Global Proteomic Analysis of the Insoluble, Soluble, and Supernatant Fractions of the Psychrophilic Archaeon Methanococcoides burtonii Part I: The Effect of Growth Temperature Timothy J. Williams,†,‡ Dominic W. Burg,†,‡ Mark J. Raftery,§ Anne Poljak,§,| Michael Guilhaus,§ Oliver Pilak,‡ and Ricardo Cavicchioli*,‡ School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, 2052, NSW, Australia, Bioanalytical Mass Spectrometry Facility, The University of New South Wales, Sydney, 2052, NSW, Australia, and School of Medical Sciences, The University of New South Wales, Sydney, 2052, Australia Received June 10, 2009
The response of the cold-adapted (psychrophilic) methanogenic archaeon Methanococcoides burtonii to growth temperature was investigated using differential proteomics (postincorporation isobaric labeling) and tandem liquid chromatography-mass spectrometry (LC/LC-MS/MS). This is the first proteomic study of M. burtonii to include techniques that specifically enrich for both surface and membrane proteins and to assess the effects of growth temperature (4 vs 23 °C) and carbon source (trimethylamine vs methanol) on cellular protein levels. Numerous surface layer proteins were more abundant at 4 °C, indicating an extensive remodeling of the cell envelope in response to low temperature. Many of these surface proteins contain domains associated with cell adhesion. Within the cell, small proteins each composed of a single TRAM domain were recovered as important cold adaptation proteins and might serve as RNA chaperones, in an analogous manner to Csp proteins (absent from M. burtonii). Other proteins that had higher abundances at 4 °C can be similarly tied to relieving or resolving the adverse affects of cold growth temperature on translational capacity and correct protein folding. The proteome of M. burtonii grown at 23 °C was dominated by oxidative stress proteins, as well as a large number of integral membrane proteins of unknown function. This is the first truly global proteomic study of a psychrophilic archaeon and greatly expands knowledge of the cellular mechanisms underpinning cold adaptation in the Archaea. Keywords: proteome • LC/LC-MS/MS • iTRAQ • membrane protein • archaea • methanogen • psychrophile • methylotroph • cell envelope • S-layer • nucleic acid binding • oxidative stress • translation • transcriptional regulator
Earth’s biosphere is dominated by naturally cold environments (e.g., polar, alpine, deep ocean, seasonally cold habitats), and microbial life has evolved to proliferate throughout all of these regions. Polar environments in particular are very sensitive to changes in global temperature and play critical roles in maintaining microbial processes that are central to ensuring the world’s ecosystems remain balanced and productive.1 Studies examining cold adapted (psychrophilic) members of the Archaea, Bacteria, and Eucarya have revealed that certain molecular mechanisms of adaptation are characteristic of psychrophiles across all lineages.2,3 Some mechanisms of adaptation may be expected to be shared across all psychro-
philes given that microorganisms are isothermal and have to contend with the same impacts that temperatures at or close to freezing have on reaction rates and the structures of cellular components. The latter include impositions caused by increased stability of inhibitory RNA secondary structures, decreased translational capacity, and reduced membrane fluidity.2,4 However, evolution has resulted in some microbial lineages being superior in terms of their capacity to thermally adapt. This is well illustrated by the methanogenic archaea, the only microbial group known to be able to grow at temperatures as high as 122 °C5 or as low as -2 °C6 and all temperatures in between. There is clearly a need to better understand those elements that are fundamental to cold adaptation and those that are specific to particular groups or individual species.
* To whom correpondence should be addressed. Rick Cavicchioli, School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, 2052, NSW, Australia. E-mail
[email protected]; Tel. (+61) 2 9385 3516; Fax (+61) 2 9385 2742. † These authors contributed equally. ‡ School of Biotechnology and Biomolecular Sciences. § Bioanalytical Mass Spectrometry Facility. | School of Medical Sciences.
