Advertisement

Extremophiles

, Volume 23, Issue 1, pp 101–118 | Cite as

Combined transcriptomics–metabolomics profiling of the heat shock response in the hyperthermophilic archaeon Pyrococcus furiosus

  • Ana M. Esteves
  • Gonçalo Graça
  • Lindsay Peyriga
  • Inês M. Torcato
  • Nuno Borges
  • Jean-Charles Portais
  • Helena SantosEmail author
Original Paper

Abstract

Pyrococcus furiosus is a remarkable archaeon able to grow at temperatures around 100 °C. To gain insight into how this model hyperthermophile copes with heat stress, we compared transcriptomic and metabolomic data of cells subjected to a temperature shift from 90 °C to 97 °C. In this study, we used RNA-sequencing to characterize the global variation in gene expression levels, while nuclear magnetic resonance (NMR) and targeted ion exchange liquid chromatography–mass spectrometry (LC–MS) were used to determine changes in metabolite levels. Of the 552 differentially expressed genes in response to heat shock conditions, 257 were upregulated and 295 were downregulated. In particular, there was a significant downregulation of genes for synthesis and transport of amino acids. At the metabolite level, 37 compounds were quantified. The level of di-myo-inositol phosphate, a canonical heat stress solute among marine hyperthermophiles, increased considerably (5.4-fold) at elevated temperature. Also, the levels of mannosylglycerate, UDP-N-acetylglucosamine (UDPGlcNac) and UDP-N-acetylgalactosamine were enhanced. The increase in the pool of UDPGlcNac was concurrent with an increase in the transcript levels of the respective biosynthetic genes. This work provides the first metabolomic analysis of the heat shock response of a hyperthermophile.

Keywords

Heat shock Pyrococcus furiosus Metabolomics RNA-seq 

Notes

Acknowledgements

This work was supported by: Project LISBOA-01-0145-FEDER-007,660 (Microbiologia Molecular, Estrutural e Celular) funded by FEDER through COMPETE2020—Programa Operacional Competitividade e Internacionalização (POCI) and by national funds from FCT—Fundação para a Ciência e a Tecnologia and by project ONEIDA (LISBOA-01-0145-FEDER-016,417) co-funded by FEEI—“Fundos Europeus Estruturais e de Investimento” from “Programa Operacional Regional Lisboa 2020” and by national funds from FCT. The NMR equipment at CERMAX is part of the National NMR Network and is partially supported by Infrastructure Project no. 022,161 (co-financed by FEDER through COMPETE 2020, POCI and PORL and FCT through PIDDAC). Mass Spectrometry investigations were carried out at MetaToul (Metabolomics & Fluxomics Facitilies, Toulouse, France, www.metatoul.fr) which is part of MetaboHUB (The French National infrastructure for metabolomics and fluxomics, www.metabohub.fr, MetaboHUB-ANR-11-INBS-0010). MetaToul is supported by grants from the Région Occitanie, the FEDER (through FEDER-FSE 2014-2020), Toulouse Metropole, the Infrastructures en Biologie, Santé et Agronomie (IBiSa, France), the Centre National de la Recherche Scientifique (CNRS) and the Institut National de la Recherche Agronomique (INRA). We thank D. L. Turner for critical reading of the manuscript.

Supplementary material

792_2018_1065_MOESM1_ESM.pptx (473 kb)
Supplementary material 1 (PPTX 472 kb)
792_2018_1065_MOESM2_ESM.pdf (795 kb)
Supplementary material 2 (PDF 795 kb)

