Prokaryotic structural maintenance of chromosomes (SMC) proteins: distribution, phylogeny, and comparison with MukBs and additional prokaryotic and eukaryotic coiled-coil proteins.

Structural maintenance of chromosomes (SMC) proteins are known to be essential for chromosome segregation in some prokaryotes and in eukaryotes. A systematic search for the distribution of SMC proteins in prokaryotes with fully or partially sequenced genomes showed that they form a larger family than previously anticipated and raised the number of known prokaryotic homologs to 54. Secondary structure predictions revealed that the length of the globular N-terminal and C-terminal domains is extremely well conserved in contrast to the hinge domain and coiled-coil domains which are considerably shorter in several bacterial species. SMC proteins are present in all gram-positive bacteria and in nearly all archaea while they were found in less than half of the gram-negative bacteria. Phylogenetic analyses indicate that the SMC tree roughly resembles the 16S rRNA tree, but that cyanobacteria and Aquifex aeolicus obtained smc genes by lateral transfer from archaea. Fourteen out of 22 smc genes located in fully sequenced genomes seem to be co-transcribed with a second gene out of six different gene families, indicating that the deduced gene products might be involved in similar functions. The SMC proteins were compared with other prokaryotic proteins with long coiled-coil domains. The lengths of different protein domains and signature sequences allowed to differentiate SMCs, MukBs, which were found to be confined to gamma proteobacteria, and two subfamilies of COG 0419 including the SbcC nuclease from E. coli. A phylogenetic analysis was performed including the prokaryotic coiled-coil proteins as well as SMCs and Rad18 proteins from selected eukaryotes.

[1]  M. Slupska,et al.  Genes involved in the determination of the rate of inversions at short inverted repeats , 2000, Genes to cells : devoted to molecular & cellular mechanisms.

[2]  K. Asai,et al.  A Bacillus subtilis gene‐encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition , 1998, Molecular microbiology.

[3]  L. Kirkham,et al.  The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[4]  N. Cozzarelli,et al.  Closing the ring: links between SMC proteins and chromosome partitioning, condensation, and supercoiling. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[5]  H. Niki,et al.  Bidirectional migration of SeqA‐bound hemimethylated DNA clusters and pairing of oriC copies in Escherichia coli , 2000, Genes to cells : devoted to molecular & cellular mechanisms.

[6]  P. Graumann Bacillus subtilis SMC Is Required for Proper Arrangement of the Chromosome and for Efficient Segregation of Replication Termini but Not for Bipolar Movement of Newly Duplicated Origin Regions , 2000, Journal of bacteriology.

[7]  R. Jessberger,et al.  Mammalian SMC3 C-terminal and Coiled-coil Protein Domains Specifically Bind Palindromic DNA, Do Not Block DNA Ends, and Prevent DNA Bending* , 1999, The Journal of Biological Chemistry.

[8]  W. Pearson Rapid and sensitive sequence comparison with FASTP and FASTA. , 1990, Methods in enzymology.

[9]  P B Moens,et al.  Characterization of a novel human SMC heterodimer homologous to the Schizosaccharomyces pombe Rad18/Spr18 complex. , 2001, Molecular biology of the cell.

[10]  Dmitrij Frishman,et al.  PEDANTic genome analysis , 1997 .

[11]  M. Heck,et al.  Review: SMCs in the world of chromosome biology- from prokaryotes to higher eukaryotes. , 2000, Journal of structural biology.

[12]  R. Losick,et al.  Subcellular Localization of Bacillus subtilis SMC, a Protein Involved in Chromosome Condensation and Segregation , 1998, Journal of bacteriology.

[13]  R. Jessberger,et al.  Structural maintenance of chromosomes (SMC) proteins: conserved molecular properties for multiple biological functions. , 1999, European journal of biochemistry.

[14]  Michael Y. Galperin,et al.  The COG database: new developments in phylogenetic classification of proteins from complete genomes , 2001, Nucleic Acids Res..

[15]  T. Ogura,et al.  The new gene mukB codes for a 177 kd protein with coiled‐coil domains involved in chromosome partitioning of E. coli. , 1991, The EMBO journal.

[16]  P. Bork,et al.  Measuring genome evolution. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Thomas L. Madden,et al.  Applications of network BLAST server. , 1996, Methods in enzymology.

[18]  J. Felsenstein Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. , 1996, Methods in enzymology.

[19]  T. Hirano,et al.  SMC-mediated chromosome mechanics: a conserved scheme from bacteria to vertebrates? , 1999, Genes & development.

[20]  A. Lehmann,et al.  A novel SMC protein complex in Schizosaccharomyces pombe contains the Rad18 DNA repair protein , 2000, The EMBO journal.

[21]  H. Erickson,et al.  The Symmetrical Structure of Structural Maintenance of Chromosomes (SMC) and MukB Proteins: Long, Antiparallel Coiled Coils, Folded at a Flexible Hinge , 1998, The Journal of cell biology.

[22]  T. Ogura,et al.  E.coli MukB protein involved in chromosome partition forms a homodimer with a rod‐and‐hinge structure having DNA binding and ATP/GTP binding activities. , 1992, The EMBO journal.

[23]  T. Hirano Chromosome cohesion, condensation, and separation. , 2000, Annual review of biochemistry.

[24]  D. Leach,et al.  DNA cleavage and degradation by the SbcCD protein complex from Escherichia coli. , 1999, Nucleic acids research.

[25]  P. Graumann SMC proteins in bacteria: condensation motors for chromosome segregation? , 2001, Biochimie.

[26]  T. Hirano,et al.  ATP‐dependent aggregation of single‐stranded DNA by a bacterial SMC homodimer , 1998, The EMBO journal.

[27]  R. B. Jensen,et al.  The Caulobacter crescentus smc gene is required for cell cycle progression and chromosome segregation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. Löwe,et al.  Crystal structure of the SMC head domain: an ABC ATPase with 900 residues antiparallel coiled-coil inserted. , 2001, Journal of molecular biology.

[29]  R. Bernander Chromosome replication, nucleoid segregation and cell division in archaea. , 2000, Trends in microbiology.

[30]  H. Niki,et al.  Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli , 1999, The EMBO journal.

[31]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[32]  J R Roth,et al.  Selfish operons: horizontal transfer may drive the evolution of gene clusters. , 1996, Genetics.

[33]  A. Lupas Prediction and analysis of coiled-coil structures. , 1996, Methods in enzymology.

[34]  A. Grossman,et al.  Characterization of a prokaryotic SMC protein involved in chromosome partitioning. , 1998, Genes & development.

[35]  A. Ruepp,et al.  A 71-kDa protein from Halobacterium salinarium belongs to a ubiquitous P-loop ATPase superfamily with head-rod-tail structure , 1997, Archives of Microbiology.

[36]  T. Hirano SMC protein complexes and higher-order chromosome dynamics. , 1998, Current opinion in cell biology.

[37]  R. Bernander Archaea and the cell cycle , 1998, Molecular microbiology.