1887

Abstract

In this study, the effects of growth conditions on archaellation in were examined. Cells were grown in a variety of media, including complex, minimal and with formate as the electron donor, with different nitrogen sources, varied salinities and at a variety of growth temperatures. Of the conditions tested, Western blot results showed that major archaellin FlaB2 levels only varied detectably as a result of growth temperature. Whilst the amount of FlaB2 was similar for cells grown at < 35 °C, protein levels decreased at 38 °C and were barely detectable at 42 °C. Quantitative reverse transcription PCR experiments demonstrated that the transcript levels were almost undetectable at 42 °C. Electron microscopy confirmed that the FlaB2 levels detected by Western blots corresponded to the state of archaellation, with cells grown at 42 °C being mostly non-archaellated. Unexpectedly, a lower apparent molecular mass for FlaB2 was observed in Western blots of cells grown at temperatures >38 °C, suggestive of a truncation in the attached -linked tetrasaccharide at higher growth temperatures. MS analysis of archaella isolated from cells grown at 40 °C confirmed that FlaB2 was now decorated with a trisaccharide in which the third sugar was also lacking the attached threonine and acetamidino modifications found in the WT glycan.

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2016-02-01
2024-03-28
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References

  1. Alam M., Oesterhelt D. 1984; Morphology, function and isolation of halobacterial flagella. J Mol Biol 176:459–475 [View Article][PubMed]
    [Google Scholar]
  2. Albers S. V., Jarrell K. F. 2015; The archaellum: how Archaea swim. Front Microbiol 6:23 [View Article][PubMed]
    [Google Scholar]
  3. Balch W. E., Fox G. E., Magrum L. J., Woese C. R., Wolfe R. S. 1979; Methanogens: reevaluation of a unique biological group. Microbiol Rev 43:260–296[PubMed]
    [Google Scholar]
  4. Banerjee A., Ghosh A., Mills D. J., Kahnt J., Vonck J., Albers S. V. 2012; FlaX, a unique component of the crenarchaeal archaellum, forms oligomeric ring-shaped structures and interacts with the motor ATPase FlaI. J Biol Chem 287:43322–43330 [View Article][PubMed]
    [Google Scholar]
  5. Banerjee A., Tsai C. L., Chaudhury P., Tripp P., Arvai A. S., Ishida J. P., Tainer J. A., Albers S. V. 2015; FlaF is a β-sandwich protein that anchors the archaellum in the archaeal cell envelope by binding the S-layer protein. Structure 23:863–872 [View Article][PubMed]
    [Google Scholar]
  6. Bardy S. L., Mori T., Komoriya K., Aizawa S., Jarrell K. F. 2002; Identification and localization of flagellins FlaA and FlaB3 within flagella of Methanococcus voltae . J Bacteriol 184:5223–5233 [View Article][PubMed]
    [Google Scholar]
  7. Bayley D. P., Jarrell K. F. 1998; Further evidence to suggest that archaeal flagella are related to bacterial type IV pili. J Mol Evol 46:370–373[PubMed]
    [Google Scholar]
  8. Bellack A., Huber H., Rachel R., Wanner G., Wirth R. 2011; Methanocaldococcus villosus sp. nov., a heavily flagellated archaeon that adheres to surfaces and forms cell-cell contacts. Int J Syst Evol Microbiol 61:1239–1245 [View Article][PubMed]
    [Google Scholar]
  9. Bradley D. E. 1980; A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can J Microbiol 26:146–154 [View Article][PubMed]
    [Google Scholar]
  10. Burrows L. L. 2012; Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu Rev Microbiol 66:493–520 [View Article][PubMed]
    [Google Scholar]