References

  1. Adams MW, Holden JF, Menon AL, Schut GJ, Grunden AM, Hou C, Hutchins MA, Jenney FE Jr, Kim C, Ma K, Pan G, Roy R, Sapra R, Story SV, Verhagen MF (2001) Key role for sulfur in peptide metabolism and in regulation of three hydrogenases in the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 183:716–724.  https://doi.org/10.1128/JB.183.2.716-724.2001 CrossRefGoogle Scholar
  2. Anders C, Niewoehner O, Duerst A, Jinek M (2014) Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513(7519):569–573.  https://doi.org/10.1038/nature13579 CrossRefGoogle Scholar
  3. Atkinson DE (1968) Energy charge of adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7:4030–4034.  https://doi.org/10.1021/bi00851a033 CrossRefGoogle Scholar
  4. Atomi H, Matsumi R, Imanaka T (2004) Reverse gyrase is not a prerequisite for hyperthermophilic life. J Bacteriol 186:4829–4833.  https://doi.org/10.1128/JB.186.14.4829-4833.2004 CrossRefGoogle Scholar
  5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57:289–300Google Scholar
  6. Bingol K, Brüschweiler R (2014) Multidimensional approaches to NMR-based metabolomics. Anal Chem 86:47–57.  https://doi.org/10.1021/ac403520j CrossRefGoogle Scholar
  7. Bolten CJ, Kiefer P, Letisse F, Portais JC, Wittmann C (2007) Sampling for metabolome analysis of microorganisms. Anal Chem 79:3843–3849.  https://doi.org/10.1021/ac0623888 CrossRefGoogle Scholar
  8. Boonyaratanakornkit BB, Simpson AJ, Whitehead TA, Fraser CM, El-Sayed NM, Clark DS (2005) Transcriptional profiling of the hyperthermophilic methanarchaeon Methanococcus jannaschii in response to lethal heat and non-lethal cold shock. Environ Microbiol 7:789–797.  https://doi.org/10.1111/j.1462-2920.2005.00751.x CrossRefGoogle Scholar
  9. Brito-Echeverría J, Lucio M, López-López A, Antón J, Schmitt-Kopplin P, Rosselló-Móra R (2011) Response to adverse conditions in two strains of the extremely halophilic species Salinibacter ruber. Extremophiles 15:379–389.  https://doi.org/10.1007/s00792-011-0366-3 CrossRefGoogle Scholar
  10. Chan KG, Priya K, Chang CY, Abdul Rahman AY, Tee KK, Yin WF (2016) Transcriptome analysis of Pseudomonas aeruginosa PAO1 grown at both body and elevated temperatures. PeerJ 4:e2223.  https://doi.org/10.7717/peerj.2223 CrossRefGoogle Scholar
  11. Esteves AM, Chandrayan SK, McTernan PM, Borges N, Adams MW, 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.  https://doi.org/10.1128/AEM.00559-14 CrossRefGoogle Scholar
  12. Faijes M, Mars AE, Smid EJ (2007) Comparison of quenching and extraction methodologies for metabolome analysis of Lactobacillus plantarum. Microb Cell Fact 6:27.  https://doi.org/10.1186/1475-2859-6-27 CrossRefGoogle Scholar
  13. Fiala G, Stetter KO (1986) Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100 degrees. C. Arch Microbiol 145:56–61.  https://doi.org/10.1007/BF00413027 CrossRefGoogle Scholar
  14. Fleury B, Kelley WL, Lew D, Götz F, Proctor RA, Vaudaux P (2009) Transcriptomic and metabolic responses of Staphylococcus aureus exposed to supra-physiological temperatures. BMC Microbiol 9:76.  https://doi.org/10.1186/1471-2180-9-76 CrossRefGoogle Scholar
  15. Fukui T, Atomi H, Kanai T, Matsumi R, Fujiwara S, Imanaka T (2005) Complete genome sequence of the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1 and comparison with Pyrococcus genomes. Genome Res 15:352–363.  https://doi.org/10.1101/gr.3003105 CrossRefGoogle Scholar
  16. Gao H, Wang Y, Liu X, Yan T, Wu L, Alm E, Arkin A, Thompson DK, Zhou J (2004) Global transcriptome analysis of the heat shock response of Shewanella oneidensis. J Bacteriol 186:7796–7803.  https://doi.org/10.1128/JB.186.22.7796-7803.2004 CrossRefGoogle Scholar
