Home LiteratureArticle Details
PMID: 15466593 Published · epublish English Comparative Study Journal Article

Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging.

Nucleic acids research ·Vol. 32 ·No. 17 ·2004-00-00 ·Pages 5260-79

Iyer LM, Makarova KS, Koonin EV, Aravind L

Abstract

Recently, it has been shown that a predicted P-loop ATPase (the HerA or MlaA protein), which is highly conserved in archaea and also present in many bacteria but absent in eukaryotes, has a bidirectional helicase activity and forms hexameric rings similar to those described for the TrwB ATPase. In this study, the FtsK-HerA superfamily of P-loop ATPases, in which the HerA clade comprises one of the major branches, is analyzed in detail. We show that, in addition to the FtsK and HerA clades, this superfamily includes several families of characterized or predicted ATPases which are predominantly involved in extrusion of DNA and peptides through membrane pores. The DNA-packaging ATPases of various bacteriophages and eukaryotic double-stranded DNA viruses also belong to the FtsK-HerA superfamily. The FtsK protein is the essential bacterial ATPase that is responsible for the correct segregation of daughter chromosomes during cell division. The structural and evolutionary relationship between HerA and FtsK and the nearly perfect complementarity of their phyletic distributions suggest that HerA similarly mediates DNA pumping into the progeny cells during archaeal cell division. It appears likely that the HerA and FtsK families diverged concomitantly with the archaeal-bacterial division and that the last universal common ancestor of modern life forms had an ancestral DNA-pumping ATPase that gave rise to these families. Furthermore, the relationship of these cellular proteins with the packaging ATPases of diverse DNA viruses suggests that a common DNA pumping mechanism might be operational in both cellular and viral genome segregation. The herA gene forms a highly conserved operon with the gene for the NurA nuclease and, in many archaea, also with the orthologs of eukaryotic double-strand break repair proteins MRE11 and Rad50. HerA is predicted to function in a complex with these proteins in DNA pumping and repair of double-stranded breaks introduced during this process and, possibly, also during DNA replication. Extensive comparative analysis of the 'genomic context' combined with in-depth sequence analysis led to the prediction of numerous previously unnoticed nucleases of the NurA superfamily, including a specific version that is likely to be the endonuclease component of a novel restriction-modification system. This analysis also led to the identification of previously uncharacterized nucleases, such as a novel predicted nuclease of the Sir2-type Rossmann fold, and phosphatases of the HAD superfamily that are likely to function as partners of the FtsK-HerA superfamily ATPases.

MeSH Terms
Adenosine Triphosphatases/chemistry,classification,genetics Amino Acid Sequence Archaea/enzymology,genetics Archaeal Proteins/chemistry,classification,genetics Bacteria/enzymology,genetics Bacterial Proteins/chemistry,classification,genetics Capsid Proteins/physiology Cell Division Chromosome Segregation Endonucleases/chemistry Escherichia coli Proteins Evolution, Molecular Genomics Membrane Proteins/chemistry,classification,genetics Membrane Transport Proteins/chemistry,classification,genetics Molecular Sequence Data Phylogeny Protein Structure, Tertiary Sequence Alignment Viral Proteins/chemistry,classification,genetics Virus Assembly/genetics Viruses/enzymology,genetics
Chemicals
Archaeal Proteins Bacterial Proteins Capsid Proteins Escherichia coli Proteins FtsK protein, E coli Membrane Proteins Membrane Transport Proteins Viral Proteins Endonucleases Adenosine Triphosphatases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Iyer Lakshminarayan M
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA.
Makarova Kira S
Koonin Eugene V
Aravind L
References (106)
106 references, click to expand
  1. Characterization of ATP and DNA binding activities of TrwB, the coupling protein essential in plasmid R388 conjugation.
    J Biol Chem. 1999 Dec 17;274(51):36117-24 PMID: 10593894
  2. The bacterial replicative helicase DnaB evolved from a RecA duplication.
    Genome Res. 2000 Jan;10(1):5-16 PMID: 10645945
  3. TraG from RP4 and TraG and VirD4 from Ti plasmids confer relaxosome specificity to the conjugal transfer system of pTiC58.
