Biology:Archaellum

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An archaellum (plural: archaella, formerly archaeal flagellum) is a unique whip-like structure on the cell surface of many archaea. The name was proposed in 2012 following studies that showed it to be evolutionarily and structurally different from the bacterial and eukaryotic flagella. The archaellum is functionally the same – it can be rotated and is used to swim in liquid environments. The archaellum was found to be structurally similar to the type IV pilus.[1][2]

History

In 1977, archaea were first classified as a separate group of prokaryotes in the three-domain system of Carl Woese and George E. Fox, based on the differences in the sequence of ribosomal RNA (16S rRNA) genes.[3][4] 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.[5][6][7] Bacterial type IV pili are surface structures that can be extended and retracted to give a twitching motility and are used to adhere to or move on solid surfaces; their "tail" proteins are called pilins.[8][9] To underline these differences, Ken Jarrell and Sonja-Verena Albers proposed to change the name of the archaeal flagellum to archaellum.[10]

Structure

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

Components

2015 model of the crenarchaeal archaellum.[1]

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.[7] The genetic locus contains genes encoding archaellins (flaA and flaB)[lower-alpha 1] - the structural components of the filament - and motor components (flaI, flaJ, flaH). The locus furthermore encodes other accessory proteins (flaG, flaF, flaC, flaD, flaE, and flaX). FlaX is only found in Crenarchaeota and FlaCDE (which can exist as individual proteins or as fusion proteins) in Euryarchaeotes. FlaX and FlaCDE are thought to have similar functions, and an unknown protein is also thought to fulfil the same function in Thaumarchaeota.

The archaellum operon used to be historically known as fla (from "flagellum"), but in order to avoid confusion with the bacterial flagellum and to be consistent with the remaining nomenclature (archaellum, archaellins), it has been recently proposed to be renamed to arl (archaellin-related genes) [11]. Consequently, the name of the genes is also differen (e.g., flaJ is now arlJ). Therefore, in the specialised literature both nomenclatures can be found, with the arl nomenclature being increasingly more used since 2018.

Genetic analysis in different archaea revealed that each of these components is essential for assembly of the archaellum.[12][13][14][15][16] 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.[17]

Functional characterization has been performed for ArlI, a Type II/IV secretion system ATPase super-family member[18] and PibD/FlaK.[17][19][20] FlaI forms a hexamer which hydrolyses ATP and most likely generates energy to assemble the archaellum and to power its rotation. PibD cleaves the N-terminus of the archaellins before they can be assembled. ArlH (PDB: 2DR3​) has a RecA-like fold and inactive ATPase domains. ArlH and ArlJ are the two other core components that together with ArlI form a core platform/motor. ArlX acts as a scaffold around the motor in Crenarchaeota.[21] ArlF and ArlG are potentially part of the stator of the archaellum motor; ArlF binds the S-layer, and ArlG forms filaments that seem to be "capped" by ArlF. Therefore, these two proteins potentially act together to attach the motor complex to the S-layer and to provide a rigid structure against which the rotating components of the motor - likely ArlJ - can rotate [22][23].

The genes coding for arlC, arlD, and arlE are only present in Euryarchaeota and interact with chemotaxis proteins (e.g., CheY, CheD and CheC2, and the archaea-specific CheF) to sense environmental signals (such as exposure to light of specific wavelength, nutrient conditions etc.).[24][25]

Structure and assembly: type IV pilus (T4P) and archaellum

In the 1980s, Dieter Oesterhelt’s laboratory showed for the first time that haloarchaea switch the rotation of their archaellum from clockwise to counterclockwise upon blue light pulses.[26][27] This led microbiologists to believe that the archaeal motility structure is not only functionally, but also structurally reminiscent of bacterial flagella. Nevertheless, evidence started to build up indicating that archaella and flagella shared their function, but not their structure and evolutionary history. For example, in contrast to flagellins, archaellins (the protein monomers which form the archaellum filament) 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.[28] In Crenarchaeota PibD and in euryarchaeota FlaK are PilD homologs, whch are essential for the maturation of the archaellins. Furthermore, archaellins are N-glycosylated[29][30] which has not been described for bacterial flagellins, where O-linked glycosylation is evident.