  11. Chaban B., Voisin S., Kelly J., Logan S. M., Jarrell K. F. 2006; Identification of genes involved in the biosynthesis and attachment of Methanococcus voltae N-linked glycans: insight into N-linked glycosylation pathways in Archaea. Mol Microbiol 61:259–268 [View Article][PubMed]
    [Google Scholar]
  12. Chaban B., Ng S. Y., Kanbe M., Saltzman I., Nimmo G., Aizawa S., Jarrell K. F. 2007; 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 66:596–609 [View Article][PubMed]
    [Google Scholar]
  13. Costa K. C., Yoon S. H., Pan M., Burn J. A., Baliga N. S., Leigh J. A. 2013; Effects of H2 and formate on growth yield and regulation of methanogenesis in Methanococcus maripaludis . J Bacteriol 195:1456–1462 [View Article][PubMed]
    [Google Scholar]
  14. Ding Y., Jones G. M., Uchida K., Aizawa S., Robotham A., Logan S. M., Kelly J., Jarrell K. F. 2013; Identification of genes involved in the biosynthesis of the third and fourth sugars of the Methanococcus maripaludis archaellin N-linked tetrasaccharide. J Bacteriol 195:4094–4104 [View Article][PubMed]
    [Google Scholar]
  15. Ding Y., Uchida K., Aizawa S., Murphy K., Berezuk A., Khursigara C. M., Chong J. P. J., Jarrell K. F. 2015; Effects of N-glycosylation site removal in archaellins on the assembly and function of archaella in Methanococcus maripaludis . PLoS One 10:e0116402 [View Article][PubMed]
    [Google Scholar]
  16. Eichler J., Jarrell K., Albers S. 2013; A proposal for the naming of N-glycosylation pathway components in archaea. Glycobiology 23:620–621 [View Article]
    [Google Scholar]
  17. Esquivel R. N., Pohlschroder M. 2014; A conserved type IV pilin signal peptide H-domain is critical for the post-translational regulation of flagella-dependent motility. Mol Microbiol 93:494–504 [View Article][PubMed]
    [Google Scholar]
  18. Faguy D. M., Koval S. F., Jarrell K. F. 1993; Effect of changes in mineral composition and growth temperature on filament length and flagellation in the archaeon Methanospirillum hungatei . Arch Microbiol 159:512–520 [View Article]
    [Google Scholar]
  19. Faguy D. M., Bayley D. P., Kostyukova A. S., Thomas N. A., Jarrell K. F. 1996; Isolation and characterization of flagella and flagellin proteins from the thermoacidophilic archaea Thermoplasma volcanium and Sulfolobus shibatae . J Bacteriol 178:902–905[PubMed]
    [Google Scholar]
  20. Ghosh A., Hartung S., van der Does C., Tainer J. A., Albers S. V. 2011; Archaeal flagellar ATPase motor shows ATP-dependent hexameric assembly and activity stimulation by specific lipid binding. Biochem J 437:43–52 [View Article][PubMed]
    [Google Scholar]
  21. Giltner C. L., Nguyen Y., Burrows L. L. 2012; Type IV pilin proteins: versatile molecular modules. Microbiol Mol Biol Rev 76:740–772 [View Article][PubMed]
    [Google Scholar]
  22. Henche A. L., Ghosh A., Yu X., Jeske T., Egelman E., Albers S. V. 2012; Structure and function of the adhesive type IV pilus of Sulfolobus acidocaldarius . Environ Microbiol 14:3188–3202 [View Article][PubMed]
    [Google Scholar]
  23. Hendrickson E. L., Haydock A. K., Moore B. C., Whitman W. B., Leigh J. A. 2007; Functionally distinct genes regulated by hydrogen limitation and growth rate in methanogenic Archaea. Proc Natl Acad Sci U S A 104:8930–8934 [View Article][PubMed]
    [Google Scholar]
  24. Hendrickson E. L., Liu Y., Rosas-Sandoval G., Porat I., Söll D., Whitman W. B., Leigh J. A. 2008; Global responses of Methanococcus maripaludis to specific nutrient limitations and growth rate. J Bacteriol 190:2198–2205 [View Article][PubMed]
    [Google Scholar]
