Discontinuous Occurrence of the hsp70 ( dnaK ) Gene among Archaea and Sequence Features of HSP70 Suggest a Novel Outlook on Phylogenies Inferred from This Protein
10.1128/jb.181.2.434-443.1999
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

ABSTRACT Occurrence of the hsp70 ( dnaK ) gene was investigated in various members of the domain Archaea comprising both euryarchaeotes and crenarchaeotes and in the hyperthermophilic bacteria Aquifex pyrophilus and Thermotoga 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 bacterium Thermomicrobium 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 and Thermoplasma 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 of hsp70 ( 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.

Bibliography

Gribaldo, S., Lumia, V., Creti, R., Conway de Macario, E., Sanangelantoni, A., & Cammarano, P. (1999). Discontinuous Occurrence of the hsp70 ( dnaK ) Gene among Archaea and Sequence Features of HSP70 Suggest a Novel Outlook on Phylogenies Inferred from This Protein. Journal of Bacteriology, 181(2), 434–443.

Authors 6
  1. Simonetta Gribaldo (first)
  2. Valentina Lumia (additional)
  3. Roberta Creti (additional)
  4. Everly Conway de Macario (additional)
  5. Annamaria Sanangelantoni (additional)
  6. Piero Cammarano (additional)
References 55 Referenced 83
  1. 10.1016/S0022-2836(05)80360-2
  2. Baldauf S. L. Palmer J. D. Doolittle W. F. The root of the universal tree and the origin of eucaryotes based on elongation factor phylogeny.Proc. Natl. Acad. Sci. USA93199677497754 (10.1073/pnas.93.15.7749) / Proc. Natl. Acad. Sci. USA / The root of the universal tree and the origin of eucaryotes based on elongation factor phylogeny by Baldauf S. L. (1996)
  3. Barns S. M. Delwiche C. F. Palmer J. D. Pace N. R. Perspectives on archaeal diversity, thermophily and monophily from environmental rRNA sequences.Proc. Natl. Acad. Sci. USA93199691889183 (10.1073/pnas.93.17.9188) / Proc. Natl. Acad. Sci. USA / Perspectives on archaeal diversity, thermophily and monophily from environmental rRNA sequences by Barns S. M. (1996)
  4. Blin N. Stafford D. W. A general method for the isolation of high molecular weight DNA from eukaryotes.Nucleic Acids Res.3197623032308 (10.1093/nar/3.9.2303) / Nucleic Acids Res. / A general method for the isolation of high molecular weight DNA from eukaryotes by Blin N. (1976)
  5. Bocchetta M. Ceccarelli E. Creti R. Sanangelantoni A. M. Tiboni O. Cammarano P. Arrangement and nucleotide sequence of the gene (fus) encoding elongation factor G (EF-G) from the hyperthermophilic bacterium Aquifex pyrophilus: phylogenetic depth of hyperthermophilic bacteria inferred from analysis of the EF-G/fus sequences.J. Mol. Evol.411995803812 (10.1007/BF00173160) / J. Mol. Evol. / Arrangement and nucleotide sequence of the gene (fus) encoding elongation factor G (EF-G) from the hyperthermophilic bacterium Aquifex pyrophilus: phylogenetic depth of hyperthermophilic bacteria inferred from analysis of the EF-G/fus sequences by Bocchetta M. (1995)
  6. Boorstein W. R. Zeigelhoffer T. Craig E. A. Molecular evolution of the HSP70 multigene family.J. Mol. Evol.381994117 (10.1007/BF00175490) / J. Mol. Evol. / Molecular evolution of the HSP70 multigene family by Boorstein W. R. (1994)
