1887

Abstract

Archaella are the swimming organelles in the Archaea. Recently, the first archaellum regulator in the Euryarchaeota, EarA, was identified in , one of the model organisms used for archaellum studies. EarA binds to 6 bp consensus sequences upstream of the promoter to activate the transcription of the operon, which encodes most of the proteins required for archaella synthesis. In this study, synteny analysis showed that homologues are widely distributed in the phylum of Euryarchaeota, with the notable exception of extreme halophiles. We classified Euryarchaeota species containing homologues into five classes based on the genomic location of the genes relative to and chemotaxis operons. EarA homologues from , and successfully complemented the function of EarA in a mutant, demonstrated by the restoration of FlaB2 expression in Western blot analysis and the appearance of archaella on the cell surface in complemented cells. Furthermore, the 6 bp consensus sequence was also found in the promoter region in these methanogens, indicating that the EarA homologues ly use a similar mechanism to activate transcription of the operons in their own hosts. Attempts to demonstrate complementation of the function of EarA in a mutant by the EarA homologue of were unsuccessful, despite the presence of a copy of the 6 bp consensus EarA-binding sequence upstream of the promoter in the genome.

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2017-05-01
2024-12-05
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References

  1. Jarrell KF, Ding Y, Nair DB, Siu S. Surface appendages of Archaea: structure, function, genetics and assembly. Life 2013; 3:86–117 [View Article][PubMed]
    [Google Scholar]
  2. Albers SV, Jarrell KF. The archaellum: how archaea swim. Front Microbiol 2015; 6:23 [View Article][PubMed]
    [Google Scholar]
  3. Jarrell KF, Albers SV. The archaellum: an old motility structure with a new name. Trends Microbiol 2012; 20:307–312 [View Article][PubMed]
    [Google Scholar]
  4. Ng SY, Chaban B, Jarrell KF. Archaeal flagella, bacterial flagella and type IV pili: a comparison of genes and posttranslational modifications. J Mol Microbiol Biotechnol 2006; 11:167–191 [View Article][PubMed]
    [Google Scholar]
  5. Albers SV, Jarrell KF. Archaellum moves archaea with distinction. Microbe Magazine 2015; 10:283–288 [View Article]
    [Google Scholar]
  6. Desmond E, Brochier-Armanet C, Gribaldo S. Phylogenomics of the archaeal flagellum: rare horizontal gene transfer in a unique motility structure. BMC Evol Biol 2007; 7:106 [View Article][PubMed]
    [Google Scholar]
  7. Bayley DP, Jarrell KF. Further evidence to suggest that archaeal flagella are related to bacterial type IV pili. J Mol Evol 1998; 46:370–373[PubMed]
    [Google Scholar]
  8. Peabody CR, Chung YJ, Yen MR, Vidal-Ingigliardi D, Pugsley AP et al. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 2003; 149:3051–3072 [View Article][PubMed]
    [Google Scholar]
  9. Reindl S, Ghosh A, Williams GJ, Lassak K, Neiner T et al. Insights into FlaI functions in archaeal motor assembly and motility from structures, conformations, and genetics. Mol Cell 2013; 49:1069–1082 [View Article][PubMed]
    [Google Scholar]
  10. Chaudhury P, Neiner T, D'Imprima E, Banerjee A, Reindl S et al. The nucleotide-dependent interaction of FlaH and FlaI is essential for assembly and function of the archaellum motor. Mol Microbiol 2016; 99:674–685 [View Article][PubMed]
    [Google Scholar]
  11. Meshcheryakov VA, Wolf M. Crystal structure of the flagellar accessory protein FlaH of Methanocaldococcus jannaschii suggests a regulatory role in archaeal flagellum assembly. Protein Sci 2016; 25:1147–1155 [View Article][PubMed]
    [Google Scholar]