    J Bacteriol. 2000 Mar;182(6):1541-8 PMID: 10692358
  4. Gene and context: integrative approaches to genome analysis.
    Adv Protein Chem. 2000;54:345-79 PMID: 10829232
  5. Who's your neighbor? New computational approaches for functional genomics.
    Nat Biotechnol. 2000 Jun;18(6):609-13 PMID: 10835597
  6. Exploitation of gene context.
    Curr Opin Struct Biol. 2000 Jun;10(3):366-70 PMID: 10851194
  7. Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides.
    Cell. 2000 Jun 9;101(6):589-600 PMID: 10892646
  8. The roles of mutS, sbcCD and recA in the propagation of TGG repeats in Escherichia coli.
    Nucleic Acids Res. 2000 Aug 15;28(16):3178-84 PMID: 10931934
  9. Guilt by association: contextual information in genome analysis.
    Genome Res. 2000 Aug;10(8):1074-7 PMID: 10958625
  10. T-Coffee: A novel method for fast and accurate multiple sequence alignment.
    J Mol Biol. 2000 Sep 8;302(1):205-17 PMID: 10964570
  11. Themes and variations in prokaryotic cell division.
    FEMS Microbiol Rev. 2000 Oct;24(4):531-48 PMID: 10978550
  12. Structural biology. Pumping DNA.
    Nature. 2001 Feb 1;409(6820):573, 575 PMID: 11214304
  13. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase.
    Nature. 2001 Feb 1;409(6820):637-41 PMID: 11214325
  14. Enzymatic activities of Sir2 and chromatin silencing.
    Curr Opin Cell Biol. 2001 Apr;13(2):232-8 PMID: 11248558
  15. Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines.
    Mol Microbiol. 2001 Apr;40(2):294-305 PMID: 11309113
  16. Crystal structure of a SIR2 homolog-NAD complex.
    Cell. 2001 Apr 20;105(2):269-79 PMID: 11336676
  17. Zonula occludens toxin structure-function analysis. Identification of the fragment biologically active on tight junctions and of the zonulin receptor binding domain.
    J Biol Chem. 2001 Jun 1;276(22):19160-5 PMID: 11278543
  18. Structure of the histone deacetylase SIRT2.
    Nat Struct Biol. 2001 Jul;8(7):621-5 PMID: 11427894
  19. DNA transport in bacteria.
    Nat Rev Mol Cell Biol. 2001 Jul;2(7):538-45 PMID: 11433368
  20. Circles: the replication-recombination-chromosome segregation connection.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8189-95 PMID: 11459952
  21. Structure and mechanism of the RuvB Holliday junction branch migration motor.
    J Mol Biol. 2001 Aug 10;311(2):297-310 PMID: 11478862
  22. Common origin of four diverse families of large eukaryotic DNA viruses.
    J Virol. 2001 Dec;75(23):11720-34 PMID: 11689653
  23. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division.
    Mol Microbiol. 2001 Oct;42(2):395-413 PMID: 11703663
  24. Bacterial ancestry of actin and tubulin.
    Curr Opin Microbiol. 2001 Dec;4(6):634-8 PMID: 11731313
  25. The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life.
    Proc Natl Acad Sci U S A. 2004 May 18;101(20):7716-20 PMID: 15123802
  26. The SHS2 module is a common structural theme in functionally diverse protein groups, like Rpb7p, FtsA, GyrI, and MTH1598/TM1083 superfamilies.
    Proteins. 2004 Sep 1;56(4):795-807 PMID: 15281131
  27. On the maximum likelihood method in molecular phylogenetics.
    J Mol Evol. 1991 May;32(5):443-5 PMID: 1904100
  28. Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria.
    Nucleic Acids Res. 1992 Jul 11;20(13):3279-85 PMID: 1630899
  29. The second cholera toxin, Zot, and its plasmid-encoded and phage-encoded homologues constitute a group of putative ATPases with an altered purine NTP-binding motif.
    FEBS Lett. 1992 Nov 2;312(1):3-6 PMID: 1426234
  30. The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain.
    J Bacteriol. 1993 Mar;175(6):1723-34 PMID: 8449880
  31. Gene A32 product of vaccinia virus may be an ATPase involved in viral DNA packaging as indicated by sequence comparisons with other putative viral ATPases.