  17. García-Alcalde F, Okonechnikov K, Carbonell J, Cruz LM, Götz S, Tarazona S, Dopazo J, Meyer TF, Conesa A (2012) Qualimap: evaluating next-generation sequencing alignment data. Bioinformatics 28:2678–2679.  https://doi.org/10.1093/bioinformatics/bts503 CrossRefGoogle Scholar
  18. Hartmann E, König H (1990) Comparison of the biosynthesis of the methanobacterial pseudomurein and the eubacterial murein. Naturwissenschaften 77:472–475.  https://doi.org/10.1007/BF01135923 CrossRefGoogle Scholar
  19. Hasan CM, Shimizu K (2008) Effect of temperature up-shift on fermentation and metabolic characteristics in view of gene expressions in Escherichia coli. Microb Cell Fact 7:35.  https://doi.org/10.1186/1475-2859-7-35 CrossRefGoogle Scholar
  20. Helmann JD, Wu MF, Kobel PA, Gamo FJ, Wilson M, Morshedi MM, Navre M, Paddon C (2001) Global transcriptional response of Bacillus subtilis to heat shock. J Bacteriol 183:7318–7328.  https://doi.org/10.1128/JB.183.24.7318-7328.2001 CrossRefGoogle Scholar
  21. Jozefczuk S, Klie S, Catchpole G, Szymanski J, Cuadros-Inostroza A, Steinhauser D, Selbig J, Willmitzer L (2010) Metabolomic and transcriptomic stress response of Escherichia coli. Mol Syst Biol 6:364.  https://doi.org/10.1038/msb.2010.18 CrossRefGoogle Scholar
  22. Kalisiak J, Trauger SA, Kalisiak E, Morita H, Fokin VV, Adams MW, Sharpless KB, Siuzdak G (2008) Identification of a new endogenous metabolite and the characterization of its protein interactions through an immobilization approach. J Am Chem Soc 131:378–386.  https://doi.org/10.1021/ja808172n CrossRefGoogle Scholar
  23. Keese AM, Schut GJ, Ouhammouch M, Adams MW, Thomm M (2010) Genome-wide identification of targets for the archaeal heat shock regulator phr by cell-free transcription of genomic DNA. J Bacteriol 192:1292–1298.  https://doi.org/10.1128/JB.00924-09 CrossRefGoogle Scholar
  24. Kengen SW, de Bok FA, van Loo ND, Dijkema C, Stams AJ, de Vos WM (1994) Evidence for the operation of a novel Embden-Meyerhof pathway that involves ADP-dependent kinases during sugar fermentation by Pyrococcus furiosus. J Biol Chem 269:17537–17541Google Scholar
  25. Kiefer P, Nicolas C, Letisse F, Portais JC (2007) Determination of carbon labeling distribution of intracellular metabolites from single fragment ions by ion chromatography tandem mass spectrometry. Anal Biochem 360:182–188.  https://doi.org/10.1016/j.ab.2006.06.032 CrossRefGoogle Scholar
  26. Kim S, Lee do Y, Wohlgemuth G, Park HS, Fiehn O, Kim KH (2013) Evaluation and optimization of metabolome sample preparation methods for Saccharomyces cerevisiae. Anal Chem 85:2169–2176.  https://doi.org/10.1021/ac302881e CrossRefGoogle Scholar
  27. König K, Hartmann E, Kärcher U (1994) Pathways and principles of the biosynthesis of methanobacterial cell wall polymers. Syst Appl Microbiol 16:510–517.  https://doi.org/10.1016/S0723-2020(11)80320-6 CrossRefGoogle Scholar
  28. Koning SM, Konings WN, Driessen AJM (2002) Biochemical evidence for the presence of two α-glucoside ABC-transport systems in the hyperthermophilic archaeon Pyrococcus furiosus. Archaea 1:19–25CrossRefGoogle Scholar
  29. Lee HS, Shockley KR, Schut GJ, Conners SB, Montero CI, Johnson MR, Chou CJ, Bridger SL, Wigner N, Brehm SD, Jenney FE Jr, Comfort DA, Kelly RM, Adams MW (2006) Transcriptional and biochemical analysis of starch metabolism in the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 188:2115–2125.  https://doi.org/10.1128/JB.188.6.2115-2125.2006 CrossRefGoogle Scholar