  25. Jarrell K. F., Albers S. V. 2012; The archaellum: an old motility structure with a new name. Trends Microbiol 20:307–312 [View Article][PubMed]
    [Google Scholar]
  26. Jarrell K. F., Stark M., Nair D. B., Chong J. P. J. 2011; Flagella and pili are both necessary for efficient attachment of Methanococcus maripaludis to surfaces. FEMS Microbiol Lett 319:44–50 [View Article][PubMed]
    [Google Scholar]
  27. Jarrell K. F., Ding Y., Nair D. B., Siu S. 2013; Surface appendages of archaea: structure, function, genetics and assembly. Life (Basel) 3:86–117[PubMed]
    [Google Scholar]
  28. Jarrell K. F., Ding Y., Meyer B. H., Albers S. V., Kaminski L., Eichler J. 2014; N-linked glycosylation in Archaea: a structural, functional, and genetic analysis. Microbiol Mol Biol Rev 78:304–341 [View Article][PubMed]
    [Google Scholar]
  29. Jones G. M., Wu J., Ding Y., Uchida K., Aizawa S., Robotham A., Logan S. M., Kelly J., Jarrell K. F. 2012; Identification of genes involved in the acetamidino group modification of the flagellin N-linked glycan of Methanococcus maripaludis . J Bacteriol 194:2693–2702 [View Article][PubMed]
    [Google Scholar]
  30. Kalmokoff M. L., Jarrell K. F. 1991; Cloning and sequencing of a multigene family encoding the flagellins of Methanococcus voltae . J Bacteriol 173:7113–7125[PubMed]
    [Google Scholar]
  31. Kaminski L., Guan Z., Yurist-Doutsch S., Eichler J. 2013; Two distinct N-glycosylation pathways process the Haloferax volcanii S-layer glycoprotein upon changes in environmental salinity. MBio 4:e00716–e00713 [View Article][PubMed]
    [Google Scholar]
  32. Kelly J., Logan S. M., Jarrell K. F., VanDyke D. J., Vinogradov E. 2009; A novel N-linked flagellar glycan from Methanococcus maripaludis . Carbohydr Res 344:648–653 [View Article][PubMed]
    [Google Scholar]
  33. Laemmli U. K. 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [View Article][PubMed]
    [Google Scholar]
  34. Lassak K., Ghosh A., Albers S. V. 2012a; Diversity, assembly and regulation of archaeal type IV pili-like and non-type-IV pili-like surface structures. Res Microbiol 163:630–644 [View Article][PubMed]
    [Google Scholar]
  35. Lassak K., Neiner T., Ghosh A., Klingl A., Wirth R., Albers S. V. 2012b; Molecular analysis of the crenarchaeal flagellum. Mol Microbiol 83:110–124 [View Article][PubMed]
    [Google Scholar]
  36. Lassak K., Peeters E., Wróbel S., Albers S. V. 2013; The one-component system ArnR: a membrane-bound activator of the crenarchaeal archaellum. Mol Microbiol 88:125–139 [View Article][PubMed]
    [Google Scholar]
  37. Leigh J. A., Albers S. V., Atomi H., Allers T. 2011; Model organisms for genetics in the domain Archaea: methanogens, halophiles, Thermococcales and Sulfolobales . FEMS Microbiol Rev 35:577–608 [View Article][PubMed]
    [Google Scholar]
  38. Lie T. J., Leigh J. A. 2002; Regulatory response of Methanococcus maripaludis to alanine, an intermediate nitrogen source. J Bacteriol 184:5301–5306 [View Article][PubMed]
    [Google Scholar]
  39. Lie T. J., Leigh J. A. 2003; A novel repressor of nif and glnA expression in the methanogenic archaeon Methanococcus maripaludis . Mol Microbiol 47:235–246 [View Article][PubMed]
    [Google Scholar]
  40. Marwan W., Alam M., Oesterhelt D. 1991; Rotation and switching of the flagellar motor assembly in Halobacterium halobium . J Bacteriol 173:1971–1977[PubMed]
    [Google Scholar]
  41. Meyer B. H., Peyfoon E., Dietrich C., Hitchen P., Panico M., Morris H. R., Dell A., Albers S. V. 2013; Agl16, a thermophilic glycosyltransferase mediating the last step of N-glycan biosynthesis in the thermoacidophilic crenarchaeon Sulfolobus acidocaldarius . J Bacteriol 195:2177–2186 [View Article][PubMed]
