1887

Abstract

has a highly condensed nucleoid which is implicated in its resistance to radiation. However, the mechanisms by which such compaction is achieved, and the proteins responsible, are still unknown. Here we have examined the genome of for the presence of proteins homologous to those that have been associated with nucleoid condensation. We found two different proteins homologous to the bacterial nucleoid-associated protein HU, one with an N-terminal and one with a C-terminal extension relative to the amino acid sequence of the HU found in . Sequence analysis revealed that one of these HU homologues represents a novel type with a high number of prolines in its C-terminal extension, whereas the other one has motifs similar to the N terminus of the HU homologue from the radio-resistant bacterium . The occurrence of two such HU homologue proteins with these two different terminal extensions in one organism appears to be unique among the Bacteria.

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2011-07-01
2020-01-24
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References

  1. Azam T. A., Ishihama A.. ( 1999;). Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J Biol Chem274:33105–33113 [CrossRef][PubMed]
    [Google Scholar]
  2. Bahloul A., Boubrik F., Rouviere-Yaniv J.. ( 2001;). Roles of Escherichia coli histone-like protein HU in DNA replication: HU-beta suppresses the thermosensitivity of dnaA46ts . Biochimie83:219–229 [CrossRef][PubMed]
    [Google Scholar]
  3. Barry C. E. III, Hayes S. F., Hackstadt T.. ( 1992;). Nucleoid condensation in Escherichia coli that express a chlamydial histone homolog. Science256:377–379 [CrossRef][PubMed]
    [Google Scholar]
  4. Bharath M. M., Ramesh S., Chandra N. R., Rao M. R.. ( 2002;). Identification of a 34 amino acid stretch within the C-terminus of histone H1 as the DNA-condensing domain by site-directed mutagenesis. Biochemistry41:7617–7627 [CrossRef][PubMed]
    [Google Scholar]
  5. Blasius M., Sommer S., Hübscher U.. ( 2008;). Deinococcus radiodurans: what belongs to the survival kit?. Crit Rev Biochem Mol Biol43:221–238 [CrossRef][PubMed]
    [Google Scholar]
  6. Christodoulou E., Vorgias C. E.. ( 2002;). The thermostability of DNA-binding protein HU from mesophilic, thermophilic, and extreme thermophilic bacteria. Extremophiles6:21–31 [CrossRef][PubMed]
    [Google Scholar]
  7. Cole C., Barber J. D., Barton G. J.. ( 2008;). The Jpred 3 secondary structure prediction server. Nucleic Acids Res36:Web Server issueW197–W201 [CrossRef][PubMed]
    [Google Scholar]
  8. Cuff J. A., Clamp M. E., Siddiqui A. S., Finlay M., Barton G. J.. ( 1998;). JPred: a consensus secondary structure prediction server. Bioinformatics14:892–893 [CrossRef][PubMed]
    [Google Scholar]
  9. Dame R. T., Goosen N.. ( 2002;). HU: promoting or counteracting DNA compaction?. FEBS Lett529:151–156 [CrossRef][PubMed]
    [Google Scholar]
  10. Dillon S. C., Dorman C. J.. ( 2010;). Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol8:185–195 [CrossRef][PubMed]
    [Google Scholar]
  11. Distel D. L., Morrill W., MacLaren-Toussaint N., Franks D., Waterbury J.. ( 2002;). Teredinibacter turnerae gen. nov., sp. nov., a dinitrogen-fixing, cellulolytic, endosymbiotic gamma-proteobacterium isolated from the gills of wood-boring molluscs (Bivalvia: Teredinidae). Int J Syst Evol Microbiol52:2261–2269 [CrossRef][PubMed]
    [Google Scholar]
  12. Englander J., Klein E., Brumfeld V., Sharma A. K., Doherty A. J., Minsky A.. ( 2004;). DNA toroids: framework for DNA repair in Deinococcus radiodurans and in germinating bacterial spores. J Bacteriol186:5973–5977 [CrossRef][PubMed]
    [Google Scholar]
  13. Felsenstein J.. ( 1989;). phylip – phylogeny inference package (version 3.2). Cladistics5:164–166
    [Google Scholar]
  14. Fuerst J. A.. ( 2005;). Intracellular compartmentation in planctomycetes. Annu Rev Microbiol59:299–328 [CrossRef][PubMed]
    [Google Scholar]
  15. Fuerst J. A., Webb R. I.. ( 1991;). Membrane-bounded nucleoid in the eubacterium Gemmata obscuriglobus . Proc Natl Acad Sci U S A88:8184–8188 [CrossRef][PubMed]
    [Google Scholar]