  7. Brown J. R. Doolittle W. F. Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications.Proc. Natl. Acad. Sci. USA92199524412445 (10.1073/pnas.92.7.2441) / Proc. Natl. Acad. Sci. USA / Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications by Brown J. R. (1995)
  8. Brown J. R. Masuchi Y. Robb F. T. Doolittle W. F. Evolutionary relationships of bacterial and archaeal glutamine synthetase genes.J. Mol. Evol.381994566576 (10.1007/BF00175876) / J. Mol. Evol. / Evolutionary relationships of bacterial and archaeal glutamine synthetase genes by Brown J. R. (1994)
  9. Bult C. J. White O. Olsen G. J. Zhou L. Fleischmann R. D. Sutton G. G. Blake J. A. FitzGerald L. M. Clayton R. A. Gocayne J. D. Kerlavage A. R. Dougherty B. A. Tomb J.-F. Adams M. D. Reich C. I. Overbeek R. Kirkness E. F. Weinstock K. G. Merrick J. M. Glodek A. Scott J. L. Geoghagen N. S. M. Weidman J. F. Fuhrmann J. L. Nguyen D. Utterback T. R. Kelley J. M. Peterson J. D. Sadow P. W. Hanna M. C. Cotton M. D. Roberts K. M. Hurst M. A. Kaine B. P. Borodovsky M. Klenk H.-P. Fraser C. M. Smith H. O. Woese C. R. Venter J. C. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschi.Science273199610581073 (10.1126/science.273.5278.1058) / Science / Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschi by Bult C. J. (1996)
  10. Burggraff S. Olsen G. J. Stetter K. O. Woese C. R. A phylogenetic analysis of Aquifex pyrophilus.Syst. Appl. Microbiol.151992352356 (10.1016/S0723-2020(11)80207-9) / Syst. Appl. Microbiol. / A phylogenetic analysis of Aquifex pyrophilus by Burggraff S. (1992)
  11. Cammarano P. R. Creti A. M. Sanangelantoni and P. Palm. Splitting the Archaea? A phylogeny of translational elongation factor G(2) sequences inferred from an optimized selection of alignment positions. J. Mol. Evol. in press.
  12. Cavalier-Smith T. Origins of secondary metabolism.Ciba Found. Symp.17119926487 / Ciba Found. Symp. / Origins of secondary metabolism by Cavalier-Smith T. (1992)
  13. Craig E. A. Kang P. J. Boorstein W. A review of the role of 70k Da heat shock proteins in protein translocation across membranes.Antonie Leeuwenhoek581990137146 (10.1007/BF00548924) / Antonie Leeuwenhoek / A review of the role of 70k Da heat shock proteins in protein translocation across membranes by Craig E. A. (1990)
  14. Deckert G. Warren P. V. Gaasterland T. Young W. G. Lenox A. L. Graham D. E. Overbeek R. Snead M. A. Keller M. Aujay M. Huber R. Feldman R. A. Short J. M. Olsen G. J. Swanson R. V. The complete genome of the hyperthermophilic bacterium Aquifex aeolicus.Nature3921998353358 (10.1038/32831) / Nature / The complete genome of the hyperthermophilic bacterium Aquifex aeolicus by Deckert G. (1998)
  15. Devereux J. Haeberli P. Smithies O. A comprehensive set of sequence analysis program for the VAX.Nucleic Acids Res.121984387395 (10.1093/nar/12.1Part1.387) / Nucleic Acids Res. / A comprehensive set of sequence analysis program for the VAX by Devereux J. (1984)
  16. Felsenstein J. PHYLIP (Phylogeny Inference Package) version 3.5c. 1993 Department of Genetics University of Washington Seattle Wash (Distributed by the author.)