Within the domain Archaea, few psychrophilic isolates are available for study, and the Antarctic archaeon Methanococcoides burtonii has developed into a robust model for assessing molecular mechanisms of cold adaptation.3 M. burtonii is a methylotrophic methanogen adapted to growth at temperatures of 1-2 °C that exists at the bottom of Ace Lake.3,7 Several thousand years ago, Ace Lake was connected to the Southern
Introduction
640 Journal of Proteome Research 2010, 9, 640–652 Published on Web 12/01/2009
10.1021/pr900509n
2010 American Chemical Society
research articles
Part I: The Effect of Growth Temperature 8
Ocean as a marine basin. While the lake is now a stable meromictic system with an upper-aerobic and bottom-anaerobic zone, the microbiota in the lake, including M. burtonii, are derived from the ocean. The history of the lake therefore provides a unique opportunity to study the evolution of marine microbes. Recently, the genome sequence of M. burtonii was completed, revealing a range of novel characteristics associated with its adaptation and evolution to life in a cold lake system.9 A particular feature of the genomic analysis was the important roles ascribed to genes involved in membrane and cell envelope biogenesis and genes encoding integral membrane proteins such as transporters. Despite being isolated from permanently cold waters and being able to grow at subzero temperatures, M. burtonii is capable of growth up to a maximum temperature of ∼28 °C; this temperature response classifies it as a eurypsychrophile.2,3 This capacity to tolerate a wide range of temperatures extending into the mesophilic range is typical of many microbes isolated from permanently cold environments. However, although elevated temperatures can be tolerated, temperatures that generate the fastest rates of growth (Topt) can be stressful for psychrophiles. For M. burtonii, Topt is 23 °C, a growth temperature at which the cells experience heat stress.2,3 Previous proteomic studies of M. burtonii have characterized whole-cell, soluble proteins using tandem liquid chromatography-tandem mass spectrometry (LC/LC-MS/MS) to gain a snapshot of proteins synthesized during growth at 4 °C,10 and 2D-PAGE LC-MS/MS and ICAT has been developed to initiate quantitative proteomics of cells growing at 4 vs 23 °C.11,12 In addition, LC/LC-MS/MS methods were developed for the analysis of secreted proteins.13 These studies have been restricted to growth in complex media (MFM) that provides trimethylamine (TMA) as a carbon source. In the present study, we extended proteomic analyses to include growth of M. burtonii in defined media with methanol as substrate (M-medium), enabling us to identify new proteins specific to cold adaptation under these growth conditions. By comparing proteome profiles for cells growing at 4 and 23 °C, we were able to identify core proteins involved in growth temperature specific adaptation. By comparing proteome profiles for cells growing in MFM and M-medium, we were also able to investigate responses to differences in carbon sources (TMA vs methanol) and to defined vs complex media; this work is presented in Part II14 of this study. In view of the genomic analysis highlighting the importance of cell envelope, membrane, and secreted proteins (see above), we developed new methods for analyzing less soluble proteins. To achieve quantitative proteomics with multiple growth conditions, we utilized isobaric tags for quantification (iTRAQ) enabling the nonspecific labeling of the N-terminus of expressed proteins.15 By performing quantitative proteomics on soluble, insoluble, and secreted fractions of cells grown at 4 and 23 °C in MFM and M-medium, we achieved for the first time a thorough assessment of both thermal (this work) and metabolic (Part II14) adaptation in M. burtonii.