Another stark difference between the archaellum and the flagellum is the diameter of their filaments. While the bacterial flagellum is hollow, which allows flagellin monomers to travel through its interior to the tip of the growing filament, the archaellum filament is thiner, precluding the passage of archaellin monomers [31][32][33][34][35]. This evidence suggested that the mechanism of assembly of the archaellum is more similar to the assembly mechanism observed in type IV pili (in which the monomers assemble at the bottom of the growing filament) than the assembly mechanism of flagella via a type III secretion system[36][37].

The similarities between archaella and T4P became more obvious with the identification of two archaella motor complex proteins that have homologues in T4P and type IV and II secretion systems. Specifically, ArkJ and ArlI are homologous to PilC and PilB/PilT, respectively. ArlJ is a membrane proteins for which little is structurally and functionally known, and ArlI is the only ATPase found in the archaellum operon, thus suggesting that this protein powers the assembly and the rotation of the filament [38][7][18].

Functional analogs

Despite the limited number 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[16][39][40] and semi-solid surfaces.[41][42] Increasing biochemical and biophysical information has further consolidated the early observations of archaella mediated swimming in archaea. Like the bacterial flagellum,[43][44] the archaellum also mediates surface attachment and cell-cell communication.[45][46] However, unlike the bacterial flagellum archaellum has not shown to play a role in archaeal biofilm formation.[47] 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. Also, archaellum have been found to be able to have a metal-binding site.[31]

