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Breaking the mould: archaea with all four chaperoning systems
BBRC Biochemical and Biophysical Research Communications 301 (2003) 811–812 www.elsevier.com/locate/ybbrc
Breakthroughs and Views
Breaking the mould: archaea with all four chaperoning systems Everly Conway de Macario,a,* Dennis L. Maeder,b and Alberto J.L. Macarioa a
Wadsworth Center, NYSDOH, and Department of Biomedical Sciences, SUNY Albany, Empire State Plaza, P.O. Box 509, Albany, NY 1220, USA b Center of Marine Biotechnology, University of Maryland Biotechnology Institute, 701 E. Pratt St., Baltimore, MD 21202, USA Received 24 December 2002
The chaperonins GroEL/GroES believed to occur only in bacteria and in the eukaryotic-cell organelles of bacterial ancestry [1] were found for the first time in an archaeon along with the other three main chaperoning systems. GroEL and GroES were named bacterial or group I chaperonins to distinguish them from group II chaperonins typical of the eukaryotic- and archaeal-cell cytosols [2]. The genome of the archaeon Methanosarcina acetivorans was sequenced (http://www-genome.wi.mit.edu/ annotation/microbes/methanosarcina/) and we found the GroEL/GroES organized in a locus similar to that of bacteria. In addition, genes encoding prefoldin subunits, the components of the molecular chaperone machine [Hsp70(DnaK), Hsp40(DnaJ), and GrpE], and thermosome subunits or chaperonins group II were also found in M. acetivorans (Fig. 1A). Information available in the databases indicate that these systems are also present in other Methanosarcina species but in no other archaea. M. acetivorans is, therefore, representative of a unique group of prokaryotes containing all four main chaperoning systems. A critical question is raised by these findings: did M. acetivorans receive the groEL/S genes by inheritance or by lateral transfer from a bacterium as suggested for Methanosarcina mazeii (http:// www.g2l.bio.uni-goettingen.de/mm/index.html). Lateral transfer would appear likely if one considers that the hsp70(dnaK) gene in some archaeal species seems to be of a bacterial origin [1]. However, comparative analy* Corresponding author. Fax: 1-518-474-1213. E-mail address: [email protected] (E. Conway de Macario).
ses of the M. acetivorans GroEL/S with those in databases and phylogenetic-tree constructions produced evidence against a bacterial origin, Fig. 1B. The tree illustrates the distinct divisions for the well conserved small subunit rRNA for the three domains of life (Fig. 1C). Remarkably in the case of GroEL of genus Methanosarcina, unique amongst the archaea, the point of junction with the otherwise resolved eukaryotes and eubacteria is more deeply rooted than the major radiations within these domains. This leaves open the contingency of a direct line of inheritance from a deep root. Furthermore, there is no candidate branch that offers the possibility of recent lateral transfer as a mechanism of introduction of groEL into the archaea. The long branch of Methanosarcina is consistent with a long period of adaptation in the absence of evolutionary pressure, but the close similarity between Methanosarcina species indicates that evolutionary constraints now apply strongly. These findings give new perspectives into the origin and evolution of chaperones, and into the role that Methanosarcina species and their direct ancestors might have played in the dispersion of the genes encoding chaperones, i.e., molecules that must have played a crucial role in survival since the dawn of life. A fundamental question now is whether or not M. acetivorans is the progenitor of the four chaperoning systems. Our data indicate that M. acetivorans occupies a unique place in the evolution of protein folding and refolding mechanisms, and suggest that experimental analysis of this organism will provide essential clues for understanding the origins of chaperoning pathways and networks.
0006-291X/03/$ - see front matter Ó 2003 Elsevier Science (USA). All rights reserved. doi:10.1016/S0006-291X(03)00047-0
812
E. Conway de Macario et al. / Biochemical and Biophysical Research Communications 301 (2003) 811–812
Fig. 1. Relative location of the genes encoding the four chaperoning systems in the M. acetivorans genome (A). GroEL (B) and Small Subunit (SSU) rRNA (C) neighbor-joining trees. Sequences were extracted from NCBI databases, and aligned using CLUSTAL W, running under CLUSTAL_X (v1.8) [3,4]. Trees were bootstrapped with 1000 trials on refined datasets, and files were displayed and edited using Tree Explorer [5].
References [1] A.J.L. Macario, M. Lange, B.K. Ahring, E. Conway de Macario, Stress genes and proteins in the Archaea, Microbiol. Mol. Biol. Rev. 63 (1999) 923–967. [2] N.A. Ranson, H.E. White, H.R. Saibil, Chaperonins, J. Biochem. 333 (1998) 233–242. [3] J.D. Thomson, D.G. Higgins, T.J. Gibson, CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment
through sequence weighting position-specific gap penalties and weight matrix choice, Nucleic Acids Res. 22 (1994) 4673–4680. [4] J.D. Thomson, T.J. Gibson, F. Plewniak, F. Jeanmougin, D.G. Higgins, The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools, Nucleic Acids Res. 25 (1997) 4876–4882. [5] S. Kumar, K. Tamura, I.B. Jacobsen, N. Masatoshi, MEGA2: Molecular Evolutionary Genetics Analysis Software, Arizona State University, Tempe, Arizona, 2001.
