Archaea; cell walls; S-layer; (glyco-)proteins; protein structure
Abstract :
[en] The archaea are recognized as a separate third domain of life together with the bacteria and eucarya. The
archaea include the methanogens, extreme halophiles, thermoplasmas, sulfate reducers and sulfur metabolizing
thermophiles, which thrive in different habitats such as anaerobic niches, salt lakes, and marine
hydrothermals systems and continental solfataras. Many of these habitats represent extreme environments
in respect to temperature, osmotic pressure and pH-values and remind on the conditions of the
early earth. The cell envelope structures were one of the first biochemical characteristics of archaea studied
in detail. The most common archaeal cell envelope is composed of a single crystalline protein or glycoprotein
surface layer (S-layer), which is associated with the outside of the cytoplasmic membrane. The
S-layers are directly exposed to the extreme environment and can not be stabilized by cellular components.
Therefore, from comparative studies of mesophilic and extremely thermophilic S-layer proteins
hints can be obtained about the molecular mechanisms of protein stabilization at high temperatures.
First crystallization experiments of surface layer proteins under microgravity conditions were successful.
Here, we report on the biochemical features of selected mesophilic and extremely archaeal S-layer (glyco-)
proteins.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Claus, Harald; Johannes Gutenberg-Universität - Mainz
Akça, Erol; Johannes Gutenberg-Universität - Mainz
Debaerdemaeker, Tony; Universität Ulm
Evrard, Christine ; Université Catholique de Louvain - UCL > Département de Chimie > Laboratoire de Chimie et de Cristallographie
Declercq, Jean-Paul; Université Catholique de Louvain - UCL > Département de Chimie > Laboratoire de Chimie et de Cristallographie
König, Helmut; Johannes Gutenberg-Universität - Mainz
Language :
English
Title :
Primary Structure of Selected Archaeal Mesophilic and Extremely Thermophilic Outer Surface Layer Proteins
Akça E., Claus H., Schultz N., Karbach G., Schlott B., Debaerdemaeker T., Declercq J.-P., König H. (2002) Genes and derived amino acid sequences of S-layer proteins isolated from mesophilic, thermophilic and extremely thermophilic methanococci. Extremophiles, In press; .
Baumeister W., Volker S., Santarius U. (1991) The three-dimensional structure of the surface protein of Acidianus brierleyi determined by electron crystallography. System. Appl. Microbiol. 14:103-110.
Baumeister W., Lembcke G. (1992) Structural features of archaebacterial cell envelopes. J. Bioenerg. Biomembr. 24:567-575.
Bayley D.P., Koval S.F. (1994) Membrane association and isolation of the S-layer protein of Methanoculleus marisnigri. Can. J. Microbiol. 40:237-241.
Beveridge T.J., Graham L.L. (1991) Surface layers of bacteria. Microbiol. Rev. 55:684-705.
Beveridge T.J., Koval S.F. Advances in Paracrystalline Bacterial Surface Layers, New York, Plenum Press; 1993.
Beveridge T.J. (1997) Functions of S-layers. FEMS Microbiol. Rev. 20:99-149.
Boot H.J., Pouwels P.H. (1996) Expression, secretion and antigenic variation of bacterial S-layer proteins. Mol. Microbiol. 21:1117-1123.
Bröckl G., Behr M., Fabry M., Hensel R., Kaudewitz H., Biendl E., König H. (1991) Analysis and nucleotide sequence of the genes encoding the surface-layer glycoproteins of the hyperthermophilic methanogens Methanothermus fervidus and Methanothermus sociabilis. Eur. J. Biochem. 199:147-152.
Bult C.J. (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273:1058-1072.
Cambillau C., Claverie J.M. (2000) Structural and genomic correlates of hyperthermostabilty. J. Biol. Chem. 275:32383-32386.
Chakravarty S., Varadarajan R. (2000) Elucidation of determinants of protein stability through genome sequence analysis. FEBS Lett. 470:65-69.
Dalgaard J.Z., Garrett R.A. (1993) Archaeal hyperthermophile genes. The Biochemistry of Archaea (Archaebacteria) , (M. Kates, D. J. Kushner, T. A. Matheson, eds). Amsterdam, Elsevier; 535-563.
