobius web server. Nucleic Acids Res 35: W429-W432.
28. Kanehisa, M., and Goto, S. (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30.
29. Koide, T., Reiss, D.J., Bare, J.C., Pang, W.L., Facciotti, M.T., Schmid, A.K., etal. (2009) Prevalence of transcription promoters within archaeal operons and coding sequences. Mol Syst Biol 5: 285.
30. Kramer, G., Rauch, T., Rist, W., Vorderwulbecke, S., Patzelt, H., Schulze-Specking, A., etal. (2002) L23 protein functions as a chaperone docking site on the ribosome. Nature 419: 171-174.
31. Kruger, M., Treude, T., Wolters, H., Nauhaus, K., and Boetius, A. (2005) Microbial methane turnover in different marine habitats. Palaeogeogr Palaeoclimatol Palaeoecol 227: 6-17.
32. Laksanalamai, P., Narayan, S., Luo, H., and Robb, F.T. (2009) Chaperone action of a versatile small heat shock protein from Methanococcoides burtonii, a cold adapted archaeon. Proteins 75: 275-281.
33. Lauro, F.M., Allen, M., Wilkins, D., Williams, T.J., and Cavicchioli, R. (2010) Genetics, genomics and evolution of psychrophiles. In Extremophiles Handbook. Horikoshi, K. (ed.). Tokyo, Japan: Springer Japan KK (in press). doi: 10.1007/978-4-431-53898-1-6.6.
34. Li, C., Geering, K., and Horisberger, J.D. (2006) The third sodium binding site of Na, K-ATPase is functionally linked to acidic pH-activated inward current. J Membr Biol 213: 1-9.
35. Lim, J., Thomas, T., and Cavicchioli, R. (2000) Low temperature regulated DEAD-box RNA helicase from the antarctic archaeon, Methanococcoides burtonii. J Mol Biol 297: 553-567.
36. Little, B., Wagner, P., Ray, R., Pope, R., and Scheetz, R. (1991) Biofilms: an ESEM evaluation of artifacts introduced during SEM preparation. J Industrial Microbiol 8: 213-222.
37. Liu, S., Graham, J.E., Bigelow, L., Morse, P.D., 2nd, and Wilkinson, B.J. (2002) Identification of Listeria monocytogenes genes expressed in response to growth at low temperature. Appl Environ Microbiol 68: 1697-1705.
38. Macario, A.J., and Conway De Macario, E. (2001) The molecular chaperone system and other anti-stress mechanisms in archaea. Front Biosci 1: D262-D283.
39. Macke, T.J., Ecker, D.J., Gutell, R.R., Gautheret, D., Case, D.A., and Sampath, R. (2001) RNAMotif, an RNA secondary structure definition and search algorithm. Nucleic Acids Res 29: 4724-4735.
40. Mahapatra, A., Patel, A., Soares, J.A., Larue, R.C., Zhang, J.K., Metcalf, W.W., and Krzycki, J.A. (2006) Characterization of a Methanosarcina acetivorans mutant unable to translate UAG as pyrrolysine. Mol Microbiol 59: 56-66.
41. von Mering, C., Huynen, M., Jaeggi, D., Schmidt, S., Bork, P., and Snel, B. (2003) STRING: a database of predicted functional associations between proteins. Nucleic Acids Res 31: 258-261.
42. Meuer, J., Kuettner, H.C., Zhang, J.K., Hedderich, R., and Metcalf, W.W. (2002) Genetic analysis of the archaeon Methanosarcina barkeri fusaro reveals a central role for ech hydrogenase and ferredoxin in methanogenesis and carbon fixation. Proc Natl Acad Sci USA 99: 5632-5637.
43. Murray, A.E., and Grzymski, J.J. (2007) Diversity and genomics of antarctic marine micro-organisms. Philos Trans R Soc Lond B Biol Sci 362: 2259-2271.
44. Nichols, D.S., Miller, M.R., Davies, N.W., Goodchild, A., Raftery, M., and Cavicchioli, R. (2004) Cold adaptation in the antarctic archaeon Methanococcoides burtonii involves membrane lipid unsaturation. J Bacteriol 186: 8508-8515.
45. Noon, K.R., Guymon, R., Crain, P.F., McCloskey, J.A., Thomm, M., Lim, J., and Cavicchioli, R. (2003) Influence of temperature on tRNA modification in archaea: Methanococcoides burtonii (optimum growth temperature [topt], 23 degrees C) and Stetteria hydrogenophila (topt, 95 degrees C). J Bacteriol 185: 5483-5490.
46. Ozcan, N., Ejsing, C.S., Shevchenko, A., Lipski, A., Morbach, S., and Kramer, R. (2007) Osmolality, temperature, and membrane lipid composition modulate the activity of betaine transporter BetP in Corynebacterium glutamicum. J Bacteriol 189: 7485-7496.
47. Pavesi, G., Mereghetti, P., Mauri, G., and Pesole, G. (2004) Weeder web: discovery of transcription factor binding sites in a set of sequences from co-regulated genes. Nucleic Acids Res 32: W199-W203.
48. Phadtare, S., and Inouye, M. (2004) Genome-wide transcriptional analysis of the cold shock response in wild-type and cold-sensitive, quadruple-csp-deletion strains of Escherichia coli. J Bacteriol 186: 7007-7014.
49. Pogliano, K.J., and Beckwith, J. (1993) The cs sec mutants of Escherichia coli reflect the cold sensitivity of protein export itself. Genetics 133: 763-773.