Experimental Procedures Culture Conditions. M. burtonii (DSM 6242) cultures were grown in MFM.7,11 M-medium (pH 6.8) is based on Sowers,16 and contained: 23.38 g L-1 NaCl, 12.32 g L-1 MgSO4.6H2O, 0.76 g L-1 KCl, 0.14 g L-1 CaCl2.2H2O, 0.5 g L-1 NH4Cl, 1 mg L-1 resazurin, 10 mL vitamin solution (as for MFM), 10 mL mineral solution (as for MFM), 0.2 mL L-1 32% (v/v) HCl, 0.75 g L-1
-1
thioglycolic acid, 1.12 g L Na2HPO4.7H2O, 0.25 g L-1 -1 cysteine · HCl · H2O, and 3 g L Na2CO3. After autoclaving, Na2S (0.025% w/v final concentration) and methanol (50 mM final concentration added as two equal aliquots during growth) were added anaerobically. M. burtonii was grown in 100 mL volumes of MFM and M-medium at 4 or 23 °C under a gas phase of 80:20 N2/CO2. Cultures were inoculated 1:100 from cultures grown under the same conditions. Harvesting of M. burtonii Cultures and Fraction Separation. Three fractions were obtained from each harvested culture: supernatant (enriched for secreted proteins), insoluble (enriched for integral membrane, membrane-associated proteins, and dense macromolecular complexes), and soluble. Cultures were harvested at late logarithmic phase (optical density at 620 nm [OD620] of 0.25) by centrifugation at 3200× g for 35 min at 4 °C. The supernatant was filtered through a 15 mL Amicon centrifugal concentration unit (Millipore, Billerica, MA) with a 3 kDa cutoff by centrifugation at 5000× g, with at least two subsequent buffer exchanges with 25 mM NaHCO3. The resulting filtrate constituted the supernatant fraction.13 The insoluble and soluble fractions were separated using a method modified from Blonder et al.17 The cell pellet was suspended by vortexing in 1 mL disruption buffer (50 mM Tris.Cl; 2 mM EDTA, pH 7.2; 0.4 mM phenylmethanesulphonylfluoride). The pellet was ultrasonically disrupted on ice using a digital sonifier 250 (Branson Ultrasonics, Danbury, CT). The resulting suspension was diluted to 10 mL in ice-cold 0.1 M NaCO3 pH 11.2 and agitated on a shaker in an ice-water bath for 1 h. The suspension was transferred to 5 mL OptiSeal tubes (Beckman Coulter, Palo Alto, CA), and ultracentrifuged for 1 h at 115 000× g. The resulting supernatant was retained and filtered, as described above for the supernatant fraction, to generate the soluble fraction. The insoluble pellet was washed twice with dH2O, and then 25 mM NaHCO3 was added for a further round of ultracentrifugation (115 000× g, 20 min). The resulting supernatant was discarded. The pellet was resuspended in 2 mL of 25 mM NaHCO3 by brief sonication and concentrated in a centrifugal concentrator as described above. This homogenate was the insoluble fraction. Insoluble protein fractions required solubilization prior to trypsin digestion; this was achieved by thermally denaturing the proteins at 90 °C for 2 min, adding HPLC grade methanol to a final methanol concentration of 60% (v/v), and briefly sonicating the proteinsolvent mixture. The amount of protein in each cellular fraction was estimated at 595 nm using the method of Bradford18 with bovine serum albumin as the standard. The integrity of the cell pellet was determined by measuring the activity ratio of the cytoplasmic enzyme glutamate dehydrogenase (GDH) in the soluble and supernatant fractions.13 GDH activity was ∼1:10 between soluble and supernatant assays, for cells grown at 4 and 23 °C in MFM and M-medium, illustrating that cells under all growth conditions had remained relatively intact during processing.13 The relative abundance of the GDH protein in the soluble and supernatant fractions was also measured using iTRAQ labeling (see below) and found to be ∼1:10. Sample Preparation for iTRAQ Labeling and LC/LC-MS/ MS. The 4plex iTRAQ postincorporation labeling system (Applied Biosystems, Forster City, CA) was used according to the manufacturer’s instructions.15 Four separate comparisons were carried out for each fraction (soluble, insoluble, supernatant): 4 vs 23 °C for cells grown in MFM; 4 vs 23 °C for cells grown in M-medium; cells grown in MFM vs M-medium at 4 °C; cells Journal of Proteome Research • Vol. 9, No. 2, 2010 641