  17. Gogarten J. P. Kibak H. Dittrich P. Taiz L. Bowman E. Bowman M. Manolson M. F. Poole R. J. Date T. Oshima T. Konishi T. Denda K. Yoshida M. Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes.Proc. Natl. Acad. Sci. USA86198966616665 (10.1073/pnas.86.17.6661) / Proc. Natl. Acad. Sci. USA / Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes by Gogarten J. P. (1989)
  18. Golding G. B. Gupta R. S. Protein based phylogenies support a chimeric origin for the eukaryotic genome.Mol. Biol. Evol.12199516 (10.1093/oxfordjournals.molbev.a040178) / Mol. Biol. Evol. / Protein based phylogenies support a chimeric origin for the eukaryotic genome by Golding G. B. (1995)
  19. Gribaldo S. Cammarano P. The root of the universal tree of life inferred from anciently duplicated genes encoding components of the protein-targeting machinery.J. Mol. Evol.471998508516 (10.1007/PL00006407) / J. Mol. Evol. / The root of the universal tree of life inferred from anciently duplicated genes encoding components of the protein-targeting machinery by Gribaldo S. (1998)
  20. 10.1128/jb.174.14.4594-4605.1992
  21. Gupta R. S. Golding G. B. Evolution of HSP70 gene and its implications regarding relationships between Archaebacteria, Eubacteria and Eukaryotes.J. Mol. Evol.371993573582 (10.1007/BF00182743) / J. Mol. Evol. / Evolution of HSP70 gene and its implications regarding relationships between Archaebacteria, Eubacteria and Eukaryotes by Gupta R. S. (1993)
  22. Gupta R. S. Singh B. Phylogenetic analysis of 70 kDa heat shock protein sequences suggests a chimeric origin for the eukaryotic cell nucleus.Curr. Biol.4199411041114 (10.1016/S0960-9822(00)00249-9) / Curr. Biol. / Phylogenetic analysis of 70 kDa heat shock protein sequences suggests a chimeric origin for the eukaryotic cell nucleus by Gupta R. S. (1994)
  23. Gupta R. S. Aitken K. Falah M. Singh B. Cloning of Giardia lamblia heat shock protein hsp70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum.Proc. Natl. Acad. Sci. USA91199428952899 (10.1073/pnas.91.8.2895) / Proc. Natl. Acad. Sci. USA / Cloning of Giardia lamblia heat shock protein hsp70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum by Gupta R. S. (1994)
  24. Gupta R. S. Golding G. B. The origin of the eukaryotic cell.Trends Biochem. Sci.211996166171 (10.1016/S0968-0004(96)20013-1) / Trends Biochem. Sci. / The origin of the eukaryotic cell by Gupta R. S. (1996)
  25. 10.1128/jb.179.2.345-357.1997
  26. Hartl F. U. Molecular chaperones in cellular protein folding.Nature3811996571580 (10.1038/381571a0) / Nature / Molecular chaperones in cellular protein folding by Hartl F. U. (1996)
  27. Henikoff S. Henikoff J. G. Amino acid substitution matrices from protein blocks.Proc. Natl. Acad. Sci. USA8919921091510919 (10.1073/pnas.89.22.10915) / Proc. Natl. Acad. Sci. USA / Amino acid substitution matrices from protein blocks by Henikoff S. (1992)
  28. Herbert M. Kropinski A. M. Jarrel K. F. Heat shock response of the archaebacterium Methanococcus voltae.J. Bacteriol.173199132243227 (10.1128/JB.173.10.3224-3227.1991) / J. Bacteriol. / Heat shock response of the archaebacterium Methanococcus voltae by Herbert M. (1991)
  29. 10.1007/BF00409880
  30. Huber R. Wilharm T. Huber D. Trincone A. Burggraf S. Konig H. Rachel H. Rockinger I. Fricke H. Stetter K. O. Aquifex pyrophilus gen. nov. sp. nov. represents a novel group of marine hyperthermophilic hydrogen oxidizing Bacteria.Syst. Appl. Microbiol.151992340351 (10.1016/S0723-2020(11)80206-7) / Syst. Appl. Microbiol. / Aquifex pyrophilus gen. nov. sp. nov. represents a novel group of marine hyperthermophilic hydrogen oxidizing Bacteria by Huber R. (1992)
  31. Iwabe N. Kuma K. Hasegawa M. Osawa S. Miyata T. Evolutionary relationship of Archaea, Bacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes.Proc. Natl. Acad. Sci. USA86198993559359 (10.1073/pnas.86.23.9355) / Proc. Natl. Acad. Sci. USA / Evolutionary relationship of Archaea, Bacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes by Iwabe N. (1989)