Das R., Gerstein M. (2000) The stability of thermophilic proteins: A study based on comprehensive genome comparison. Funct. Integr. Genomics 1:76-88.
Deatherage J.F., Taylor K.A., Amos L.A. (1983) Three-dimensional arrangement of the cell wall protein of Sulfolobus acidocaldarius. J. Mol. Biol. 167:823-848.
Egelseer E.M., Danhorn D., Pleschberger M., Hotzy C., Sleytr U.B., Sara M. (2001) Characterization of an S-layer glycoprotein produced in the course of S-layer variation of Bacillus stearothermophilus ATCC 12980 and sequencing and cloning the sbsD gene encoding the protein moiety. Arch. Microbiol. 177:70-80.
Engelhardt H., Peters J. (1998) Structural research on surface layers: A focus on stability, surface layer domains, and surface layer-cell wall interactions. J. Struct. Biol. 124:276-302.
Evrard Ch., Declercq J.-P., Debaerdemaeker T., König H. (1999) The first successful crystallization of a prokaryotic extremely thermophilic outer surface layer glycoprotein. Z. Kristallogr. 214:427-429.
Fiala G., Stetter K. (1986) Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C. Arch. Microbiol. 145:56-61.
Haney P.J., Badger J.H., Buldak G.L., Reich C.I., Woese C.R., Olsen G.J. (1999) Thermal adaption analyzed by comparison of protein sequences from mesophilic and extremely thermophilic Methanococcus species. Proc. Natl. Acad. Sci. USA 96:3578-3583.
Kandler O., König H. (1978) Chemical composition of the peptidoglycan-free cell walls of methanogenic bacteria. Arch. Microbiol. 118:141-152.
Kandler O., König H. (1985) Cell envelopes of archaebacteria. The Bacteria. A Treatise on Structure and Function. Archaebacteria , (C. R. Woese, R. S. Wolfe, eds.), New York, Academic Press; 8:413-457.
Kandler O., König H. (1993) Cell envelopes of archaea: Structure and chemistry. The Biochemistry of Archaea (Archaebacteria) , (M. Kates, D. J. Kushner, A. T. Matheson, eds.). Amsterdam, Elsevier Science Publishers; 223-259.
Kansy W.J., Carinato M.E., Monteggia L.M., Konisky J. (1994) In vivo transcripts of the S-layer encoding structural gene of the archaeon Methanococcus voltae. Gene 148:131-135.
Karlson P., Doenecke D., Koolman J. Kurzes Lehrbuch der Biochemie für Mediziner und Naturwissenschaftler, Stuttgart, G. Thieme Verlag; 1994.
Kärcher U., Schröder H., Haslinger E., Allmaier G., Schreiner R., Wieland F., Haselbeck A., König H. (1993) Primary structure of the heterosaccharide of the surface glycoprotein of Methanothermus fervidus. J. Biol. Chem. 268:26821-26826.
Keswani J., Orkand S., Premachandran U., Mandelco L., Franklin M.J., Whitman W.B. (1996) Phylogeny and taxonomy of mesophilic Methanococcus spp. and comparison of rRNA, DNA hybridization, and phenotypic methods. Int. J. System. Bact. 46:727-735.
König H. (1986) Chemical composition of cell envelopes of methanogenic bacteria isolated from human and animal feces. System. Appl. Microbiol. 8:159-162.
König H., Stetter K.O. (1982) Isolation and characterization of Methanolobus tindarius, sp. nov., a coccoid methanogen growing only on methanol and methylamines. Zbl. Bakt. Hyg., I. Abt. Orig. C 3:478-490.
König H., Messner P. (1997) International Workshop on Structure, Biochemistry, Molecular Biology and Applications of Microbial S-Layers. Special Issue. FEMS Microbiol. Rev. 20 1-2.
König H., Kralik R., Kandler O. (1982) Structure and modifications of pseudomurein in Methanobacteriales. Zbl. Bakt. Hyg., I. Abt. Orig. C 3:179-191.