50. Price, M.N., Huang, K.H., Alm, E.J., and Arkin, A.P. (2005) A novel method for accurate operon predictions in all sequenced prokaryotes. Nucleic Acids Res 33: 880-892.
51. Priester, J.H., Horst, A.M., Van de Werfhorst, L.C., Saleta, J.L., Mertes, L.A., and Holden, P.A. (2007) Enhanced visualization of microbial biofilms by staining and environmental scanning electron microscopy. J Microbiol Methods 68: 577-587.
52. Rabinovich, A., Jin, V.X., Rabinovich, R., Xu, X., and Farnham, P.J. (2008) E2F in vivo binding specificity: comparison of consensus versus nonconsensus binding sites. Genome Res 18: 1763-1777.
53. Reid, I.N., Sparks, W.B., Lubnow, S., McGrath, M., Livio, M., Valenti, J., etal. (2006) Terrestrial models for extraterrestrial life: methanogens and halophiles at martian temperatures. Int J Astrobiol 5: 89-97.
54. Robador, A., Brüchert, V., and Jørgensen, B.B. (2009) The impact of temperature change on the activity and community composition of sulfate-reducing bacteria in arctic versus temperate marine sediments. Environ Microbiol 11: 1692-1703.
55. Russell, N.J. (2008) Membrane components and cold sensing. In Psychrophiles: From Biodiversity to Biotechnology. Membrane Components and Cold Sensing. Margesin, R., Schinner, F., Marx, J.-C., and Gerday, C. (eds). Berlin Heidelberg, Germany: Springer, pp. 177-190.
56. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M.A., and Barrell, B. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
57. Saunders, N.F., Thomas, T., Curmi, P.M., Mattick, J.S., Kuczek, E., Slade, R., etal. (2003) Mechanisms of thermal adaptation revealed from the genomes of the antarctic archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Res 13: 1580-1588.
58. Saunders, N.F., Goodchild, A., Raftery, M., Guilhaus, M., Curmi, P.M., and Cavicchioli, R. (2005) Predicted roles for hypothetical proteins in the low-temperature expressed proteome of the antarctic archaeon Methanococcoides burtonii. J Proteome Res 4: 464-472.
59. Saunders, N.F., Ng, C., Raftery, M., Guilhaus, M., Goodchild, A., and Cavicchioli, R. (2006) Proteomic and computational analysis of secreted proteins with type I signal peptides from the antarctic archaeon Methanococcoides burtonii. J Proteome Res 5: 2457-2464.
60. Siddiqui, K.S., and Cavicchioli, R. (2006) Cold-adapted enzymes. Annu Rev Biochem 75: 403-433.
61. Sowers, K., Boone, J.E., and Gunsalus, R.P. (1993) Disaggregation of Methanosarcina spp. and growth as single cells at elevated osmolarity. Appl Environ Microbiol 59: 3832-3839.
62. Sowers, K.R., and Gunsalus, R.P. (1995) Halotolerance in Methanosarcina spp.: role of N(sup(epsilon))-acetyl-(beta)-lysine, (alpha)-glutamate, glycine betaine, and K(sup+) as compatible solutes for osmotic adaptation. Appl Environ Microbiol 61: 4382-4388.
63. Stothard, P., and Wishart, D.S. (2005) Circular genome visualization and exploration using CGView. Bioinformatics 21: 537-539.
64. Thijs, G., Lescot, M., Marchal, K., Rombauts, S., De Moor, B., Rouze, P., and Moreau, Y. (2001) A higher-order background model improves the detection of promoter regulatory elements by gibbs sampling. Bioinformatics 17: 1113-1122.
65. Ting, L., Williams, T.J., Cowley, M.J., Lauro, F.M., Guilhaus, M., Raftery, M.J., and Cavicchioli, R. (2010) Cold adaptation in the marine bacterium, Sphingopyxis alaskensis, assessed using quantitative proteomics. Environ Microbiol 12: 2658-2676.
66. Toledo-Arana, A., Dussurget, O., Nikitas, G., Sesto, N., Guet-Revillet, H., Balestrino, D., etal. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950-956.
67. Tusher, V.G., Tibshirani, R., and Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121.
68. Vernikos, G.S., and Parkhill, J. (2006) Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22: 2196-2203.
69. Vetter, Y.A., Deming, J.W., Jumars, P.A., and Krieger-Brockett, B.B. (1998) A predictive model of bacterial foraging by means of freely released extracellular enzymes. Microb Ecol 36: 75-92.
70. Williams, T.J., Burg, D.W., Raftery, M.J., Poljak, A., Guilhaus, M., Pilak, O., and Cavicchioli, R. (2010a) Global proteomic analysis of the insoluble, soluble, and supernatant fractions of the psychrophilic archaeon Methanococcoides burtonii part I: the effect of growth temperature. J Proteome Res 9: 640-652.
71. Williams, T.J., Burg, D.W., Ertan, H., Raftery, M.J., Poljak, A., Guilhaus, M., and Cavicchioli, R. (2010b) Global proteomic analysis of the insoluble, soluble, and supernatant fractions of the psychrophilic archaeon Methanococcoides burtonii part II: the effect of different methylated growth substrates. J Proteome Res 9: 653-663.
72. Zeeberg, B.R., Feng, W., Wang, G., Wang, M.D., Fojo, A.T., Sunshine, M., etal. (2003) GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol 4: R28.