  30. Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26:589–595.  https://doi.org/10.1093/bioinformatics/btp698 CrossRefGoogle Scholar
  31. Martins LO, Santos H (1995) Accumulation of mannosylglycerate and di-myo-inositol-phosphate by Pyrococcus furiosus in response to salinity and temperature. Appl Environ Microbiol 61:3299–3303Google Scholar
  32. Mashego MR, Rumbold K, De Mey M, Vandamme E, Soetaert W, Heijnen JJ (2007) Microbial metabolomics: past, present and future methodologies. Biotechnol Lett 29:1–16.  https://doi.org/10.1007/s10529-006-9218-0 CrossRefGoogle Scholar
  33. Meyer H, Liebeke M, Lalk M (2010) A protocol for the investigation of the intracellular Staphylococcus aureus metabolome. Anal Biochem 401:250–259.  https://doi.org/10.1016/j.ab.2010.03.003 CrossRefGoogle Scholar
  34. Meyer H, Weidmann H, Lalk M (2013) Methodological approaches to help unravel the intracellular metabolome of Bacillus subtilis. Microb Cell Fact 12:69.  https://doi.org/10.1186/1475-2859-12-69 CrossRefGoogle Scholar
  35. Millard P, Massou S, Wittmann C, Portais JC, Létisse F (2014) Sampling of intracellular metabolites for stationary and non-stationary 13C metabolic flux analysis in Escherichia coli. Anal Biochem 465:38–49.  https://doi.org/10.1016/j.ab.2014.07.026 CrossRefGoogle Scholar
  36. Mitsuzawa S, Deguchi S, Horikoshi K (2006) Cell structure degradation in Escherichia coli and Thermococcus sp. strain Tc-1-95 associated with thermal death resulting from brief heat treatment. FEMS Microbiol Lett 260:100–105.  https://doi.org/10.1111/j.1574-6968.2006.00301.x CrossRefGoogle Scholar
  37. Morii H, Kiyonari S, Ishino Y, Koga Y (2009) A novel biosynthetic pathway of archaetidyl-myo-inositol via archaetidyl-myo-inositol phosphate from CDP-archaeol and d-glucose 6-phosphate in methanoarchaeon Methanothermobacter thermautotrophicus cells. J Biol Chem 284:30766-20774.  https://doi.org/10.1074/jbc.M109.034652 CrossRefGoogle Scholar
  38. Morii H, Ogawa M, Fukuda K, Taniguchi H (2014) Ubiquitous distribution of phosphatidylinositol phosphate synthase and archaetidylinositol phosphate synthase in Bacteria and Archaea, which contain inositol phospholipid. Biochem Biophys Res Commun 443:86–90.  https://doi.org/10.1016/j.bbrc.2013.11.054 CrossRefGoogle Scholar
  39. Nicholson JK, Lindon JC (2008) Systems biology: metabonomics. Nature 455:1054–1056.  https://doi.org/10.1038/4551054a CrossRefGoogle Scholar
  40. Noll KM, Lapierre P, Gogarten JP, Nanavati DM (2008) Evolution of mal ABC transporter operons in the Thermococcales and Thermotogales. BMC Evol Biol 8:7.  https://doi.org/10.1186/1471-2148-8-7 CrossRefGoogle Scholar
  41. Nonaka G, Blankschien M, Herman C, Gross CA, Rhodius VA (2006) Regulon and promoter analysis of the E. coli heat-shock factor, 32, reveals a multifaceted cellular response to heat stress. Genes Dev 20:1776–1789.  https://doi.org/10.1101/gad.1428206 CrossRefGoogle Scholar
  42. Palmer AG, Cavanagh J, Wright PE, Rance M (1991) Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy. J Magn Reson 93:151–170.  https://doi.org/10.1016/0022-2364(91)90036-S Google Scholar
  43. Patti GJ, Yanes O, Siuzdak G (2012) Metabolomics: the apogee of the omics trilogy. Nat Rev Mol Cell Biol 13:263–269.  https://doi.org/10.1038/nrm3314 CrossRefGoogle Scholar
  44. Pinu FR, Villas-Boas SG, Aggio R (2017) Analysis of intracellular metabolites from microorganisms: quenching and extraction protocols. Metabolites.  https://doi.org/10.3390/metabo7040053 Google Scholar