    Virus Genes. 1993 Feb;7(1):89-94 PMID: 8470370
  32. PHD--an automatic mail server for protein secondary structure prediction.
    Comput Appl Biosci. 1994 Feb;10(1):53-60 PMID: 8193956
  33. Promiscuous DNA transfer system of Agrobacterium tumefaciens: role of the virB operon in sex pilus assembly and synthesis.
    Mol Microbiol. 1994 Apr;12(1):17-22 PMID: 7914664
  34. An essential virulence protein of Agrobacterium tumefaciens, VirB4, requires an intact mononucleotide binding domain to function in transfer of T-DNA.
    Mol Gen Genet. 1994 Dec 15;245(6):704-15 PMID: 7830718
  35. Zonula occludens toxin modulates tight junctions through protein kinase C-dependent actin reorganization, in vitro.
    J Clin Invest. 1995 Aug;96(2):710-20 PMID: 7635964
  36. DNA processing reactions in bacterial conjugation.
    Annu Rev Biochem. 1995;64:141-69 PMID: 7574478
  37. Dali: a network tool for protein structure comparison.
    Trends Biochem Sci. 1995 Nov;20(11):478-80 PMID: 8578593
  38. ProMod and Swiss-Model: Internet-based tools for automated comparative protein modelling.
    Biochem Soc Trans. 1996 Feb;24(1):274-9 PMID: 8674685
  39. A duplicated catalytic motif in a new superfamily of phosphohydrolases and phospholipid synthases that includes poxvirus envelope proteins.
    Trends Biochem Sci. 1996 Jul;21(7):242-3 PMID: 8755242
  40. Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods.
    Methods Enzymol. 1996;266:418-27 PMID: 8743697
  41. Extracting protein alignment models from the sequence database.
    Nucleic Acids Res. 1997 May 1;25(9):1665-77 PMID: 9108146
  42. Archaea and the origin(s) of DNA replication proteins.
    Cell. 1997 Jun 27;89(7):995-8 PMID: 9215620
  43. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  44. Confirmation of the arginine-finger hypothesis for the GAP-stimulated GTP-hydrolysis reaction of Ras.
    Nat Struct Biol. 1997 Sep;4(9):686-9 PMID: 9302992
  45. SEALS: a system for easy analysis of lots of sequences.
    Proc Int Conf Intell Syst Mol Biol. 1997;5:333-9 PMID: 9322058
  46. G proteins. The arginine finger strikes again.
    Nature. 1997 Oct 16;389(6652):673-4 PMID: 9338774
  47. Repair by recombination of DNA containing a palindromic sequence.
    Mol Microbiol. 1997 Nov;26(3):597-606 PMID: 9402028
  48. The catalytic domain of the P-type ATPase has the haloacid dehalogenase fold.
    Trends Biochem Sci. 1998 Apr;23(4):127-9 PMID: 9584613
  49. Role of the C terminus of FtsK in Escherichia coli chromosome segregation.
    J Bacteriol. 1998 Dec;180(23):6424-8 PMID: 9829960
  50. AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes.
    Genome Res. 1999 Jan;9(1):27-43 PMID: 9927482
  51. Spatial regulation of cytokinesis in bacteria.
    Curr Opin Microbiol. 2001 Dec;4(6):647-52 PMID: 11731315
  52. Transmembrane topology prediction methods: a re-assessment and improvement by a consensus method using a dataset of experimentally-characterized transmembrane topologies.
    In Silico Biol. 2002;2(1):19-33 PMID: 11808871
  53. FtsK Is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases.
    Cell. 2002 Jan 25;108(2):195-205 PMID: 11832210
  54. FtsK: Maxwell's Demon?
    Mol Cell. 2002 Feb;9(2):206-7 PMID: 11864592
  55. Classification and evolution of P-loop GTPases and related ATPases.
    J Mol Biol. 2002 Mar 15;317(1):41-72 PMID: 11916378
  56. The ESAT-6/WXG100 superfamily -- and a new Gram-positive secretion system?
    Trends Microbiol. 2002 May;10(5):209-12 PMID: 11973144
  57. A novel family of mobile genetic elements is limited to the germline genome in Tetrahymena thermophila.
    Nucleic Acids Res. 2002 Jun 1;30(11):2524-37 PMID: 12034842
  58. Detection of novel members, structure-function analysis and evolutionary classification of the 2H phosphoesterase superfamily.