    [Google Scholar]
  42. Moore B. C., Leigh J. A. 2005; Markerless mutagenesis in Methanococcus maripaludis demonstrates roles for alanine dehydrogenase, alanine racemase, and alanine permease. J Bacteriol 187:972–979 [View Article][PubMed]
    [Google Scholar]
  43. Mukhopadhyay B., Johnson E. F., Wolfe R. S. 2000; A novel pH2 control on the expression of flagella in the hyperthermophilic strictly hydrogenotrophic methanarchaeaon Methanococcus jannaschii . Proc Natl Acad Sci U S A 97:11522–11527 [View Article][PubMed]
    [Google Scholar]
  44. Näther D. J., Rachel R., Wanner G., Wirth R. 2006; Flagella of Pyrococcus furiosus: multifunctional organelles, made for swimming, adhesion to various surfaces, and cell-cell contacts. J Bacteriol 188:6915–6923 [View Article][PubMed]
    [Google Scholar]
  45. Ng S. Y., Chaban B., Jarrell K. F. 2006; Archaeal flagella, bacterial flagella and type IV pili: a comparison of genes and posttranslational modifications. J Mol Microbiol Biotechnol 11:167–191 [View Article][PubMed]
    [Google Scholar]
  46. Ng S. Y. M., Wu J., Nair D. B., Logan S. M., Robotham A., Tessier L., Kelly J. F., Uchida K., Aizawa S., Jarrell K. F. 2011; Genetic and mass spectrometry analyses of the unusual type IV-like pili of the archaeon Methanococcus maripaludis . J Bacteriol 193:804–814 [View Article][PubMed]
    [Google Scholar]
  47. Orell A., Peeters E., Vassen V., Jachlewski S., Schalles S., Siebers B., Albers S. V. 2013; Lrs14 transcriptional regulators influence biofilm formation and cell motility of Crenarchaea. ISME J 7:1886–1898 [View Article][PubMed]
    [Google Scholar]
  48. Peabody C. R., Chung Y. J., Yen M. R., Vidal-Ingigliardi D., Pugsley A. P., Saier M. H. Jr 2003; Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:3051–3072 [View Article][PubMed]
    [Google Scholar]
  49. Pohlschröder M., Giménez M. I., Jarrell K. F. 2005; Protein transport in Archaea: Sec and twin arginine translocation pathways. Curr Opin Microbiol 8:713–719 [View Article][PubMed]
    [Google Scholar]
  50. Pohlschroder M., Ghosh A., Tripepi M., Albers S. V. 2011; Archaeal type IV pilus-like structures – evolutionarily conserved prokaryotic surface organelles. Curr Opin Microbiol 14:357–363 [View Article][PubMed]
    [Google Scholar]
  51. Reimann J., Lassak K., Khadouma S., Ettema T. J., Yang N., Driessen A. J., Klingl A., Albers S. V. 2012; Regulation of archaella expression by the FHA and von Willebrand domain-containing proteins ArnA and ArnB in Sulfolobus acidocaldarius . Mol Microbiol 86:24–36 [View Article][PubMed]
    [Google Scholar]
  52. Reindl S., Ghosh A., Williams G. J., Lassak K., Neiner T., Henche A. L., Albers S. V., Tainer J. A. 2013; Insights into FlaI functions in archaeal motor assembly and motility from structures, conformations, and genetics. Mol Cell 49:1069–1082 [View Article][PubMed]
    [Google Scholar]
  53. Schopf S., Wanner G., Rachel R., Wirth R. 2008; An archaeal bi-species biofilm formed by Pyrococcus furiosus and Methanopyrus kandleri . Arch Microbiol 190:371–377 [View Article][PubMed]
    [Google Scholar]
  54. Shahapure R., Driessen R. P., Haurat M. F., Albers S. V., Dame R. T. 2014; The archaellum: a rotating type IV pilus. Mol Microbiol 91:716–723 [View Article][PubMed]
    [Google Scholar]
  55. Shimoyama T., Kato S., Ishii S., Watanabe K. 2009; Flagellum mediates symbiosis. Science 323:1574 [View Article][PubMed]
    [Google Scholar]