  45. Pysz MA, Ward DE, Shockley KR, Montero CI, Conners SB, Johnson MR, Kelly RM (2004) Transcriptional analysis of dynamic heat-shock response by the hyperthermophilic bacterium Thermotoga maritima. Extremophiles 8:209–217.  https://doi.org/10.1007/s00792-004-0379-2 CrossRefGoogle Scholar
  46. Ramakrishnan V, Verhagen MFJM, Adams MW (1997) Characterization of di-myo-inositol-1,1′-phosphate in the hyperthermophilic bacterium Thermotoga maritima. Appl Environ Microbiol 63:347–350Google Scholar
  47. Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40:253–266.  https://doi.org/10.1016/j.molcel.2010.10.006 CrossRefGoogle Scholar
  48. Robb FT, Maeder DL, Brown JR, DiRuggiero J, Stump MD, Yeh RK, Weiss RB, Dunn DM (2001) Genomic sequence of hyperthermophile, Pyrococcus furiosus: implications for physiology and enzymology. Methods Enzymol 330:134–157.  https://doi.org/10.1016/S0076-6879(01)30372-5 CrossRefGoogle Scholar
  49. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140.  https://doi.org/10.1093/bioinformatics/btp616 CrossRefGoogle Scholar
  50. Rodionov DA, Kurnasov OV, Stec B, Wang Y, Roberts MF, Osterman AL (2007) Genomic identification and in vitro reconstitution of a complete biosynthetic pathway for the osmolyte di-myo-inositol-phosphate. Proc Natl Acad Sci USA 104:4279–4284.  https://doi.org/10.1073/pnas.0609279104 CrossRefGoogle Scholar
  51. Rodrigues MV, Borges N, Henriques M, Lamosa P, Ventura R, Fernandes C, Empadinhas N, Maycock C, da Costa MS, Santos H (2007) Bifunctional CTP: inositol-1-phosphate cytidylyltransferase/CDP-inositol:inositol-1-phosphate transferase, the key enzyme for di-myo-inositol-phosphate synthesis in several (hyper)thermophiles. J Bacteriol 189:5405–5412.  https://doi.org/10.1128/JB.00465-07 CrossRefGoogle Scholar
  52. Rohlin L, Trent JD, Salmon K, Kim U, Gunsalus RP, Liao JC (2005) Heat shock response of Archaeoglobus fulgidus. J Bacteriol 187:6046–6057.  https://doi.org/10.1128/JB.187.17.6046-6057.2005 CrossRefGoogle Scholar
  53. Santos H, Lamosa P, Borges N, Gonçalves LG, Pais T, Rodrigues MV (2011) Organic compatible solutes of prokaryotes that thrive in hot environments: The importance of ionic compounds for thermostabilization. In: Horikoshi K, Antranikian G, Bull AT, Robb FT, Stetter KO (eds) Extremophiles handbook. Springer, Tokyo, pp 497–520CrossRefGoogle Scholar
  54. Scott JW, Poole FL, Adams MW (2014) Characterization of ten heterotetrameric NDP-dependent acyl-CoA synthetases of the hyperthermophilic archaeon Pyrococcus furiosus. Archaea.  https://doi.org/10.1155/2014/176863 Google Scholar
  55. Sévin DC, Sauer W (2014) Ubiquinone accumulation improves osmotic-stress tolerance in Escherichia coli. Nat Chem Biol 10:266–272.  https://doi.org/10.1038/nchembio.1437 CrossRefGoogle Scholar
  56. Shaka AJ, Lee CJ, Pines A (1988) Iterative schemes for bilinear operators; application to spin decoupling. J Magn Reson 77:274–293.  https://doi.org/10.1016/0022-2364(88)90178-3 Google Scholar
  57. Shockley KR, Ward DE, Chhabra SR, Conners SB, Montero CI, Kelly RM (2003) Heat shock response by the hyperthermophilic archaeon Pyrococcus furiosus. Appl Environ Microbiol 69:2365–2371.  https://doi.org/10.1128/AEM.69.4.2365-2371.2003 CrossRefGoogle Scholar
  58. Soini J, Falschlehner C, Mayer C, Böhm D, Weinel S, Panula J, Vasala A, Neubauer P (2005) Transient increase of ATP as a response to temperature up-shift in Escherichia coli. Microb Cell Fact 4:9.  https://doi.org/10.1186/1475-2859-4-9 CrossRefGoogle Scholar