Breakthroughs and Views
Breaking the mould: archaea with all four chaperoning systems Everly Conway de Macario,a,* Dennis L. Maeder,b and Alberto J.L. Macarioa a
Wadsworth Center, NYSDOH, and Department of Biomedical Sciences, SUNY Albany, Empire State Plaza, P.O. Box 509, Albany, NY 1220, USA b Center of Marine Biotechnology, University of Maryland Biotechnology Institute, 701 E. Pratt St., Baltimore, MD 21202, USA Received 24 December 2002
The chaperonins GroEL/GroES believed to occur only in bacteria and in the eukaryotic-cell organelles of bacterial ancestry [1] were found for the first time in an archaeon along with the other three main chaperoning systems. GroEL and GroES were named bacterial or group I chaperonins to distinguish them from group II chaperonins typical of the eukaryotic- and archaeal-cell cytosols [2]. The genome of the archaeon Methanosarcina acetivorans was sequenced (http://www-genome.wi.mit.edu/ annotation/microbes/methanosarcina/) and we found the GroEL/GroES organized in a locus similar to that of bacteria. In addition, genes encoding prefoldin subunits, the components of the molecular chaperone machine [Hsp70(DnaK), Hsp40(DnaJ), and GrpE], and thermosome subunits or chaperonins group II were also found in M. acetivorans (Fig. 1A). Information available in the databases indicate that these systems are also present in other Methanosarcina species but in no other archaea. M. acetivorans is, therefore, representative of a unique group of prokaryotes containing all four main chaperoning systems. A critical question is raised by these findings: did M. acetivorans receive the groEL/S genes by inheritance or by lateral transfer from a bacterium as suggested for Methanosarcina mazeii (http:// www.g2l.bio.uni-goettingen.de/mm/index.html). Lateral transfer would appear likely if one considers that the hsp70(dnaK) gene in some archaeal species seems to be of a bacterial origin [1]. However, comparative analy* Corresponding author. Fax: 1-518-474-1213. E-mail address: [email protected] (E. Conway de Macario).
ses of the M. acetivorans GroEL/S with those in databases and phylogenetic-tree constructions produced evidence against a bacterial origin, Fig. 1B. The tree illustrates the distinct divisions for the well conserved small subunit rRNA for the three domains of life (Fig. 1C). Remarkably in the case of GroEL of genus Methanosarcina, unique amongst the archaea, the point of junction with the otherwise resolved eukaryotes and eubacteria is more deeply rooted than the major radiations within these domains. This leaves open the contingency of a direct line of inheritance from a deep root. Furthermore, there is no candidate branch that offers the possibility of recent lateral transfer as a mechanism of introduction of groEL into the archaea. The long branch of Methanosarcina is consistent with a long period of adaptation in the absence of evolutionary pressure, but the close similarity between Methanosarcina species indicates that evolutionary constraints now apply strongly. These findings give new perspectives into the origin and evolution of chaperones, and into the role that Methanosarcina species and their direct ancestors might have played in the dispersion of the genes encoding chaperones, i.e., molecules that must have played a crucial role in survival since the dawn of life. A fundamental question now is whether or not M. acetivorans is the progenitor of the four chaperoning systems. Our data indicate that M. acetivorans occupies a unique place in the evolution of protein folding and refolding mechanisms, and suggest that experimental analysis of this organism will provide essential clues for understanding the origins of chaperoning pathways and networks.
0006-291X/03/$ - see front matter Ó 2003 Elsevier Science (USA). All rights reserved. doi:10.1016/S0006-291X(03)00047-0
812
E. Conway de Macario et al. / Biochemical and Biophysical Research Communications 301 (2003) 811–812
Fig. 1. Relative location of the genes encoding the four chaperoning systems in the M. acetivorans genome (A). GroEL (B) and Small Subunit (SSU) rRNA (C) neighbor-joining trees. Sequences were extracted from NCBI databases, and aligned using CLUSTAL W, running under CLUSTAL_X (v1.8) [3,4]. Trees were bootstrapped with 1000 trials on refined datasets, and files were displayed and edited using Tree Explorer [5].
References [1] A.J.L. Macario, M. Lange, B.K. Ahring, E. Conway de Macario, Stress genes and proteins in the Archaea, Microbiol. Mol. Biol. Rev. 63 (1999) 923–967. [2] N.A. Ranson, H.E. White, H.R. Saibil, Chaperonins, J. Biochem. 333 (1998) 233–242. [3] J.D. Thomson, D.G. Higgins, T.J. Gibson, CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment
through sequence weighting position-specific gap penalties and weight matrix choice, Nucleic Acids Res. 22 (1994) 4673–4680. [4] J.D. Thomson, T.J. Gibson, F. Plewniak, F. Jeanmougin, D.G. Higgins, The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools, Nucleic Acids Res. 25 (1997) 4876–4882. [5] S. Kumar, K. Tamura, I.B. Jacobsen, N. Masatoshi, MEGA2: Molecular Evolutionary Genetics Analysis Software, Arizona State University, Tempe, Arizona, 2001.