Discontinuous Occurrence of the hsp70(dnaK) Gene among Archaea and Sequence Features of HSP70 Suggest a Novel Outlook on Phylogenies Inferred from This Protein

ABSTRACT Occurrence of the hsp70 (dnaK) gene was investigated in various members of the domain Archaeacomprising both euryarchaeotes and crenarchaeotes and in the hyperthermophilic bacteria Aquifex pyrophilus andThermotoga maritima representing the deepest offshoots in phylogenetic trees of bacterial 16S rRNA sequences. The gene was not detected in 8 of 10 archaea examined but was found in A. pyrophilus and T. maritima, from which it was cloned and sequenced. Comparative analyses of the HSP70 amino acid sequences encoded in these genes, and others in the databases, showed that (i) in accordance with the vicinities seen in rRNA-based trees, the proteins from A. pyrophilus and T. maritima form a thermophilic cluster with that from the green nonsulfur bacteriumThermomicrobium roseum and are unrelated to their counterparts from gram-positive bacteria, proteobacteria/mitochondria, chlamydiae/spirochetes, deinococci, and cyanobacteria/chloroplasts; (ii) the T. maritima HSP70 clusters with the homologues from the archaea Methanobacterium thermoautotrophicum andThermoplasma acidophilum, in contrast to the postulated unique kinship between archaea and gram-positive bacteria; and (iii) there are exceptions to the reported association between an insert in HSP70 and gram negativity, or vice versa, absence of insert and gram positivity. Notably, the HSP70 from T. maritima lacks the insert, although T. maritima is phylogenetically unrelated to the gram-positive bacteria. These results, along with the absence ofhsp70 (dnaK) in various archaea and its presence in others, suggest that (i) different taxa retained either one or the other of two hsp70 (dnaK) versions (with or without insert), regardless of phylogenetic position; and (ii) archaea are aboriginally devoid of hsp70(dnaK), and those that have it must have received it from phylogenetically diverse bacteria via lateral gene transfer events that did not involve replacement of an endogenous hsp70(dnaK) gene.

[1]  S. Henikoff,et al.  Amino acid substitution matrices. , 2000, Advances in protein chemistry.

[2]  Roberta Creti,et al.  The Archaea Monophyly Issue: A Phylogeny of Translational Elongation Factor G(2) Sequences Inferred from an Optimized Selection of Alignment Positions , 1999, Journal of Molecular Evolution.

[3]  Simonetta Gribaldo,et al.  The Root of the Universal Tree of Life Inferred from Anciently Duplicated Genes Encoding Components of the Protein-Targeting Machinery , 1998, Journal of Molecular Evolution.

[4]  R. Huber,et al.  The complete genome of the hyperthermophilic bacterium Aquifex aeolicus , 1998, Nature.

[5]  F. Brinkman,et al.  Phylogenetic analysis. , 1998, Methods of biochemical analysis.

[6]  R. Fleischmann,et al.  The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus , 1997, Nature.

[7]  G. Church,et al.  Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics , 1997, Journal of bacteriology.

[8]  E. Stackebrandt,et al.  The presence of a dnaK (HSP70) multigene family in members of the orders Planctomycetales and Verrucomicrobiales , 1997, Journal of bacteriology.

[9]  B. Ahring,et al.  Heat-Shock Response in Methanosarcina mazei S-6 , 1997, Current Microbiology.

[10]  K. Strimmer,et al.  Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[11]  R. Gupta,et al.  Sequencing of heat shock protein 70 (DnaK) homologs from Deinococcus proteolyticus and Thermomicrobium roseum and their integration in a protein-based phylogeny of prokaryotes , 1997, Journal of bacteriology.

[12]  G. Church,et al.  Complete Genome Sequence of Methanobacterium thermoautotrophicum D H: Functional Analysis and Comparative Genomics , 1997 .

[13]  A. Dress,et al.  Multiple DNA and protein sequence alignment based on segment-to-segment comparison. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. R. Brown,et al.  A chimeric origin for eukaryotes re-examined. , 1996, Trends in biochemical sciences.