  12. Banerjee A, Neiner T, Tripp P, Albers SV. Insights into subunit interactions in the Sulfolobus acidocaldarius archaellum cytoplasmic complex. FEBS J 2013; 280:6141–6149 [View Article][PubMed]
    [Google Scholar]
  13. Banerjee A, Tsai CL, Chaudhury P, Tripp P, Arvai AS et al. FlaF is a β-Sandwich protein that anchors the archaellum in the archaeal cell envelope by binding the S-Layer protein. Structure 2015; 23:863–872 [View Article][PubMed]
    [Google Scholar]
  14. Bardy SL, Jarrell KF. Cleavage of preflagellins by an aspartic acid signal peptidase is essential for flagellation in the archaeon Methanococcus voltae. Mol Microbiol 2003; 50:1339–1347 [View Article][PubMed]
    [Google Scholar]
  15. Bardy SL, Jarrell KF. FlaK of the archaeon Methanococcus maripaludis possesses preflagellin peptidase activity. FEMS Microbiol Lett 2002; 208:53–59 [View Article][PubMed]
    [Google Scholar]
  16. Albers SV, Szabó Z, Driessen AJ. Archaeal homolog of bacterial type IV prepilin signal peptidases with broad substrate specificity. J Bacteriol 2003; 185:3918–3925 [View Article][PubMed]
    [Google Scholar]
  17. Henche AL, van Wolferen M, Ghosh A, Albers SV. Dissection of key determinants of cleavage activity in signal peptidase III (SPaseIII) PibD. Extremophiles 2014; 18:905–913 [View Article][PubMed]
    [Google Scholar]
  18. Ng SY, Vandyke DJ, Chaban B, Wu J, Nosaka Y et al. Different minimal signal peptide lengths recognized by the archaeal prepilin-like peptidases FlaK and PibD. J Bacteriol 2009; 191:6732–6740 [View Article][PubMed]
    [Google Scholar]
  19. Szabó Z, Sani M, Groeneveld M, Zolghadr B, Schelert J et al. Flagellar motility and structure in the hyperthermoacidophilic archaeon Sulfolobus solfataricus. J Bacteriol 2007; 189:4305–4309 [View Article][PubMed]
    [Google Scholar]
  20. Reimann J, Lassak K, Khadouma S, Ettema TJ, Yang N et al. Regulation of archaella expression by the FHA and von Willebrand domain-containing proteins ArnA and ArnB in Sulfolobus acidocaldarius. Mol Microbiol 2012; 86:24–36 [View Article][PubMed]
    [Google Scholar]
  21. Hoffmann L, Schummer A, Reimann J, Haurat MF, Wilson AJ et al. Expanding the archaellum regulatory network - the eukaryotic protein kinases ArnC and ArnD influence motility of Sulfolobus acidocaldarius. Microbiologyopen 2017; 6:e00414 [View Article][PubMed]
    [Google Scholar]
  22. Reimann J, Esser D, Orell A, Amman F, Pham TK et al. Archaeal signal transduction: impact of protein phosphatase deletions on cell size, motility, and energy metabolism in Sulfolobus acidocaldarius. Mol Cell Proteomics 2013; 12:3908–3923 [View Article][PubMed]
    [Google Scholar]
  23. Lassak K, Peeters E, Wróbel S, Albers SV. The one-component system ArnR: a membrane-bound activator of the crenarchaeal archaellum. Mol Microbiol 2013; 88:125–139 [View Article][PubMed]
    [Google Scholar]
  24. Haurat MF, Figueiredo AS, Hoffmann L, Li L, Herr K et al. ArnS, a kinase involved in starvation-induced archaellum expression. Mol Microbiol 2017; 103:181–194 [View Article][PubMed]
    [Google Scholar]
  25. Orell A, Fröls S, Albers SV. Archaeal biofilms: the great unexplored. Annu Rev Microbiol 2013; 67:337–354 [View Article][PubMed]
    [Google Scholar]
  26. Orell A, Peeters E, Vassen V, Jachlewski S, Schalles S et al. Lrs14 transcriptional regulators influence biofilm formation and cell motility of Crenarchaea. ISME J 2013; 7:1886–1898 [View Article][PubMed]
    [Google Scholar]
  27. Ding Y, Nash J, Berezuk A, Khursigara CM, Langelaan DN et al. Identification of the first transcriptional activator of an archaellum operon in a euryarchaeon. Mol Microbiol 2016; 102:54–70 [View Article][PubMed]
    [Google Scholar]