  16. Ghosh S., Grove A.. ( 2004;). Histone-like protein HU from Deinococcus radiodurans binds preferentially to four-way DNA junctions. J Mol Biol337:561–571 [CrossRef][PubMed]
    [Google Scholar]
  17. Ghosh S., Grove A.. ( 2006;). The Deinococcus radiodurans-encoded HU protein has two DNA-binding domains. Biochemistry45:1723–1733 [CrossRef][PubMed]
    [Google Scholar]
  18. Grove A.. ( 2010;). Functional evolution of bacterial histone-like HU proteins. Curr Issues Mol Biol13:1–12[PubMed]
    [Google Scholar]
  19. Grove A., Lim L.. ( 2001;). High-affinity DNA binding of HU protein from the hyperthermophile Thermotoga maritima . J Mol Biol311:491–502 [CrossRef][PubMed]
    [Google Scholar]
  20. Hansen J. C., Lu X., Ross E. D., Woody R. W.. ( 2006;). Intrinsic protein disorder, amino acid composition, and histone terminal domains. J Biol Chem281:1853–1856 [CrossRef][PubMed]
    [Google Scholar]
  21. Jobb G., von Haeseler A., Strimmer K.. ( 2004;). treefinder: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol4:18 [CrossRef][PubMed]
    [Google Scholar]
  22. Keane T. M., Creevey C. J., Pentony M. M., Naughton T. J., Mclnerney J. O.. ( 2006;). Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol6:29 [CrossRef][PubMed]
    [Google Scholar]
  23. Kumar S., Sardesai A. A., Basu D., Muniyappa K., Hasnain S. E.. ( 2010;). DNA clasping by mycobacterial HU: the C-terminal region of HupB mediates increased specificity of DNA binding. PLoS ONE5:e12551 [CrossRef][PubMed]
    [Google Scholar]
  24. Laine B., Kmiecik D., Sautiere P., Biserte G., Cohen-Solal M.. ( 1980;). Complete amino-acid sequences of DNA-binding proteins HU-1 and HU-2 from Escherichia coli . Eur J Biochem103:447–461 [CrossRef][PubMed]
    [Google Scholar]
  25. Lawrence J. G., Ochman H.. ( 1997;). Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol44:383–397 [CrossRef][PubMed]
    [Google Scholar]
  26. Lieber A., Leis A., Kushmaro A., Minsky A., Medalia O.. ( 2009;). Chromatin organization and radio resistance in the bacterium Gemmata obscuriglobus . J Bacteriol191:1439–1445 [CrossRef][PubMed]
    [Google Scholar]
  27. Lindsay M. R., Webb R. I., Strous M., Jetten M. S., Butler M. K., Forde R. J., Fuerst J. A.. ( 2001;). Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol175:413–429 [CrossRef][PubMed]
    [Google Scholar]
  28. Luger K., Mäder A. W., Richmond R. K., Sargent D. F., Richmond T. J.. ( 1997;). Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature389:251–260 [CrossRef][PubMed]
    [Google Scholar]
  29. Luijsterburg M. S., Noom M. C., Wuite G. J., Dame R. T.. ( 2006;). The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: a molecular perspective. J Struct Biol156:262–272 [CrossRef][PubMed]
    [Google Scholar]
  30. Luijsterburg M. S., White M. F., van Driel R., Dame R. T.. ( 2008;). The major architects of chromatin: architectural proteins in bacteria, archaea and eukaryotes. Crit Rev Biochem Mol Biol43:393–418 [CrossRef][PubMed]
    [Google Scholar]
  31. Maeder D. L., Bohm L.. ( 1991;). The C-domain in the H1 histone is structurally conserved. Biochim Biophys Acta1076:233–238 [CrossRef][PubMed]
    [Google Scholar]
  32. Medrano-Soto A., Moreno-Hagelsieb G., Vinuesa P., Christen J. A., Collado-Vides J.. ( 2004;). Successful lateral transfer requires codon usage compatibility between foreign genes and recipient genomes. Mol Biol Evol21:1884–1894 [CrossRef][PubMed]
    [Google Scholar]
  33. Mertens K., Lantsheer L., Samuel J. E.. ( 2005;). A minimal set of DNA repair genes is sufficient for survival of Coxiella burnetii under oxidative stress. Ann N Y Acad Sci1063:73–75 [CrossRef][PubMed]
    [Google Scholar]
  34. Mukherjee A., DiMario P. J., Grove A.. ( 2009;). Mycobacterium smegmatis histone-like protein Hlp is nucleoid associated. FEMS Microbiol Lett291:232–240 [CrossRef][PubMed]
    [Google Scholar]
  35. Prabhakar S., Annapurna P. S., Jain N. K., Dey A. B., Tyagi J. S., Prasad H. K.. ( 1998;). Identification of an immunogenic histone-like protein (HLPMt) of Mycobacterium tuberculosis . Tuber Lung Dis79:43–53 [CrossRef][PubMed]
    [Google Scholar]
  36. Remacha M., Kaul R., Sherburne R., Wenman W. M.. ( 1996;). Functional domains of chlamydial histone H1-like protein. Biochem J315:481–486[PubMed]