Kreisl P., Kandler O. (1986) Chemical structure of the cell wall polymer of Methanosarcina. Syst. Appl. Microbiol. 7:293-299.
Kurr M., Huber R., König H., Jannasch H.W., Fricke H., Trincone A., Kristjannson J.K., Stetter K.O. (1991) Methanopyrus kandleri, gen. and sp. nov. represents a novel group of hyperthermophilic methanogens, growing at 110°C. Arch. Microbiol. 156:239-247.
Lechner J., Sumper M. (1987) The primary structure of a procaryotic glycoprotein. Cloning and sequencing of the cell surface glycoprotein gene of halobacteria. J. Biol. Chem. 262:9724-9729.
Li W.T., Shriver J.W., Reeve J.N. (2000) Mutational analysis of differences in thermostability between histones from mesophilic and hyperthermophilic archaea. J. Bacteriol. 182:812-817.
Mayerhofer L.E., Conway De Macario E., Yao R., Macario A.J. (1998) Structure, organization, and expression of genes coding for envelope components in the archaeon Methanosarcina mazei S-6. Arch. Microbiol. 169:339-345.
McDonald J.H., Grasso A.M., Reito L.K. (1999) Patterns of temperature adaptation in proteins from Methanococcus and Bacillus. Mol. Biol. Evol. 16:1785-1790.
Messner P., Pum D., Sara M., Stetter K.O., Sleytr U.B. (1986) Ultrastructure of the cell envelope of the archaebacteria Thermoproteus tenax and Thermoproteus neutrophilus. J. Bacteriol. 166:1046-1054.
Niemetz R., Kärcher U., Kandler O., Tindall B.J., König H. (1997) The cell wall polymer of the extremely halophilic archaeon Natronococcus occultus. Eur. J. Biochem. 249:905-911.
Nielsen H., Engelbrecht J., Brunak S., Von Heijne G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
Patel G.B., Sprott G.D. (1990) Methanosaeta concilii gen. nov., sp. nov., ("Methanothrix concilii") and Methanosaeta thermoacetophila nom. rev., comb. nov. Int. J. Syst. Bacteriol. 40:79-82.
Peters J., Nitscii M., Kuehlmorgen B., Golbik R., Lupas A., Kellermann J., Engelhardt H., Pfander J.P., Mueller S., Goldie K., Engel A., Stetter K.O., Baumeister W. (1995) Tetrabrachion: A filamentous archaebacterial surface protein assembly of unusual structure end extreme stability. J. Mol. Biol. 245:385-401.
Phipps B.M., Huber R., Baumeister W. (1991) The cell envelope of the hyperthermophilic archaebacterium Pyrobaculum organotrophum consists of two regularly arrayed protein layers: Three-dimensional structure of the outer layer. Mol. Microbiol. 5:253-265.
Sára M., Sleytr U.B. (1987) Charge distribution on the S-layer of Bacillus stearothermophilus NRS 1536/3c and importance of charged groups for morphogenesis and function. J. Bacteriol. 169:2804-2809.
Sára M., Sleytr U.B. (2000) S-layer proteins. J. Bacteriol. 182:859-868.
Schäffer C., Messner P. (2001) Glycobiology of surface layer proteins. Biochimie 83:591-599.
Schleifer K.H., Steber J., Mayer H. (1982) Chemical composition and structure of the cell wall of Halococcus morrhuae. Zbl. Bakt., Hyg., I. Abt. Orig. C3:171-178.
Sleytr U.B. (1997) Basic and applied S-layer research: An overview. FEMS Microbiol. Rev. 20:5-12.
Sleytr U.B., Beveridge T.J. (1999) Bacterial S-layers. Trends in Microbiol. 7:253-260.
Southam G., Firtel M., Blackford B.L., Jericho M.H., Xu W., Mulhern P.J., Beveridge T.J. (1993) Transmission electron microscopy, scanning tunneling microscopy, and atomic force microscopy of the cell envelope layers of the archaeobacterium Methanospirillum hungatei GP1. J. Bacteriol. 175:1946-1955.