  28. Chaban B, Ng SY, Kanbe M, Saltzman I, Nimmo G et al. Systematic deletion analyses of the fla genes in the flagella operon identify several genes essential for proper assembly and function of flagella in the archaeon, Methanococcus maripaludis. Mol Microbiol 2007; 66:596–609 [View Article][PubMed]
    [Google Scholar]
  29. Moore BC, Leigh JA. Markerless mutagenesis in Methanococcus maripaludis demonstrates roles for alanine dehydrogenase, alanine racemase, and alanine permease. J Bacteriol 2005; 187:972–979 [View Article][PubMed]
    [Google Scholar]
  30. Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS. Methanogens: reevaluation of a unique biological group. Microbiol Rev 1979; 43:260–296[PubMed]
    [Google Scholar]
  31. Lie TJ, Wood GE, Leigh JA. Regulation of nif expression in Methanococcus maripaludis: roles of the euryarchaeal repressor NrpR, 2-oxoglutarate, and two operators. J Biol Chem 2005; 280:5236–5241 [View Article][PubMed]
    [Google Scholar]
  32. Ferrante G, Richards JC, Sprott GD. Structures of polar lipids from the thermophilic, deep-sea archaeobacterium Methanococcus jannaschii. Biochem Cell Biol 1990; 68:274–283 [View Article][PubMed]
    [Google Scholar]
  33. Oberto J. SyntTax: a web server linking synteny to prokaryotic taxonomy. BMC Bioinformatics 2013; 14:4 [View Article][PubMed]
    [Google Scholar]
  34. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008; 36:W465–W469 [View Article][PubMed]
    [Google Scholar]
  35. Tumbula DL, Makula RA, Whitman WB. Transformation of Methanococcus maripaludis and identification of a Pst I-like restriction system. FEMS Microbiol Lett 1994; 121:309–314 [View Article]
    [Google Scholar]
  36. Ng SY, Zolghadr B, Driessen AJ, Albers SV, Jarrell KF. Cell surface structures of archaea. J Bacteriol 2008; 190:6039–6047 [View Article][PubMed]
    [Google Scholar]
  37. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article][PubMed]
    [Google Scholar]
  38. Nagahisa K, Ezaki S, Fujiwara S, Imanaka T, Takagi M. Sequence and transcriptional studies of five clustered flagellin genes from hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1. FEMS Microbiol Lett 1999; 178:183–190 [View Article][PubMed]
    [Google Scholar]
  39. Näther-Schindler DJ, Schopf S, Bellack A, Rachel R, Wirth R. Pyrococcus furiosus flagella: biochemical and transcriptional analyses identify the newly detected flaB0 gene to encode the major flagellin. Front Microbiol 2014; 5:695 [View Article][PubMed]
    [Google Scholar]
  40. Del Rosario RC, Diener F, Diener M, Oesterhelt D. The steady-state phase distribution of the motor switch complex model of Halobacterium salinarum. Math Biosci 2009; 222:117–126 [View Article][PubMed]
    [Google Scholar]
  41. Schlesner M, Miller A, Streif S, Staudinger WF, Müller J et al. Identification of Archaea-specific chemotaxis proteins which interact with the flagellar apparatus. BMC Microbiol 2009; 9:56 [View Article][PubMed]
    [Google Scholar]
  42. Kinosita Y, Uchida N, Nakane D, Nishizaka T. Direct observation of rotation and steps of the archaellum in the swimming halophilic archaeon Halobacterium salinarum. Nat Microbiol 2016; 1:16148 [View Article][PubMed]
    [Google Scholar]
  43. Streif S, Staudinger WF, Marwan W, Oesterhelt D. Flagellar rotation in the archaeon Halobacterium salinarum depends on ATP. J Mol Biol 2008; 384:1–8 [View Article][PubMed]
    [Google Scholar]
  44. Patenge N, Berendes A, Engelhardt H, Schuster SC, Oesterhelt D. The fla gene cluster is involved in the biogenesis of flagella in Halobacterium salinarum. Mol Microbiol 2001; 41:653–663 [View Article][PubMed]
    [Google Scholar]
  45. Alam M, Oesterhelt D. Morphology, function and isolation of halobacterial flagella. J Mol Biol 1984; 176:459–475 [View Article][PubMed]
    [Google Scholar]
