Archaellum

From Wikipedia, the free encyclopedia
Jump to: navigation, search

An archaellum (plural: archaella) is a new name for the unique whip-like structure on the cell surface of many archaea (formerly called the archaeal flagellum). It can be rotated and is used to swim in liquid environments.

History[edit]

Archaea were first classified as a separate group of prokaryotes in 1977 by Carl Woese and George E. Fox based on the differences in the sequence of ribosomal RNA (16S rRNA) genes.[1][2] This domain possesses numerous fundamental traits distinct from both the bacterial and the eukaryotic domains. Many archaea possess a rotating motility structure that at first seemed to resemble the bacterial and eukaryotic flagella. The flagellum (Latin for whip) is a lash-like appendage that protrudes from the cell. In the last two decades, it was discovered that the archaeal flagella, although functionally similar to bacterial and eukaryotic flagella, structurally resemble bacterial type IV pili.[3][4][5] Bacterial type IV pili are surface structures that can be extended and retracted and are used to adhere to or move on solid surfaces.[6][7] To underline these differences, Ken Jarrell and Sonja-Verena Albers proposed to change the name of the archaeal flagellum to archaellum.[8]

Structure of the Archaellum[edit]

Electron micrographs of Sulfolobus acidocaldarius MW001 during normal growth. Indication of archaella (black arrows) and pili (white arrows). Negative staining with uranyl acetate.

Components of the Archaellum[edit]

Most proteins that make up the archaellum are encoded within one genetic locus. This genetic locus contains 7-13 genes which encode proteins involved in either assembly or function of the archaellum.[5] The genetic locus contains genes encoding archaellins (flaA and flaB) - the structural components of the filament - and core components (flaI, flaJ, flaH). The locus furthermore encodes accessory proteins (FlaG, FlaF, FlaX) and signaling components (FlaC, FlaD, FlaE). Genetic analysis in different archaea revealed that each of these components is essential for assembly of the archaellum.[9][10][11][12][13] Whereas most of the fla-associated genes are generally found in Euryarchaeota, one or more of these genes are absent from the fla-operon in Crenarchaeota. The prepilin peptidase (called PibD in crenarchaeota and FlaK in euryarchaeota) is essential for the maturation of the archaellins and is generally encoded elsewhere on the chromosome.[14]

Functional characterization has only been performed for FlaI, a Type II/IV secretion system ATPase super-family member [15] and PibD/FlaK.[14][16][17] FlaI forms a hexamer which hydrolyses ATP and most likely generates energy to assemble the archaellum. PibD cleaves the N-terminus of the archaellins before they can be assembled. FlaH and FlaJ are the two other core components that together with FlaI are proposed to form a platform on which the archaellum assembly occurs. The exact role of accessory proteins FlaF, FlaG, and FlaX is poorly understood. The genes coding for the signaling components such as flaC, flaD, flaE are only present in Euryarchaeota and interact with Chemotaxis proteins (e.g., CheY, CheD and CheC2) to sense environmental signals (such as exposure to light of specific wavelength, nutrient conditions etc.).[18]

Structure and assembly: Bacterial flagellum, Type IV pilus and Archaellum[edit]

In the 1980s, Dieter Oesterhelt’s laboratory showed for the first time that haloarchaea switch the rotation of their archaellum from clockwise to counterclockwise up on blue light pulses.[19][20] This led microbiologists to believe that the archaeal motility structure is not only functionally, but also structurally reminiscent of bacterial flagella. However, in contrast to flagellins, archaellins are produced as preproteins which are processed by a specific peptidase prior to assembly. Their signal peptide is homologous to class III signal peptides of type IV prepilins that are processed in Gram-negative bacteria by the peptidase PilD.[21] In crenarchaeota PibD and in euryarchaeota FlaK are PilD homologs, that are essential for the maturation of the archaellins. Furthermore, archaellins are N-glycosylated [22][23] which has not been described for bacterial flagellins, where O-linked glycosylation is evident. Two other components of the archaellum assembly system, namely, FlaI and FlaJ are homologous to components of type IV pili, PilB and PilC, respectively. Moreover, the structure of the archaellum filament resembles type IV pili as it has no central lumen [24] excluding the possibility that it might assembled in a similar fashion like bacterial flagella via a type III secretion system.[25] Additionally, it was demonstrated that the rotation of the archaellum is dependent on ATP concentration in the cell rather than PMF (proton motive force) as in the bacterial flagellum.[26]