Stetter K.O. (1992) The genus Archaeoglobus. The Prokaryotes. A Handbook of Bacteria: Ecophysiology, Isolation, Identification, Applications, 2nd Ed. , (A. Balows, H. G. Trüper, M. dworkin, W. Harder, K.-H. Schleifer, eds.). Berlin, Springer, Verlag; 1:707-711.
Stetter K.O., Thomm M., Winter J., Wildgruber G., Huber H., Zillig W., Janecovic D., König H., Palm P., Wunderl S. (1981) Methanothermus fervidus, sp. nov., a novel extremely thermophilic methanogen isolated from an Icelandic hot spring. Zbl. Bakt. Hyg., I. Abt. Orig. C 2:166-178.
Stetter K.O., König H., Stackebrandt E. (1983) Pyrodictium gen. nov., a new genus of submarine disc-shaped sulphur reducing archaebacteria growing optimally at 105°C. System. Appl. Microbiol. 4:535-551.
Stetter K.O., Thomm M., Winter J., Wildgruber G., Huber H., Zillig W., Janecovic D., König H., Palm P., Wunderl S. (1981) Methanothermus fervidus, sp. nov., a novel extremely thermophilic methanogen isolated from an Icelandic hot spring. Zbl. Bakt. Hyg., I. Abt. Orig. C 2:166-178.
Sumper M. (1993) S-layer glycoproteins from moderately and extremely halophilic archeobacteria. Advances in Bacterial Paracrystalline Surface Layers , (T.J. Beveridge, S.E Koval, eds.), (NATO ASI Series A: Life Sciences). New York, Plenum Press; 252:109-117.
Sumper M., Wieland F.T. (1995) Bacterial glycoproteins. Glycoproteins , (J. Montreuil, J. F. G. Vliegenthart, H. Schachter, eds.). Amsterdam, Elsevier; 455-473.
Sumper M., Berg E., Mengele R., Strobel L. (1990) Primary structure and glycosylation of the S-layer protein of Haloferax volcanii. J. Bacteriol. 172:7111-7118.
Tabassum R.K., Sandman K.M., Reeve J.N. (1992) HMt, a histone-related protein from Methanobacterium thermoautotrophicum. J. Bacteriol. 174:7890-7895.
Thomm M. (1996) Archaeal transcription factors and their role in transcription inititation. FEMS Microbiol. Rev. 18:159-171.
Wakai H., Nakamura S., Kawasaki H., Takada K., Mizutani S., Aono R., Horikoshi K. (1997) Cloning and sequencing of the gene encoding the cell surface glycoprotein of Haloarcula japonica strain TR-1. Extremophiles 1:29-35.
Wildgruber G., Thomm M., König H., Ober K., Ricchiuto T., Stetter K.O. (1982) Methanoplanus limicola, a platesphaped methanogen representing a novel family, the Methanoplanaceae. Arch. Microbiol. 132:31-36.
Wildhaber I., Santarius U., Baumeister W. (1987) Three-dimensional structure of the surface protein of Desulfurococcus mobilis. J. Bacteriol. 169:5563-5568.
Yang L.L., Haug A. (1979) Purification and partial characterization of a procaryotic glycoprotein from the plasma membran of Thermoplasma acidophilum. Biochim. Biophys. Acta 556:277-365.
Zellner G., Alten C., Stackebrandt E., Conway De Macario E., Winter J. (1987) Isolation and characterization of Methanocorpusculum parvum, gen. nov. spec. nov., a new tungsten requiring, coccoid methanogen. Arch. Microbiol. 147:13-20.
Zellner G., Messner P., Kneifel H., Tindall B.J., Winter J., Stackebrandt E. (1989) Methanolacinia gen. nov., incorporating Methanomicrobium paynteri as Methanolacinia paynteri comb. nov. J. Gen. Appl. Microbiol. 35:185-202.
Zillig W., Holz I., Janekovic D., Klenk H.P., Imsel E., Trent J., Wunderl S., Forjaz V.H., Coutinho R., Ferreira T. (1990) Hyperthermus butylicus, a hyperthermophilic sulfur-reducing archaebacterium that ferments peptides. J. Bacteriol. 172:3959-3965.
