Abstract
Cold-adaptive methanogens contribute significantly to methane emission from the cold area, while the cold-adaptive mechanisms used by Archaea remain elusive. Methanolobus psychrophilus R15, a cold-adaptive methanogen isolated from a Tibetan plateau wetland, grows at 0–25 °C and optimally at 18 °C when isolated; however, it grows optimally at 30 °C after culturing at 18 °C for several years. Aiming to gain insights into the protein profiles that are involved in optimal growth and cold adaptation of this methanogen, here, we performed a comparative proteomic study using 2D DIGE on the cultures grown at 30, 18 and 4 °C. 1439 protein spots (3167 ORFs annotated in the R15 genome) were detected, and 202 of 322 differentially expressed protein spots were identified by MALDI-TOF/TOF. The protein abundance of most enzymes involved in methanogenesis, energy conservation and central metabolism were increased at 30 °C, while most ribosome proteins were decreased at 30 °C. Proteasome and ROS scavengers increased expressions at 4 °C, suggesting more aberrant proteins and ROS formed at lower temperatures. Different from the cold-adaptive Methanococcoides burtonii, some chaperones were increased at 4 °C, implying that protein folding was impaired at cold in this psychrophilic archaeon. This study indicates that diverse cold-adaptive mechanisms can be used by different methanogenic Archaea.
Similar content being viewed by others
References
Allen MA, Lauro FM, Williams TJ, Burg D, Siddiqui KS, De Francisci D et al (2009) The genome sequence of the psychrophilic archaeon, Methanococcoides burtonii: the role of genome evolution in cold adaptation. ISME J 3:1012–1035
Bairoch A, Apweiler R (2000) The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res 28:45–48
Berg A, Kockelkorn D, Ramos-Vera WH, Say RF, Zarzycki J, Hügler M et al (2010) Autotrophic carbon fixation in archaea. Nat Rev Microbiol 8:447–460
Bowman JB (2008) Genomic analysis of psychrophilic prokaryotes. In: Margesin R et al (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin/, pp 265–284
Campanaro S, Williams TJ, Burg DW, De Francisci D, Treu L, Lauro FM, Cavicchioli R (2011) Temperature-dependent global gene expression in the Antarctic archaeon Methanococcoides burtonii. Environ Microbiol 13:2018–2038
Cao Y, Li J, Jiang N, Dong X (2014) Mechanism for stabilizing mRNAs involved in methanol-dependent methanogenesis of cold-adaptive Methanosarcina mazei zm-15. Appl Environ Microbiol 80:1291–1298
Chen Z, Yu H, Li L, Hu S, Dong X (2012) The genome and transcriptome of a newly described psychrophilic archaeon, Methanolobus psychrophilus R15, reveal its cold adaptive characteristics. Environ Microbiol Rep 4:633–641
D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389
De Maayer P, Anderson D, Cary C, Cowan DA (2014) Some like it cold: understanding the survival strategies of psychrophiles. EMBO Rep 15:508–517
Farewell A, Neidhardt FC (1998) Effect of temperature on in vivo protein synthetic capacity in Escherichia coli. J Bacteriol 180:4704–4710
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282
Ferry JG (1992) Biochemistry of methanogenesis. Crit Rev Biochem Mol Biol 27:473–503
Finn MW, Tabita FR (2004) Modified pathway to synthesize ribulose 1, 5-bisphosphate in methanogenic Archaea. J Bacteriol 186:6360–6366
Franzmann PD, Stringer N, Ludwig W, Conway De Macario E, Rohde M (1992) A methanogenic archaeon from Ace Lake, Antarctica: Methanococcoides burtonii sp. nov. Sys Appl Microbiol 15:573–581
Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57:395–418
Jiang N, Wang Y, Dong X (2010) Methanol as the primary methanogenic and acetogenic precursor in the cold Zoige wetland at Tibetan plateau. Microb Ecol 60:206–213