    Nucleic Acids Res. 2002 Dec 1;30(23):5229-43 PMID: 12466548
  59. AAA proteins.
    Curr Opin Struct Biol. 2002 Dec;12(6):746-53 PMID: 12504679
  60. REBASE: restriction enzymes and methyltransferases.
    Nucleic Acids Res. 2003 Jan 1;31(1):418-20 PMID: 12520038
  61. A rotary pumping model for helicase function of MCM proteins at a distance from replication forks.
    EMBO Rep. 2003 Jan;4(1):26-30 PMID: 12524516
  62. Bacterial division: the fellowship of the ring.
    Curr Biol. 2003 Jan 8;13(1):R16-8 PMID: 12526758
  63. PCMA: fast and accurate multiple sequence alignment based on profile consistency.
    Bioinformatics. 2003 Feb 12;19(3):427-8 PMID: 12584134
  64. Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes.
    Genome Biol. 2003;4(2):R11 PMID: 12620121
  65. Cytokinesis in bacteria.
    Microbiol Mol Biol Rev. 2003 Mar;67(1):52-65, table of contents PMID: 12626683
  66. A giant virus in amoebae.
    Science. 2003 Mar 28;299(5615):2033 PMID: 12663918
  67. Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners.
    Mol Cell. 2003 Mar;11(3):571-5 PMID: 12667442
  68. The role of yeast DNA 3'-phosphatase Tpp1 and rad1/Rad10 endonuclease in processing spontaneous and induced base lesions.
    J Biol Chem. 2003 Aug 15;278(33):31434-43 PMID: 12783866
  69. The MRN complex: coordinating and mediating the response to broken chromosomes.
    EMBO Rep. 2003 Sep;4(9):844-9 PMID: 12949583
  70. Assembly dynamics of the bacterial cell division protein FTSZ: poised at the edge of stability.
    Annu Rev Microbiol. 2003;57:125-54 PMID: 14527275
  71. Evolution and classification of P-loop kinases and related proteins.
    J Mol Biol. 2003 Oct 31;333(4):781-815 PMID: 14568537
  72. Genome trees constructed using five different approaches suggest new major bacterial clades.
    BMC Evol Biol. 2001 Oct 20;1:8 PMID: 11734060
  73. A physical and functional interaction between Escherichia coli FtsK and topoisomerase IV.
    J Biol Chem. 2003 Nov 7;278(45):44639-44 PMID: 12939258
  74. Structural insights into single-stranded DNA binding and cleavage by F factor TraI.
    Structure. 2003 Nov;11(11):1369-79 PMID: 14604527
  75. Structure of the yeast Hst2 protein deacetylase in ternary complex with 2'-O-acetyl ADP ribose and histone peptide.
    Structure. 2003 Nov;11(11):1403-11 PMID: 14604530
  76. The outs and ins of bacterial type IV secretion substrates.
    Trends Microbiol. 2003 Nov;11(11):527-35 PMID: 14607070
  77. Structure and substrate binding properties of cobB, a Sir2 homolog protein deacetylase from Escherichia coli.
    J Mol Biol. 2004 Mar 26;337(3):731-41 PMID: 15019790
  78. Structural/functional homology between the bacterial and eukaryotic cytoskeletons.
    Curr Opin Cell Biol. 2004 Feb;16(1):24-31 PMID: 15037301
  79. Evolutionary history and higher order classification of AAA+ ATPases.
    J Struct Biol. 2004 Apr-May;146(1-2):11-31 PMID: 15037234
  80. Asymmetric activation of Xer site-specific recombination by FtsK.
    EMBO Rep. 2004 Apr;5(4):399-404 PMID: 15031713
  81. Recombination and chromosome segregation.
    Philos Trans R Soc Lond B Biol Sci. 2004 Jan 29;359(1441):61-9 PMID: 15065657
  82. Structure/function of the beta-barrel domain of F1-ATPase in the yeast Saccharomyces cerevisiae.
    J Biol Chem. 1999 Jun 4;274(23):16363-9 PMID: 10347195
  83. Dimerization of the Agrobacterium tumefaciens VirB4 ATPase and the effect of ATP-binding cassette mutations on the assembly and function of the T-DNA transporter.