    [Google Scholar]
  37. Rouvière-Yaniv J., Gros F.. ( 1975;). Characterization of a novel, low-molecular-weight DNA-binding protein from Escherichia coli . Proc Natl Acad Sci U S A72:3428–3432 [CrossRef][PubMed]
    [Google Scholar]
  38. Rouvière-Yaniv J., Kjeldgaard N. O.. ( 1979;). Native Escherichia coli HU protein is a heterotypic dimer. FEBS Lett106:297–300 [CrossRef][PubMed]
    [Google Scholar]
  39. Rouvière-Yaniv J., Yaniv M., Germond J. E.. ( 1979;). E. coli DNA binding protein HU forms nucleosomelike structure with circular double-stranded DNA. Cell17:265–274[PubMed][CrossRef]
    [Google Scholar]
  40. Salerno P., Larsson J., Bucca G., Laing E., Smith C. P., Flärdh K.. ( 2009;). One of the two genes encoding nucleoid-associated HU proteins in Streptomyces coelicolor is developmentally regulated and specifically involved in spore maturation. J Bacteriol191:6489–6500 [CrossRef][PubMed]
    [Google Scholar]
  41. Santarella-Mellwig R., Franke J., Jaedicke A., Gorjanacz M., Bauer U., Budd A., Mattaj I. W., Devos D. P.. ( 2010;). The compartmentalized bacteria of the Planctomycetes-Verrucomicrobia-Chlamydiae superphylum have membrane coat-like proteins. PLoS Biol8:e1000281 [CrossRef][PubMed]
    [Google Scholar]
  42. Sarkar T., Vitoc I., Mukerji I., Hud N. V.. ( 2007;). Bacterial protein HU dictates the morphology of DNA condensates produced by crowding agents and polyamines. Nucleic Acids Res35:951–961 [CrossRef][PubMed]
    [Google Scholar]
  43. Shen C. H., Chiang Y. C., Hsu C. H., Yang M. K.. ( 2007;). Identification and characterization of two uvrA genes of Xanthomonas axonopodis pathovar citri . Mol Genet Genomics277:149–160 [CrossRef][PubMed]
    [Google Scholar]
  44. Shindo H., Furubayashi A., Shimizu M., Miyake M., Imamoto F.. ( 1992;). Preferential binding of E.coli histone-like protein HUα to negatively supercoiled DNA. Nucleic Acids Res20:1553–1558 [CrossRef][PubMed]
    [Google Scholar]
  45. Spurio R., Dürrenberger M., Falconi M., La Teana A., Pon C. L., Gualerzi C. O.. ( 1992;). Lethal overproduction of the Escherichia coli nucleoid protein H-NS: ultramicroscopic and molecular autopsy. Mol Gen Genet231:201–211[PubMed][CrossRef]
    [Google Scholar]
  46. Swinger K. K., Rice P. A.. ( 2004;). IHF and HU: flexible architects of bent DNA. Curr Opin Struct Biol14:28–35 [CrossRef][PubMed]
    [Google Scholar]
  47. Tanaka H., Goshima N., Kohno K., Kano Y., Imamoto F.. ( 1993;). Properties of DNA-binding of HU heterotypic and homotypic dimers from Escherichia coli . J Biochem113:568–572[PubMed]
    [Google Scholar]
  48. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G.. ( 1997;). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res25:4876–4882 [CrossRef][PubMed]
    [Google Scholar]
  49. van Noort J., Verbrugge S., Goosen N., Dekker C., Dame R. T.. ( 2004;). Dual architectural roles of HU: formation of flexible hinges and rigid filaments. Proc Natl Acad Sci U S A101:6969–6974 [CrossRef][PubMed]
    [Google Scholar]
  50. Wagner M., Horn M.. ( 2006;). The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotechnol17:241–249 [CrossRef][PubMed]
    [Google Scholar]
  51. White S. W., Appelt K., Wilson K. S., Tanaka I.. ( 1989;). A protein structural motif that bends DNA. Proteins5:281–288 [CrossRef][PubMed]
    [Google Scholar]
  52. Whiteford D. C., Klingelhoets J. J., Bambenek M. H., Dahl J. L.. ( 2011;). Deletion of the histone-like protein (Hlp) from Mycobacterium smegmatis results in increased sensitivity to UV exposure, freezing and isoniazid. Microbiology157:327–335 [CrossRef][PubMed]
    [Google Scholar]
  53. Yang M. K., Chou M. E., Yang Y. C.. ( 2001;). Molecular characterization and expression of the recX gene of Xanthomonas campestris pv. citri . Curr Microbiol42:257–263 [CrossRef][PubMed]
    [Google Scholar]
  54. Yang J. C., Madupu R., Durkin A. S., Ekborg N. A., Pedamallu C. S., Hostetler J. B., Radune D., Toms B. S., Henrissat B. et al. ( 2009;). The complete genome of Teredinibacter turnerae T7901: an intracellular endosymbiont of marine wood-boring bivalves (shipworms). PLoS ONE4:e6085 [CrossRef][PubMed]
    [Google Scholar]
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