References

  1. In some species, the names are given as FlgA and FlgB.
  1. 1.0 1.1 "The archaellum: how Archaea swim". Frontiers in Microbiology 6: 23. 27 January 2015. doi:10.3389/fmicb.2015.00023. PMID 25699024. 
  2. "An extensively glycosylated archaeal pilus survives extreme conditions". Nature Microbiology 4 (8): 1401–1410. August 2019. doi:10.1038/s41564-019-0458-x. PMID 31110358. 
  3. "Phylogenetic structure of the prokaryotic domain: the primary kingdoms". Proceedings of the National Academy of Sciences of the United States of America 74 (11): 5088–90. November 1977. doi:10.1073/pnas.74.11.5088. PMID 270744. Bibcode1977PNAS...74.5088W. 
  4. "Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya". Proceedings of the National Academy of Sciences of the United States of America 87 (12): 4576–9. June 1990. doi:10.1073/pnas.87.12.4576. PMID 2112744. Bibcode1990PNAS...87.4576W. 
  5. "Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella". Microbiology 149 (Pt 11): 3051–3072. November 2003. doi:10.1099/mic.0.26364-0. PMID 14600218. 
  6. "Archaeal type IV pilus-like structures--evolutionarily conserved prokaryotic surface organelles". Current Opinion in Microbiology 14 (3): 357–63. June 2011. doi:10.1016/j.mib.2011.03.002. PMID 21482178. 
  7. 7.0 7.1 7.2 "Assembly and function of the archaeal flagellum". Biochemical Society Transactions 39 (1): 64–9. January 2011. doi:10.1042/BST0390064. PMID 21265748. 
  8. "Type IV pilus structure and bacterial pathogenicity". Nature Reviews. Microbiology 2 (5): 363–78. May 2004. doi:10.1038/nrmicro885. PMID 15100690. 
  9. "Type IV pili: paradoxes in form and function". Current Opinion in Structural Biology 18 (2): 267–77. April 2008. doi:10.1016/j.sbi.2007.12.009. PMID 18249533. 
  10. "The archaellum: an old motility structure with a new name". Trends in Microbiology 20 (7): 307–12. July 2012. doi:10.1016/j.tim.2012.04.007. PMID 22613456. 
  11. "Archaeal cell surface biogenesis". FEMS Microbiology Reviews 42 (5): 694–717. September 2018. doi:10.1093/femsre/fuy027. PMID 29912330. 
  12. "The fla gene cluster is involved in the biogenesis of flagella in Halobacterium salinarum". Molecular Microbiology 41 (3): 653–63. August 2001. doi:10.1046/j.1365-2958.2001.02542.x. PMID 11532133. 
  13. "The archaeal flagellum: a different kind of prokaryotic motility structure". FEMS Microbiology Reviews 25 (2): 147–74. April 2001. doi:10.1111/j.1574-6976.2001.tb00575.x. PMID 11250034. 
  14. "Mutants in flaI and flaJ of the archaeon Methanococcus voltae are deficient in flagellum assembly". Molecular Microbiology 46 (3): 879–87. November 2002. doi:10.1046/j.1365-2958.2002.03220.x. PMID 12410843. 
  15. "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 (3): 596–609. November 2007. doi:10.1111/j.1365-2958.2007.05913.x. PMID 17887963. 
  16. 16.0 16.1 "Molecular analysis of the crenarchaeal flagellum". Molecular Microbiology 83 (1): 110–24. January 2012. doi:10.1111/j.1365-2958.2011.07916.x. PMID 22081969. 
  17. 17.0 17.1 "Cleavage of preflagellins by an aspartic acid signal peptidase is essential for flagellation in the archaeon Methanococcus voltae". Molecular Microbiology 50 (4): 1339–47. November 2003. doi:10.1046/j.1365-2958.2003.03758.x. PMID 14622420. 
  18. 18.0 18.1 "Archaeal flagellar ATPase motor shows ATP-dependent hexameric assembly and activity stimulation by specific lipid binding". The Biochemical Journal 437 (1): 43–52. July 2011. doi:10.1042/BJ20110410. PMID 21506936. 
  19. "FlaK of the archaeon Methanococcus maripaludis possesses preflagellin peptidase activity". FEMS Microbiology Letters 208 (1): 53–9. February 2002. doi:10.1111/j.1574-6968.2002.tb11060.x. PMID 11934494. 
  20. "Identification of diverse archaeal proteins with class III signal peptides cleaved by distinct archaeal prepilin peptidases". Journal of Bacteriology 189 (3): 772–8. February 2007. doi:10.1128/JB.01547-06. PMID 17114255. 
  21. "The Archaellum: An Update on the Unique Archaeal Motility Structure". Trends in Microbiology 26 (4): 351–362. April 2018. doi:10.1016/j.tim.2018.01.004. PMID 29452953. 
  22. "FlaF Is a β-Sandwich Protein that Anchors the Archaellum in the Archaeal Cell Envelope by Binding the S-Layer Protein". Structure 23 (5): 863–872. May 2015. doi:10.1016/j.str.2015.03.001. PMID 25865246. 
  23. "The structure of the periplasmic FlaG-FlaF complex and its essential role for archaellar swimming motility". Nature Microbiology 5 (1): 216–225. January 2020. doi:10.1038/s41564-019-0622-3. PMID 31844299. 
  24. "Identification of Archaea-specific chemotaxis proteins which interact with the flagellar apparatus". BMC Microbiology 9: 56. March 2009. doi:10.1186/1471-2180-9-56. PMID 19291314. 