  59. Tang J (2011) Microbial metabolomics. Curr Genom 12:391–403.  https://doi.org/10.2174/138920211797248619 CrossRefGoogle Scholar
  60. Taymaz-Nikerel H, de Mey M, Ras C, ten Pierick A, Seifar RM, van Dam JC, Heijnen JJ, van Gulik WM (2009) Development and application of a differential method for reliable metabolome analysis in Escherichia coli. Anal Biochem 386:9–19.  https://doi.org/10.1016/j.ab.2008 CrossRefGoogle Scholar
  61. Theobald U, Mailinger W, Baltes M, Rizzi M, Reuss M (1997) In vivo analysis of metabolic dynamics in Saccharomyces cerevisiae: I. Experimental observations. Biotechnol Bioeng 55:305–316.  https://doi.org/10.1002/(SICI)1097-0290(19970720)55:2%3c305:AID-BIT8%3e3.0.CO;2-M CrossRefGoogle Scholar
  62. van Gulik WM (2010) Fast sampling for quantitative microbial metabolomics. Curr Opin Biotechnol 21:27–34.  https://doi.org/10.1016/j.copbio.2010.01.008 CrossRefGoogle Scholar
  63. Villas-Bôas SG, Højer-Pedersen J, Akesson M, Smedsgaard J, Nielsen J (2005) Global metabolite analysis of yeast: evaluation of sample preparation methods. Yeast 22:1155–1169.  https://doi.org/10.1002/yea.1308 CrossRefGoogle Scholar
  64. Winder CL, Dunn WB, Schuler S, Broadhurst D, Jarvis R, Stephens GM, Goodacre R (2008) Global metabolic profiling of Escherichia coli cultures: an evaluation of methods for quenching and extraction of intracellular metabolites. Anal Chem 80:2939–2948.  https://doi.org/10.1021/ac7023409 CrossRefGoogle Scholar
  65. Wishart DS, Lewis MJ, Morrissey JA, Flegel MD, Jeroncic K, Xiong Y, Cheng D, Eisner R, Gautam B, Tzur D, Sawhney S, Bamforth F, Greiner R, Li L (2008) The human cerebrospinal fluid metabolome. J Chromatogr B Analyt Technol Biomed Life Sci 871:164–173.  https://doi.org/10.1016/j.jchromb.2008.05.001 CrossRefGoogle Scholar
  66. Wittmann C, Krömer JO, Kiefer P, Binz T, Heinzle E (2004) Impact of the cold shock phenomenon on quantification of intracellular metabolites in bacteria. Anal Biochem 327:135–139.  https://doi.org/10.1016/j.ab.2004.01.002 CrossRefGoogle Scholar
  67. Wu L, Mashego MR, van Dam JC, Proll AM, Winke JL (2005) Quantitative analysis of the microbial metabolome by isotope dilution mass spectrometry using uniformly 13C-labeled cell extracts as internal standards. Anal Biochem 336:164–171.  https://doi.org/10.1016/j.ab.2004.09.001 CrossRefGoogle Scholar
  68. Ye Y, Zhang L, Hao F, Zhang J, Wang Y, Tang H (2012) Global metabolomics responses of Escherichia coli to heat stress. J Proteome Res 11:2559–2566.  https://doi.org/10.1021/pr3000128 CrossRefGoogle Scholar
  69. Zaparty M, Esser D, Gertig S, Haferkamp P, Kouril T, Manica A, Pham TK, Reimann J, Schreiber K, Sierocinski P, Teichmann D, van Wolferen M, von Jan M, Wieloch P, Albers SV, Driessen AJ, Klenk HP, Schleper C, Schomburg D, van der Oost J, Wright PC, Siebers B (2010) “Hot standards” for the thermoacidophilic archaeon Sulfolobus solfataricus. Extremophiles 14:119–142.  https://doi.org/10.1007/s00792-009-0280-0 CrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Ana M. Esteves
    • 1
  • Gonçalo Graça
    • 1
  • Lindsay Peyriga
    • 2
    • 3
  • Inês M. Torcato
    • 1
  • Nuno Borges
    • 1
  • Jean-Charles Portais
    • 2
    • 3
    • 4
  • Helena Santos
    • 1
    Email author
  1. 1.Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de LisboaOeirasPortugal
  2. 2.LISBP, Université de Toulouse, CNRS, INRA, INSAToulouseFrance
  3. 3.MetaToul-MetaboHUB, National Infrastructure of Metabolomics and FluxomicsToulouseFrance
  4. 4.Université Paul Sabatier, Université de ToulouseToulouseFrance

Personalised recommendations