  56. Siu S., Robotham A., Logan S. M., Kelly J. F., Uchida K., Aizawa S., Jarrell K. F. 2015; Evidence that biosynthesis of the second and third sugars of the archaellin tetrasaccharide in the archaeon Methanococcus maripaludis occurs by the same pathway used by Pseudomonas aeruginosa to make a di-N-acetylated sugar. J Bacteriol 197:1668–1680 [View Article][PubMed]
    [Google Scholar]
  57. Szabó Z., Sani M., Groeneveld M., Zolghadr B., Schelert J., Albers S. V., Blum P., Boekema E. J., Driessen A. J. M. 2007; Flagellar motility and structure in the hyperthermoacidophilic archaeon Sulfolobus solfataricus . J Bacteriol 189:4305–4309 [View Article][PubMed]
    [Google Scholar]
  58. Thomas N. A., Jarrell K. F. 2001; Characterization of flagellum gene families of methanogenic archaea and localization of novel flagellum accessory proteins. J Bacteriol 183:7154–7164 [View Article][PubMed]
    [Google Scholar]
  59. Towbin H., Staehelin T., Gordon J. 1979; Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76:4350–4354 [View Article][PubMed]
    [Google Scholar]
  60. Trachtenberg S., Cohen-Krausz S. 2006; The archaeabacterial flagellar filament: a bacterial propeller with a pilus-like structure. J Mol Microbiol Biotechnol 11:208–220 [View Article][PubMed]
    [Google Scholar]
  61. Tripepi M., You J., Temel S., Önder Ö., Brisson D., Pohlschröder M. 2012; N-glycosylation of Haloferax volcanii flagellins requires known Agl proteins and is essential for biosynthesis of stable flagella. J Bacteriol 194:4876–4887 [View Article][PubMed]
    [Google Scholar]
  62. Tumbula D. L., Makula R. A., Whitman W. B. 1994; Transformation of Methanococcus maripaludis and identification of a PstI-like restriction system. FEMS Microbiol Lett 121:309–314 [View Article]
    [Google Scholar]
  63. VanDyke D. J., Wu J., Logan S. M., Kelly J. F., Mizuno S., Aizawa S., Jarrell K. F. 2009; Identification of genes involved in the assembly and attachment of a novel flagellin N-linked tetrasaccharide important for motility in the archaeon Methanococcus maripaludis . Mol Microbiol 72:633–644 [View Article][PubMed]
    [Google Scholar]
  64. Voisin S., Houliston R. S., Kelly J., Brisson J. R., Watson D., Bardy S. L., Jarrell K. F., Logan S. M. 2005; Identification and characterization of the unique N-linked glycan common to the flagellins and S-layer glycoprotein of Methanococcus voltae . J Biol Chem 280:16586–16593 [View Article][PubMed]
    [Google Scholar]
  65. Weiner A., Schopf S., Wanner G., Probst A., Wirth R. 2012; Positive, neutral and negative interactions in cocultures between Pyrococcus furiosus and different methanogenic archaea. Microbiol Insights 5:1–10
    [Google Scholar]
  66. Whitman W. B., Jeanthon C. 2006; Methanococcales. In The Prokaryotes vol 3 pp 257–273 Edited by Dworkin M., Falkow S., Rosenberg E., Schleifer K. H., Stackebrandt E. New York: Springer; [CrossRef]
    [Google Scholar]
  67. Wieland F., Paul G., Sumper M. 1985; Halobacterial flagellins are sulfated glycoproteins. J Biol Chem 260:15180–15185[PubMed]
    [Google Scholar]
  68. Xia Q., Wang T., Hendrickson E. L., Lie T. J., Hackett M., Leigh J. A. 2009; Quantitative proteomics of nutrient limitation in the hydrogenotrophic methanogen Methanococcus maripaludis . BMC Microbiol 9:149 [View Article][PubMed]
    [Google Scholar]
  69. Zolghadr B., Klingl A., Koerdt A., Driessen A. J., Rachel R., Albers S. V. 2010; Appendage-mediated surface adherence of Sulfolobus solfataricus . J Bacteriol 192:104–110 [View Article][PubMed]
    [Google Scholar]
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