  32. 10.1038/37052
  33. Lange M. Macario A. J. L. Ahring B. Conway de Macario E. Heat shock response in Methanosarcina mazei S-6.Curr. Microbiol.351997116121 (10.1007/s002849900222) / Curr. Microbiol. / Heat shock response in Methanosarcina mazei S-6 by Lange M. (1997)
  34. Lindquist S. Craig E. A. The heat shock proteins.Annu. Rev. Genet.221988631677 (10.1146/annurev.ge.22.120188.003215) / Annu. Rev. Genet. / The heat shock proteins by Lindquist S. (1988)
  35. Lawson F. S. Charlebois R. L. Dillon J. A. R. Phylogenetic analysis of carbamoylphosphate synthetase genes: evolution involving multiple gene duplications, gene fusions, and insertions and deletions of surrounding sequences.Mol. Biol. Evol.131996970977 / Mol. Biol. Evol. / Phylogenetic analysis of carbamoylphosphate synthetase genes: evolution involving multiple gene duplications, gene fusions, and insertions and deletions of surrounding sequences by Lawson F. S. (1996)
  36. Ludwig W. Weizenegger M. Betzl D. Leidel E. Lenz T. Ludvigsen A. Mollendorf D. Wenzig P. Schleifer K. H. Complete nucleotide sequence of seven eubacterial genes coding for the elongation factor Tu: functional, structural and phylogenetic evaluations.Arch. Microbiol.1531990241247 (10.1007/BF00249075) / Arch. Microbiol. / Complete nucleotide sequence of seven eubacterial genes coding for the elongation factor Tu: functional, structural and phylogenetic evaluations by Ludwig W. (1990)
  37. Macario A. J. L. Dugan C. B. Conway de Macario E. A dnaK homolog in the archaebacterium Methanosarcina mazei S-6.Gene1081991133137 (10.1016/0378-1119(91)90498-Z) / Gene / A dnaK homolog in the archaebacterium Methanosarcina mazei S-6 by Macario A. J. L. (1991)
  38. Morgenstern B. Dress A. Werner T. Multiple DNA and protein sequence alignment based on segment-to-segment comparison.Proc. Natl. Acad. Sci. USA9319961209812103 (10.1073/pnas.93.22.12098) / Proc. Natl. Acad. Sci. USA / Multiple DNA and protein sequence alignment based on segment-to-segment comparison by Morgenstern B. (1996)
  39. Nimura K. Yoshikawa H. Takahashi H. Identification of dnaK multigene family in Synechococcus sp. strain PCC 7942.Biochem. Biophys. Res. Commun.2011994466471 (10.1006/bbrc.1994.1724) / Biochem. Biophys. Res. Commun. / Identification of dnaK multigene family in Synechococcus sp. strain PCC 7942 by Nimura K. (1994)
  40. 10.1128/jb.176.1.1-6.1994
  41. Pearson W. R. Lipman D. J. Improved tools for biological sequence comparisons.Proc. Natl. Acad. Sci. USA85198824442448 (10.1073/pnas.85.8.2444) / Proc. Natl. Acad. Sci. USA / Improved tools for biological sequence comparisons by Pearson W. R. (1988)
  42. Roger A. J. Brown J. R. A chimeric origin for eukaryotes re-examined.Trends Biol. Sci.211996370371 (10.1016/0968-0004(96)20023-4) / Trends Biol. Sci. / A chimeric origin for eukaryotes re-examined by Roger A. J. (1996)
  43. Sambrook J. Fritsch E. F. Maniatis T. Molecular cloning: a laboratory manual 2nd ed. 1989 Cold Spring Harbor Laboratory Cold Spring Harbor N.Y
  44. Sanger F. Nicklen S. Coulson A. R. DNA sequencing with chain-terminating inhibitors.Proc. Natl. Acad. Sci. USA74197754635467 (10.1073/pnas.74.12.5463) / Proc. Natl. Acad. Sci. USA / DNA sequencing with chain-terminating inhibitors by Sanger F. (1977)
  45. Seaton B. L. Vickery L. E. A gene encoding a new Dnak/hsp70 homolog in Escherichia coli.Proc. Natl. Acad. Sci. USA91199420662070 (10.1073/pnas.91.6.2066) / Proc. Natl. Acad. Sci. USA / A gene encoding a new Dnak/hsp70 homolog in Escherichia coli by Seaton B. L. (1994)