    Mol Microbiol. 1999 Jun;32(6):1239-53 PMID: 10383764
  84. The crystal structure of rna1p: a new fold for a GTPase-activating protein.
    Mol Cell. 1999 Jun;3(6):781-91 PMID: 10394366
  85. Structural maintenance of chromosomes (SMC) proteins: conserved molecular properties for multiple biological functions.
    Eur J Biochem. 1999 Jul;263(1):6-13 PMID: 10429180
  86. Did DNA replication evolve twice independently?
    Nucleic Acids Res. 1999 Sep 1;27(17):3389-401 PMID: 10446225
  87. Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes.
    Science. 1999 Oct 15;286(5439):552-5 PMID: 10521354
  88. Decatenation of DNA circles by FtsK-dependent Xer site-specific recombination.
    EMBO J. 2003 Dec 1;22(23):6399-407 PMID: 14633998
  89. Recognition and processing of the origin of transfer DNA by conjugative relaxase TrwC.
    Nat Struct Biol. 2003 Dec;10(12):1002-10 PMID: 14625590
  90. Mitotic mechanics: the auroras come into view.
    Curr Opin Cell Biol. 2003 Dec;15(6):672-83 PMID: 14644191
  91. Chromosome segregation in Eubacteria.
    Curr Opin Microbiol. 2003 Dec;6(6):586-93 PMID: 14662354
  92. MlaA, a hexameric ATPase linked to the Mre11 complex in archaeal genomes.
    EMBO Rep. 2004 Jan;5(1):54-9 PMID: 14710187
  93. Cell division: burning the spindle at both ends.
    Nature. 2004 Jan 22;427(6972):300-1 PMID: 14737150
  94. Generation of the BfiI restriction endonuclease from the fusion of a DNA recognition domain to a non-specific nuclease from the phospholipase D superfamily.
    J Mol Biol. 2004 Feb 6;336(1):81-92 PMID: 14741205
  95. Association of Mre11p with double-strand break sites during yeast meiosis.
    Mol Cell. 2004 Feb 13;13(3):389-401 PMID: 14967146
  96. A bipolar DNA helicase gene, herA, clusters with rad50, mre11 and nurA genes in thermophilic archaea.
    Nucleic Acids Res. 2004;32(4):1439-47 PMID: 14990749
  97. Bacterial mitotic machineries.
    Cell. 2004 Feb 6;116(3):359-66 PMID: 15016371
  98. Crystal structure of the helicase domain from the replicative helicase-primase of bacteriophage T7.
    Cell. 1999 Oct 15;99(2):167-77 PMID: 10535735
  99. Importance of F1-ATPase residue alpha-Arg-376 for catalytic transition state stabilization.
    Biochemistry. 1999 Nov 23;38(47):15493-9 PMID: 10569931
  100. Evolution of gene fusions: horizontal transfer versus independent events.
    Genome Biol. 2002;3(5):research0024 PMID: 12049665
  101. NurA, a novel 5'-3' nuclease gene linked to rad50 and mre11 homologs of thermophilic Archaea.
    EMBO Rep. 2002 Jun;3(6):537-42 PMID: 12052775
  102. Bacterial conjugation: a two-step mechanism for DNA transport.
    Mol Microbiol. 2002 Jul;45(1):1-8 PMID: 12100543
  103. Ribonucleases from T2 family.
    Crit Rev Microbiol. 2002;28(2):79-122 PMID: 12109772
  104. Sequence analysis of bacteriophage T4 DNA packaging/terminase genes 16 and 17 reveals a common ATPase center in the large subunit of viral terminases.
    Nucleic Acids Res. 2002 Sep 15;30(18):4009-21 PMID: 12235385
  105. The many functions of SMC proteins in chromosome dynamics.
    Nat Rev Mol Cell Biol. 2002 Oct;3(10):767-78 PMID: 12360193
  106. Conjugative transposons: the tip of the iceberg.
    Mol Microbiol. 2002 Nov;46(3):601-10 PMID: 12410819
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
DOI
10.1093/nar/gkh828
Published
2004-00-00
Epub
2004-00-05
Pages
5260-79
Language
English
Region
England
NLM ID
0411011
PMCID
PMC521647
Subset
IM
External Links
PubMed source DOI: 10.1093/nar/gkh828 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2