  46. Syutkin AS, Pyatibratov MG, Galzitskaya OV, Rodríguez-Valera F, Fedorov OV. Haloarcula marismortui archaellin genes as ecoparalogs. Extremophiles 2014; 18:341–349 [View Article][PubMed]
    [Google Scholar]
  47. Beznosov S, Pyatibratov M, Veluri P, Mitra S, Fedorov O. A way to identify archaellins in Halobacterium salinarum archaella by FLAG-tagging. Cent Eur J Biol 2013; 8:828–834 [View Article]
    [Google Scholar]
  48. Pyatibratov MG, Beznosov SN, Rachel R, Tiktopulo EI, Surin AK et al. Alternative flagellar filament types in the haloarchaeon Haloarcula marismortui. Can J Microbiol 2008; 54:835–844 [View Article][PubMed]
    [Google Scholar]
  49. Esquivel RN, Pohlschroder M. A conserved type IV pilin signal peptide H-domain is critical for the post-translational regulation of flagella-dependent motility. Mol Microbiol 2014; 93:494–504 [View Article][PubMed]
    [Google Scholar]
  50. Tripepi M, Imam S, Pohlschröder M. Haloferax volcanii flagella are required for motility but are not involved in PibD-dependent surface adhesion. J Bacteriol 2010; 192:3093–3102 [View Article][PubMed]
    [Google Scholar]
  51. Legerme G, Yang E, Esquivel RN, Kiljunen S, Savilahti H et al. Screening of a Haloferax volcanii transposon library reveals novel motility and adhesion mutants. Life (Basel) 2016; 6:E41 [View Article][PubMed]
    [Google Scholar]
  52. Esquivel RN, Schulze S, Xu R, Hippler M, Pohlschroder M. Identification of Haloferax volcanii pilin N-glycans with diverse roles in pilus biosynthesis, adhesion, and microcolony formation. J Biol Chem 2016; 291:10602–10614 [View Article][PubMed]
    [Google Scholar]
  53. Tripepi M, You J, Temel S, Önder Ö, Brisson D et al. N-glycosylation of Haloferax volcanii flagellins requires known Agl proteins and is essential for biosynthesis of stable flagella. J Bacteriol 2012; 194:4876–4887 [View Article][PubMed]
    [Google Scholar]
  54. Kim YH, Park KH, Kim SY, Ji ES, Kim JY et al. Identification of trimethylation at C-terminal lysine of pilin in the cyanobacterium synechocystis PCC 6803. Biochem Biophys Res Commun 2011; 404:587–592 [View Article][PubMed]
    [Google Scholar]
  55. Burnens AP, Stanley J, Sack R, Hunziker P, Brodard I et al. The flagellin N-methylase gene fliB and an adjacent serovar-specific IS200 element in Salmonella typhimurium. Microbiology 1997; 143:1539–1547 [View Article][PubMed]
    [Google Scholar]
  56. Briegel A, Ortega DR, Huang AN, Oikonomou CM, Gunsalus RP et al. Structural conservation of chemotaxis machinery across Archaea and Bacteria. Environ Microbiol Rep 2015; 7:414–419 [View Article][PubMed]
    [Google Scholar]
  57. Helmann JD. Alternative sigma factors and the regulation of flagellar gene expression. Mol Microbiol 1991; 5:2875–2882 [View Article][PubMed]
    [Google Scholar]
  58. Werner F. Molecular mechanisms of transcription elongation in Archaea. Chem Rev 2013; 113:8331–8349 [View Article][PubMed]
    [Google Scholar]
  59. Burton SP, Burton ZF. The σ enigma: bacterial σ factors, archaeal TFB and eukaryotic TFIIB are homologs. Transcription 2014; 5:e967599 [View Article][PubMed]
    [Google Scholar]
  60. Robb FT, Maeder DL, Brown JR, Diruggiero J, Stump MD et al. Genomic sequence of hyperthermophile, Pyrococcus furiosus: implications for physiology and enzymology. Methods Enzymol 2001; 330:134–157[PubMed] [CrossRef]
    [Google Scholar]
  61. Fiala G, Stetter KO. Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C. Arch Microbiol 1986; 145:56–61 [View Article]
    [Google Scholar]
  62. Jones WJ, Leigh JA, Mayer F, Woese CR, Wolfe RS. Methanococcus jannaschii sp. nov., an extremely thermophilic methanogen from a submarine hydrothermal vent. Arch Microbiol 1983; 136:254–261 [View Article]
    [Google Scholar]
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