  25. "Taxis in archaea". Emerging Topics in Life Sciences 2 (4): 535–46. December 2018. doi:10.1042/ETLS20180089. ISSN 2397-8554. 
  26. "Morphology, function and isolation of halobacterial flagella". Journal of Molecular Biology 176 (4): 459–75. July 1984. doi:10.1016/0022-2836(84)90172-4. PMID 6748081. 
  27. "Rotation and switching of the flagellar motor assembly in Halobacterium halobium". Journal of Bacteriology 173 (6): 1971–7. March 1991. doi:10.1128/jb.173.6.1971-1977.1991. PMID 2002000. 
  28. "Molecular analysis of archael flagellins: similarity to the type IV pilin-transport superfamily widespread in bacteria". Canadian Journal of Microbiology 40 (1): 67–71. January 1994. doi:10.1139/m94-011. PMID 7908603. 
  29. "S-layer glycoproteins and flagellins: reporters of archaeal posttranslational modifications". Archaea 2010: 1–13. July 2010. doi:10.1155/2010/612948. PMID 20721273. 
  30. "Sulfoquinovose synthase - an important enzyme in the N-glycosylation pathway of Sulfolobus acidocaldarius". Molecular Microbiology 82 (5): 1150–63. December 2011. doi:10.1111/j.1365-2958.2011.07875.x. PMID 22059775. 
  31. 31.0 31.1 "High-resolution archaellum structure reveals a conserved metal-binding site". EMBO Reports 20 (5). May 2019. doi:10.15252/embr.201846340. PMID 30898768. 
  32. "The structure of the archeabacterial flagellar filament of the extreme halophile Halobacterium salinarum R1M1 and its relation to eubacterial flagellar filaments and type IV pili". Journal of Molecular Biology 321 (3): 383–95. August 2002. doi:10.1016/S0022-2836(02)00616-2. PMID 12162953. 
  33. "CryoEM structure of the Methanospirillum hungatei archaellum reveals structural features distinct from the bacterial flagellum and type IV pilus". Nature Microbiology 2 (3): 16222. December 2016. doi:10.1038/nmicrobiol.2016.222. PMID 27922015. 
  34. "Refining the structure of the Halobacterium salinarum flagellar filament using the iterative helical real space reconstruction method: insights into polymorphism". Journal of Molecular Biology 346 (3): 665–76. February 2005. doi:10.1016/j.jmb.2004.12.010. PMID 15713454. 
  35. "The archaeabacterial flagellar filament: a bacterial propeller with a pilus-like structure". Journal of Molecular Microbiology and Biotechnology 11 (3–5): 208–20. 2006. doi:10.1159/000094055. PMID 16983196. https://www.karger.com/Article/FullText/94055. 
  36. "Genetics and biogenesis of bacterial flagella". Annual Review of Genetics 26: 131–58. 1992. doi:10.1146/annurev.ge.26.120192.001023. PMID 1482109. 
  37. "The archaeal flagellum: a unique motility structure". Journal of Bacteriology 178 (17): 5057–64. September 1996. doi:10.1128/JB.178.17.5057-5064.1996. PMID 8752319. 
  38. "Insights into FlaI functions in archaeal motor assembly and motility from structures, conformations, and genetics". Molecular Cell 49 (6): 1069–82. March 2013. doi:10.1016/j.molcel.2013.01.014. PMID 23416110. 
  39. "Flagella and motility behaviour of square bacteria". The EMBO Journal 3 (12): 2899–903. December 1984. doi:10.1002/j.1460-2075.1984.tb02229.x. PMID 6526006. 
  40. "Swimming behavior of selected species of Archaea". Applied and Environmental Microbiology 78 (6): 1670–4. March 2012. doi:10.1128/AEM.06723-11. PMID 22247169. 
  41. "Flagellar motility and structure in the hyperthermoacidophilic archaeon Sulfolobus solfataricus". Journal of Bacteriology 189 (11): 4305–9. June 2007. doi:10.1128/JB.00042-07. PMID 17416662. 
  42. "Isolation and characterization of insertional mutations in flagellin genes in the archaeon Methanococcus voltae". Molecular Microbiology 20 (3): 657–66. May 1996. doi:10.1046/j.1365-2958.1996.5371058.x. PMID 8736544. 
  43. "Bacterial surface translocation: a survey and a classification". Bacteriological Reviews 36 (4): 478–503. December 1972. doi:10.1128/MMBR.36.4.478-503.1972. PMID 4631369. 
  44. "The surprisingly diverse ways that prokaryotes move". Nature Reviews. Microbiology 6 (6): 466–76. June 2008. doi:10.1038/nrmicro1900. PMID 18461074. 
  45. "Flagella of Pyrococcus furiosus: multifunctional organelles, made for swimming, adhesion to various surfaces, and cell-cell contacts". Journal of Bacteriology 188 (19): 6915–23. October 2006. doi:10.1128/JB.00527-06. PMID 16980494. 
  46. "Appendage-mediated surface adherence of Sulfolobus solfataricus". Journal of Bacteriology 192 (1): 104–10. January 2010. doi:10.1128/JB.01061-09. PMID 19854908. 
  47. "Crenarchaeal biofilm formation under extreme conditions". PLOS ONE 5 (11): e14104. November 2010. doi:10.1371/journal.pone.0014104. PMID 21124788. Bibcode2010PLoSO...514104K.