research articles grown in MFM vs M-medium at 23 °C. The 4plex iTRAQ system allows 4 samples to be labeled per LC/LC-MS/MS run. Two samples for each condition were included per run, as biological replicates. All labeling experiments were run twice (2 separate injections) using LC/LC-MS/MS, to provide a technical replicate. Six labeling experiments were performed for each culture condition, which resulted in 12 biological replicates and a total of 12 LC/LC-MS/MS runs per culture condition. Prior to iTRAQ labeling, protein samples (50 µg) were reduced, alkylated, and digested. Samples of soluble, supernatant, and insoluble fractions were treated with 1 µL of 1% sodium dodecyl sulfate (SDS), then reduced with either 2 µL of tris(2-carboxyethyl)phosphine (1 mM soluble and supernatant fractions) or 5 µL of 0.1 M dithiothreitol (insoluble fraction) and incubated in the dark at 60 °C for 60 min. All samples were alkylated with iodoacetamide (2 mM for soluble and supernatant fractions, 15 mM for insoluble fraction), and incubated in the dark at 60 °C for 60 min. Supernatant and soluble protein fractions were then digested using 0.5 µg trypsin per 50 µg protein (sequencing grade porcine modified trypsin; Promega, Madison, WI) and incubated for 16 h at 37 °C. Insoluble protein fractions required solubilization prior to trypsin digestion; this was achieved by thermally denaturing the proteins at 90 °C for 2 min, adding HPLC grade methanol to a final methanol concentration of 60% (v/v), and briefly sonicating the proteinsolvent mixture. Trypsin was added to the mixture (2.5 µg trypsin per 50 µg protein), which was incubated for 5 h at 37 °C. The samples were then labeled with the iTRAQ labeling system according to the manufacturer’s instructions, and then combined. To remove any unbound iTRAQ labels, trypsin, SDS, solvents, etc., the combined samples were cleaned-up using strong cation exchange (SCX) chromatography followed by reverse phase (RP) chromatography. Soluble and supernatant fraction samples could proceed directly to SCX, but insoluble fraction samples were vacuum-dried, and sample pellets were resuspended in 5 mL of load buffer (10 mM KH2PO4, 25% acetonitrile [ACN], pH 3.0) and centrifuged at 5000× g for 5 min at 4 °C and the supernatant was retained for SCX. An Applied Biosystems Opti-Lynx cartridge/holder and a syringe pump (KD Scientific, Holliston, MA) at a flow rate of 9.5 mL h-1 were used for SCX. The eluted peptide solutions were vacuum-dried, and the pellet resuspended in 500 µL of 0.2% heptafluorobutyric acid (HFBA). A RP peptide macrotrap (Microm Bioresources, Auburn, CA) was used and prepared by washing with 1 mL ACN, then 1 mL ACN:0.25% formic acid (1:1), followed by equilibration using 1 mL of 0.2% HFBA. The peptides were loaded, and the column washed with 1.5 mL 0.2% HFBA. Peptides were eluted with 500 µL ACN:0.25% (v/v) formic acid (50:50), followed by 500 µL ACN. For peptides derived from all three cellular fractions, the eluent was vacuumdried and the pellet dissolved in 50 µL 1% formic acid, 0.05% HFBA. Mass Spectrometry and Data Analysis. Solubilized peptides were separated online with automated high throughput SCX and nano C18 LC using an Ultimate HPLC, Switchos and Famos autosampler system (LC-Packings, Amsterdam, Netherlands), and eluted stepwise with increasing concentrations of ammonium acetate (11). Samples were analyzed using an API QStar Pulsar i hybrid tandem mass spectrometer (Applied Biosystems, Foster City, CA) operated in information dependent acquisition mode. Peptides were eluted using a linear acetonitrile gradient. A time-of-flight (TOF) MS survey scan was 642
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Williams et al. acquired (m/z 350-1700, 1s). The 3 largest multiply charged ions (counts >25) were sequentially selected by the quadrupole for MS-MS analysis.19 Tandem mass spectra were accumulated for 2.5s (m/z 65-2000). Peak lists were generated using Mascot Distiller (Matrix Science, London, UK) using the default parameters. MS data were searched using Mascot against an in silico digestion of the local M. burtonii protein FASTA database created in Mascot, with appropriate parameters (tryptic digestion; variable modifications of carbamidomethylation; methionine oxidation; 4-plex iTRAQ; peptide ion mass tolerance (0.25 Da; fragment ion mass tolerance (0.2 Da; maximum number of missed cleavages set to 1). A typical fragmentation spectrum is shown in Figure S1 (Supporting Information). A decoy database created by randomizing the