Functional analogs[edit]

Archaellum versus Bacterial flagellum

Despite the limited amount of details presently available regarding the structure and assembly of archaellum, it has become increasingly evident from multiple studies that archaella play important roles in a variety of cellular processes in archaea. In spite of the structural dissimilarities with the bacterial flagellum, the main function thus far attributed for archaellum is swimming in liquid [13][27][28] and semi-solid surfaces.[29][30] Increasing biochemical and biophysical information has further consolidated the early observations of archaella mediated swimming in archaea. Like the bacterial flagellum,[31][32] the archaellum also mediates surface attachment and cell-cell communication.[33][34] However, unlike the bacterial flagellum archaellum has not shown to play a role in archaeal biofilm formation.[35] In archaeal biofilms, the only proposed function is thus far during the dispersal phase of biofilm when archaeal cells escape the community using their archaellum to further initiate the next round of biofilm formation.

See also[edit]

References[edit]

  1. ^ Woese, C.R. & Fox, G.E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A 74, 5088-90 (1977)
  2. ^ 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 U S A 87, 4576-9 (1990)
  3. ^ Peabody, C.R., Chung, Y.J., Yen, M.R., Vidal-Ingigliardi, D., Pugsley, A.P. & Saier, M.H., Jr. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149, 3051-72 (2003).
  4. ^ Pohlschroder, M., Ghosh, A., Tripepi, M. & Albers, S.V. Archaeal type IV pilus-like structures--evolutionarily conserved prokaryotic surface organelles. Curr Opin Microbiol 14, 357-63 (2011).
  5. ^ a b Ghosh, A. & Albers, S.V. Assembly and function of the archaeal flagellum. Biochem Soc Trans 39, 64-9 (2011).
  6. ^ Craig, L., Pique, M.E. & Tainer, J.A. Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2, 363-78 (2004).
  7. ^ Craig, L. & Li, J. Type IV pili: paradoxes in form and function. Current opinion in structural biology 18, 267-277 (2008).
  8. ^ Jarrell, K.F. & Albers, S.V. The archaellum: an old motility structure with a new name. Trends Microbiol 20, 307-12 (2012).
  9. ^ Patenge, N., Berendes, A., Engelhardt, H., Schuster, S.C. & Oesterhelt, D. The fla gene cluster is involved in the biogenesis of flagella in Halobacterium salinarum. Mol Microbiol 41, 653-63 (2001).
  10. ^ Thomas, N.A., Bardy, S.L. & Jarrell, K.F. The archaeal flagellum: a different kind of prokaryotic motility structure. FEMS Microbiol Rev 25, 147-74 (2001).
  11. ^ Thomas, N.A., Mueller, S., Klein, A. & Jarrell, K.F. Mutants in flaI and flaJ of the archaeon Methanococcus voltae are deficient in flagellum assembly. Mol Microbiol 46, 879-87 (2002).
  12. ^ Chaban, B., Ng, S., Kanbe, M., Saltzman, I., Nimmo, G., Aizawa, S.-I. & Jarrell, K. 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. Molecular microbiology 66, 596-609 (2007).
  13. ^ a b Lassak, K., Neiner, T., Ghosh, A., Klingl, A., Wirth, R. & Albers, S.V. Molecular analysis of the crenarchaeal flagellum. Mol Microbiol 83, 110-24 (2012).
  14. ^ a b Bardy, S.L. & Jarrell, K.F. Cleavage of preflagellins by an aspartic acid signal peptidase is essential for flagellation in the archaeon Methanococcus voltae. Mol Microbiol 50, 1339-47 (2003).
  15. ^ Ghosh, A., Hartung, S., van der Does, C., Tainer, J.A. & Albers, S.V. Archaeal flagellar ATPase motor shows ATP-dependent hexameric assembly and activity stimulation by specific lipid binding. Biochem J 437, 43-52 (2011).
  16. ^ Bardy, S.L. & Jarrell, K.F. FlaK of the archaeon Methanococcus maripaludis possesses preflagellin peptidase activity. FEMS Microbiol Lett 208, 53-9 (2002).