Jones WJ, Nagle DP Jr, Whitman WB (1987) Methanogens and the diversity of archaebacteria. Microbiol Rev 51:135–177
Maaloe O (1979) Regulation of the protein synthesizing machinery-ribosomes, tRNA, factors, and so on. Biological regulation and development. Plenum Publishing Corp, New York, pp 487–542
Neidhardt FC, Ingraham JL, Schaechter M (1990) Physiology of the bacterial cell: a molecular approach. Sinauer Associates, Inc, Sunderland, p p507
Nichols DS, Miller MR, Davies NW, Goodchild A, Raftery M, Cavicchioli R (2004) Cold adaptation in the Antarctic Archaeon Methanococcoides burtonii involves membrane lipid unsaturation. J Bacteriol 186:8508–8515
Noon KR, Guymon R, Crain PF, McCloskey JA, Thomm M, Lim J, Cavicchioli R (2003) Influence of temperature on tRNA modification in archaea: Methanococcoides burtonii [optimum growth temperature (Topt), 23°C] and Stetteria hydrogenophila (Topt, 95°C). J Bacteriol 185:5483–5490
Piette F, D’Amico S, Mazzucchelli G, Danchin A, Leprince P, Feller G (2011a) Life in the cold: a proteomic study of cold-repressed proteins in the antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Appl Environ Microbiol 77:3881–3883
Piette F, Struvay C, Feller G (2011b) The protein folding challenge in psychrophiles: facts and current issues. Environ Microbiol 13:1924–1933
Rodrigues DF, Tiedje JM (2008) Coping with our cold planet. Appl Environ Microbiol 74:1677–1686
Sato T, Atomi H, Imanaka T (2007) Archaeal type III RuBisCOs function in a pathway for AMP metabolism. Science 315:1003–1006
Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51
Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS et al (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28
Thomas T, Kumar N, Cavicchioli R (2001) Effects of ribosomes and intracellular solutes on activities and stabilities of elongation factor 2 proteins from psychrotolerant and thermophilic methanogens. J Bacteriol 183:1974–1982
Ting L, Williams TJ, Cowley MJ, Lauro FM, Guilhaus M, Raftery MJ, Cavicchioli R (2010) Cold adaptation in the marine bacterium, Sphingopyxis alaskensis, assessed using quantitative proteomics. Environ Microbiol 12:2658–2676
Verhees CH, Tuininga JE, Kengen SW, Stams AJ, van der Oost J, de Vos WM (2001) ADP-dependent phosphofructokinases in mesophilic and thermophilic methanogenic archaea. J Bacteriol 183:7145–7153
Verhees CH, Kengen SW, Tuininga JE, Schut GJ, Stams AJ, de Vos WM, van der Oost J (2003) The unique features of glycolytic pathways in Archaea. Biochem J 375:231–246
Williams TJ, Burg DW, Raftery MJ, Poljak A, Guilhaus M, Pilak O, Cavicchioli R (2010) 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
Williams TJ, Lauro FM, Ertan H, Burg DW, Poljak A, Raftery MJ, Cavicchioli R (2011) Defining the response of a microorganism to temperatures that span its complete growth temperature range (−2 to 28 °C) using multiplex quantitative proteomics. Environ Microbiol 13:2186–2203
Zhang G, Jiang N, Liu X, Dong X (2008) Methanogenesis from methanol at low temperature by a novel psychrophilic methanogen, Methanolobus psychrophilus sp. nov., prevalent in Zoige wetland of Tibetan Plateau. Appl Environ Microbiol 74:6114–6161
Acknowledgments
This work was supported by National Natural Science foundation of China under No. 30621005, 30830007 and Y2113B5531.
Conflict of interest
The authors have declared no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by H. Atomi.
Z. Chen and D. Feng contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chen, Z., Feng, D., Zhang, B. et al. Proteomic insights into the temperature responses of a cold-adaptive archaeon Methanolobus psychrophilus R15. Extremophiles 19, 249–259 (2015). https://doi.org/10.1007/s00792-014-0709-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-014-0709-y