M. burtonii local FASTA database, created with Mascot, was also searched with the same parameters. All spectra which matched the databases with a Mowse score of 30 were manually inspected to ensure ion progressions of 4 or more consecutive ions of a single class (e.g., y- or b-type ions); any matches that did not meet these criteria were rejected. From the identifications in both the M. burtonii database and the decoy database it was possible to calculate the false discovery rate (FDR) for any given experimental run.20 Any experiment that had a FDR > 0.02 was rejected. Identifications were then moved to a database for further processing. iTRAQ abundance data were determined using ProQuant software (Build 7051; Applied Biosystems, Foster City, CA) and searched against the local M. burtonii interrogator database (MS tolerance 0.2 Da; MS/MS tolerance 0.15 Da; store hits with confidence >99%; charge range for intermediate precursors of g2, e4; maximum number of missed cleavages 1; modifications: iTRAQ reagents, acetamidomethyl-cysteine, methionine sulfoxide, with maximum number of modifications set to 8; correction factors entered from the iTRAQ certificate of analysis). Data were visualized using ProGroup Viewer version 1.0.5 (Applied Biosystems, Foster City, CA). We used SPSS release 17.0.1 (IBM, Armonk, NY) to compare data variability in biological vs technical replicates of proteins identified by iTRAQ labeling and ProQuant. These demonstrated that data were reproducible across biological and technical replicates; representative scatter plots are shown in Figure S2 (Supporting Information). Data were inspected for variation in abundance (p < 0.05), with error factor (EF) values 1.5 fold) in the expressed proteome. Figure S1 shows a typical fragmentation spectrum for a peptide derived from Mbur_1950 (DEAD box RNA helicase). Figure S2 shows a scatter plot to demonstrate reproducibility across samples (biological replicates) and injections (technical replicates). This material is available free of charge via the Internet at http://pubs.acs.org. References (1) Murray, A. E.; Grzymski, J. J. Diversity and genomics of Antarctic marine micro-organisms. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2007, 362, 2259–2271. (2) Feller, G.; Gerday, C. Psychrophilic enzymes: hot topics in cold adaptation. Nat. Rev. Microbiol. 2003, 1, 200–208. (3) Cavicchioli, R. Cold-adapted archaea. Nat. Rev. Microbiol. 2006, 4, 331–343. (4) Cavicchioli, R.; Thomas, T.; Curmi, P. M. G. Cold stress response in Archaea. Extremophiles 2000, 4, 321–331. (5) Takai, K.; Nakamura, K.; Toki, T.; Tsunogai, U.; Miyazaki, M.; Miyazaki, J.; Hirayama, H.; Nakagawa, S.; Nunoura, T.; Horikoshi, K. Cell proliferation at 122°C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 10949–10954. (6) Reid, I. N.; Sparks, W. B.; Lubnow, S.; McGrath, M.; Livio, M.; Valenti, J.; Sowers, K. A.; Shukla, H. D.; MacAuley, S.; Miller, T.; Suvanasuthi, R.; Belas, R.; Colman, A.; Robb, F. T.; DasSarma, P.; Mu ¨ ller, J. A.; Coker, J. A.; Cavicchioli, R.; Chen, F.; DasSarma, S. (2006) Terrestrial models for extraterrestrial life: methanogens and halophiles at Martian temperatures. Int. J. Astrobiol. 2006, 5, 89– 97. (7) Franzmann, P. D.; Springer, N.; Ludwig, W.; Conway De Macario, E.; Rohde, M. A methanogenic archaeon from Ace Lake, Antarctica: Methanococcoides burtonii sp. nov. System. Appl. Microbiol. 1992, 15, 573–581. (8) Rankin, L. M.; Gibson, J. A. E.; Franzmann, P. D.; Burton, H. R. The chemical stratification and microbial communities of Ace Lake, Antarctica: a review of the characteristics of a marine-derived meromictic lake. Polarforschung 1999, 66, 33–52. (9) Allen, M. A.; Lauro, F. M.; Williams, T. J.; Burg, D,; Siddiqui, K. S.; De Franciscii, D.; Chong, K. W. Y.; Pilak, O.; Chew, H. H.; De Maere, M. Z.; Ting, L.; Katrib, M.; Ng, C.; Sowers, K. R.; Galeprin, M. Y.; Anderson, I. J.; Ivanova, N.; Dalin, E.; Martinez, M.; Lapidus, A.; Hauser, L.; Land, M.; Thomas, T.; Cavicchioli, R. The genome sequence of the psychrophilic archaeon, Methanococcoides burtonii: the role of genome evolution in cold-adaptation. ISME J. 2009, 3, 1012–1035. (10) Goodchild, A.; Raftery, M.; Saunders, N. F. W.; Guilhaus, M.; Cavicchioli, R. Biology of the cold adapted archaeon, Methano-
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