  17. ^ Szabó, Z., Adriana, O., Albers, S., Kissinger, J., Driessen, A. & Pohlschröder, M. Identification of diverse archaeal proteins with class III signal peptides cleaved by distinct archaeal prepilin peptidases. Journal of bacteriology 189, 772-778 (2007).
  18. ^ Schlesner, M., Miller, A., Streif, S., Staudinger, W.F., Muller, J., Scheffer, B., Siedler, F. & Oesterhelt, D. Identification of Archaea-specific chemotaxis proteins which interact with the flagellar apparatus. BMC Microbiol 9, 56 (2009).
  19. ^ Alam, M. & Oesterhelt, D. Morphology, function and isolation of halobacterial flagella. J Mol Biol 176, 459-75 (1984).
  20. ^ Marwan, W., Alam, M. & Oesterhelt, D. Rotation and switching of the flagellar motor assembly in Halobacterium halobium. J Bacteriol 173, 1971-7 (1991).
  21. ^ Faguy, D.M., Jarrell, K.F., Kuzio, J. & Kalmokoff, M.L. Molecular analysis of archael flagellins: similarity to the type IV pilin-transport superfamily widespread in bacteria. Can J Microbiol 40, 67-71 (1994).
  22. ^ Jarrell, K.F., Jones, G.M., Kandiba, L., Nair, D.B. & Eichler, J. S-layer glycoproteins and flagellins: reporters of archaeal posttranslational modifications. Archaea 2010 (2010).
  23. ^ Meyer, B.H., Zolghadr, B., Peyfoon, E., Pabst, M., Panico, M., Morris, H.R., Haslam, S.M., Messner, P., Schaffer, C., Dell, A. & Albers, S. Sulfoquinovose synthase - an important enzyme in the N-glycosylation pathway of Sulfolobus acidocaldarius. Mol Microbiol 82, 1150-1163 (2011).
  24. ^ Trachtenberg, S., Galkin, V.E. & Egelman, E.H. Refining the structure of the Halobacterium salinarum flagellar filament using the iterative helical real space reconstruction method: insights into polymorphism. J Mol Biol 346, 665-76 (2005).
  25. ^ Macnab, R.M. Genetics and biogenesis of bacterial flagella. Annu Rev Genet 26, 131-58 (1992).
  26. ^ Streif, S., Staudinger, W.F., Marwan, W. & Oesterhelt, D. Flagellar rotation in the archaeon Halobacterium salinarum depends on ATP. Journal of molecular biology 384, 1-8 (2008).
  27. ^ Alam, M., Claviez, M., Oesterhelt, D. & Kessel, M. Flagella and motility behaviour of square bacteria. EMBO J 3, 2899-903 (1984).
  28. ^ Herzog, B. & Wirth, R. Swimming behavior of selected species of Archaea. Appl Environ Microbiol 78, 1670-4 (2012).
  29. ^ Szabó, Z., Sani, M., Groeneveld, M., Zolghadr, B., Schelert, J., Albers, S.-V., Blum, P., Boekema, E. & Driessen, A. Flagellar motility and structure in the hyperthermoacidophilic archaeon Sulfolobus solfataricus. Journal of bacteriology 189, 4305-4309 (2007).
  30. ^ Jarrell, K.F., Bayley, D.P., Florian, V. & Klein, A. Isolation and characterization of insertional mutations in flagellin genes in the archaeon Methanococcus voltae. Mol Microbiol 20, 657-66 (1996).
  31. ^ Henrichsen, J. Bacterial surface translocation: a survey and a classification. Bacteriol Rev 36, 478-503 (1972).
  32. ^ Jarrell, K.F. & McBride, M.J. The surprisingly diverse ways that prokaryotes move. Nat Rev Microbiol 6, 466-76 (2008).
  33. ^ Näther, D.J., Rachel, R., Wanner, G. & Wirth, R. Flagella of Pyrococcus furiosus: multifunctional organelles, made for swimming, adhesion to various surfaces, and cell-cell contacts. Journal of bacteriology 188, 6915-6923 (2006).
  34. ^ Zolghadr, B., Klingl, A., Koerdt, A., Driessen, A.J., Rachel, R. & Albers, S.V. Appendage-mediated surface adherence of Sulfolobus solfataricus. J Bacteriol 192, 104-10 (2010).
  35. ^ Koerdt, A., Godeke, J., Berger, J., Thormann, K.M. & Albers, S.V. Crenarchaeal biofilm formation under extreme conditions. PLoS One 5, e14104 (2010).