  46. Smith D. R. Doucette-Stamm L. A. Deloughery C. Lee H. Dubois J. Aldredge T. Bashirzadeh R. Blakely D. Cook R. Gilbert K. Harrison D. Hoang L. Keagle P. Lumm W. Pothier B. Qiu D. Spadafora R. Vicaire R. Wang T. Y. Wierzbowski J. Gibson R. Jiwani N. Caruso A. Bush D. Safer H. Patwell D. Prabhakar S. McDougall S. Shimer G. Goyal A. Pietrokovski S. Church G. M. Daniles C. J. Mao J.-I. Rice P. Nölling J. Reeve J. N. Complete genome sequence of Methanobacterium thermoautotrophicum ΔH: functional analysis and comparative genomics.J. Bacteriol.179199771357155 (10.1128/JB.179.22.7135-7155.1997) / J. Bacteriol. / Complete genome sequence of Methanobacterium thermoautotrophicum ΔH: functional analysis and comparative genomics by Smith D. R. (1997)
  47. Strimmer K. Von Haeseler A. Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies.Mol. Biol. Evol.131996964969 (10.1093/oxfordjournals.molbev.a025664) / Mol. Biol. Evol. / Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies by Strimmer K. (1996)
  48. Strimmer K. Von Haeseler A. Likelihood mapping: a simple method to visualize the phylogenetic content of a sequence alignment.Proc. Natl. Acad. Sci. USA94199768156819 (10.1073/pnas.94.13.6815) / Proc. Natl. Acad. Sci. USA / Likelihood mapping: a simple method to visualize the phylogenetic content of a sequence alignment by Strimmer K. (1997)
  49. Thompson J. D. Higgins D. G. Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple alignment through sequence weighting, positions-specific gap penalties and weight matrix choice.Nucleic Acids Res.22199446734680 (10.1093/nar/22.22.4673) / Nucleic Acids Res. / CLUSTAL W: improving the sensitivity of progressive multiple alignment through sequence weighting, positions-specific gap penalties and weight matrix choice by Thompson J. D. (1994)
  50. 10.1128/jb.175.10.2961-2969.1993
  51. Van De Peer Y. Neef J. M. De Rijk P. De Vos P. De Wachter R. About the order of divergence of the major bacterial taxa during evolution.Syst. Appl. Microbiol.1719943238 (10.1016/S0723-2020(11)80028-7) / Syst. Appl. Microbiol. / About the order of divergence of the major bacterial taxa during evolution by Van De Peer Y. (1994)
  52. Ward-Rayney N. Rainey F. A. Stackebrandt E. The presence of a dnaK (HSP70) multigene family in members of the orders Planctomycetales and Verrucomicrobiales.J. Bacteriol.179199763606366 (10.1128/JB.179.20.6360-6366.1997) / J. Bacteriol. / The presence of a dnaK (HSP70) multigene family in members of the orders Planctomycetales and Verrucomicrobiales by Ward-Rayney N. (1997)
  53. Woese C. R. Fox G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms.Proc. Natl. Acad. Sci. USA511977221271 / Proc. Natl. Acad. Sci. USA / Phylogenetic structure of the prokaryotic domain: the primary kingdoms by Woese C. R. (1977)
  54. Woese C. R. Kandler O. Wheelis M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria and Eucarya.Proc. Natl. Acad. Sci. USA87199045764579 (10.1073/pnas.87.12.4576) / Proc. Natl. Acad. Sci. USA / Towards a natural system of organisms: proposal for the domains Archaea, Bacteria and Eucarya by Woese C. R. (1990)
  55. Zillig W. Palm P. Klenk H.-P. Langer D. Hudepohl U. Hain J. Lanzendorfer M. Holz I. Transcription in Archea The biochemistry of Archaea (Archaebacteria). Kates M. Kushner D. J. Matheson A. T. 1993 367 386 Elsevier Science Publishers B.V. Amsterdam The Netherlands (10.1016/S0167-7306(08)60261-6)
Dates
Type When
Created 5 years, 8 months ago (Dec. 31, 2019, 11:41 a.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 1:50 p.m.)
Indexed 1 year ago (Aug. 5, 2024, 4:37 p.m.)
Issued 26 years, 7 months ago (Jan. 15, 1999)
Published 26 years, 7 months ago (Jan. 15, 1999)
Published Print 26 years, 7 months ago (Jan. 15, 1999)
Funders 0

None

@article{Gribaldo_1999, title={Discontinuous Occurrence of the hsp70 ( dnaK ) Gene among Archaea and Sequence Features of HSP70 Suggest a Novel Outlook on Phylogenies Inferred from This Protein}, volume={181}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.181.2.434-443.1999}, DOI={10.1128/jb.181.2.434-443.1999}, number={2}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Gribaldo, Simonetta and Lumia, Valentina and Creti, Roberta and Conway de Macario, Everly and Sanangelantoni, Annamaria and Cammarano, Piero}, year={1999}, month=jan, pages={434–443} }