[15]  R. L. Charlebois,et al.  Phylogenetic analysis of carbamoylphosphate synthetase genes: complex evolutionary history includes an internal duplication within a gene which can root the tree of life. , 1996, Molecular biology and evolution.

[16]  K. Strimmer,et al.  Quartet Puzzling: A Quartet Maximum-Likelihood Method for Reconstructing Tree Topologies , 1996 .

[17]  N. Pace,et al.  Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J D Palmer,et al.  The root of the universal tree and the origin of eukaryotes based on elongation factor phylogeny. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[19]  F. Hartl Molecular chaperones in cellular protein folding , 1996, Nature.

[20]  W. Doolittle,et al.  Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[21]  G. B. Golding,et al.  Protein-based phylogenies support a chimeric origin for the eukaryotic genome. , 1995, Molecular biology and evolution.

[22]  R. Overbeek,et al.  The winds of (evolutionary) change: breathing new life into microbiology. , 1996, Journal of bacteriology.

[23]  Radhey S. Gupta,et al.  Phylogenetic analysis of 70 kD heat shock protein sequences suggests a chimeric origin for the eukaryotic cell nucleus , 1994, Current Biology.

[24]  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.

[25]  H. Yoshikawa,et al.  Identification of dnaK multigene family in Synechococcus sp. PCC7942. , 1994, Biochemical and biophysical research communications.

[26]  R. Gupta,et al.  Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[27]  B. Seaton,et al.  A gene encoding a DnaK/hsp70 homolog in Escherichia coli. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[28]  P. D. Rijk,et al.  About the Order of Divergence of the Major Bacterial Taxa During Evolution , 1994 .

[29]  A. Sanangelantoni,et al.  Cloning and sequencing of the gene encoding glutamine synthetase I from the archaeum Pyrococcus woesei: anomalous phylogenies inferred from analysis of archaeal and bacterial glutamine synthetase I sequences , 1993, Journal of bacteriology.

[30]  H. Klenk,et al.  Chapter 12 Transcription in archaea , 1993 .

[31]  M. Kates,et al.  The Biochemistry of archaea (archaebacteria) , 1993 .

[32]  T. Cavalier-smith Origins of secondary metabolism. , 2007, Ciba Foundation symposium.

[33]  S. Henikoff,et al.  Amino acid substitution matrices from protein blocks. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[34]  R. Huber,et al.  Aquifex pyrophilus gen. nov. sp. nov., Represents a Novel Group of Marine Hyperthermophilic Hydrogen-Oxidizing Bacteria , 1992 .

[35]  G. Olsen,et al.  A phylogenetic analysis of Aquifex pyrophilus. , 1992, Systematic and applied microbiology.

[36]  R. Gupta,et al.  Cloning of the HSP70 gene from Halobacterium marismortui: relatedness of archaebacterial HSP70 to its eubacterial homologs and a model for the evolution of the HSP70 gene , 1992, Journal of bacteriology.

[37]  E. Conway de Macario,et al.  A dnaK homolog in the archaebacterium Methanosarcina mazei S6. , 1991, Gene.

[38]  K. Jarrell,et al.  Heat shock response of the archaebacterium Methanococcus voltae , 1991, Journal of bacteriology.

[39]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[40]  O. Kandler,et al.  Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[41]  S. Osawa,et al.  Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Masasuke Yoshida,et al.  Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[43]  D. Lipman,et al.  Improved tools for biological sequence comparison. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[44]  J. Devereux,et al.  A comprehensive set of sequence analysis programs for the VAX , 1984, Nucleic Acids Res..

[45]  H. Hartman,et al.  The origin of the eukaryotic cell. , 1984, Speculations in science and technology.

[46]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[47]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[48]  C. Woese,et al.  Phylogenetic structure of the prokaryotic domain: The primary kingdoms , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[49]  N. Blin,et al.  A general method for isolation of high molecular weight DNA from eukaryotes. , 1976, Nucleic acids research.