Molecular analysis of archaeal flagellins: similarity to the type IV pilin – transport superfamily widespread in bacteria

Faguy, David M.; Jarrell, Ken F.; Kuzio, John; Kalmokoff, Martin

doi:10.1139/m94-011

Cited by 89 publications

(76 citation statements)

References 32 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This is suggestive of significant post-translational modification of the protein occurring in M. voltae. Earlier attempts to stain the M. voltae flagellins with glycoprotein stains such as the periodic acid Schiff reagent were unsuccessful (21). Attempts to determine the intact mass of the respective flagellins by mass spectrometry (MALDI-TOF MS and ESI-MS) have so far failed.…”

Section: Methodsmentioning

confidence: 99%

Identification and Characterization of the Unique N-Linked Glycan Common to the Flagellins and S-layer Glycoprotein of Methanococcus voltae

Voisin

Houliston

Kelly

et al. 2005

Journal of Biological Chemistry

Self Cite

131

144

View full text Add to dashboard Cite

The flagellum of Methanococcus voltae is composed of four structural flagellin proteins FlaA, FlaB1, FlaB2, and FlaB3. These proteins possess a total of 15 potential N-linked sequons (NX(S/T)) and show a mass shift on an SDS-polyacrylamide gel indicating significant posttranslational modification. We describe here the structural characterization of the flagellin glycan from M. voltae using mass spectrometry to examine the proteolytic digests of the flagellin proteins in combination with NMR analysis of the purified glycan using a sensitive, cryogenically cooled probe. Nano-liquid chromatography-tandem mass spectrometry analysis of the proteolytic digests of the flagellin proteins revealed that they are post-translationally modified with a novel Nlinked trisaccharide of mass 779 Da that is composed of three sugar residues with masses of 318, 258, and 203 Da, respectively. In every instance the glycan is attached to the peptide through the asparagine residue of a typical N-linked sequon. The glycan modification has been observed on 14 of the 15 sequon sites present on the four flagellin structural proteins. The novel glycan structure elucidated by NMR analysis was shown to be a trisaccharide composed of ␤-ManpNAcA6Thr-(1-4)-␤-GlcpNAc3NAcA-(1-3)-␤-GlcpNAc linked to Asn. In addition, the same trisaccharide was identified on a tryptic peptide of the S-layer protein from this organism implicating a common N-linked glycosylation pathway.Glycosylation of prokaryotic proteins is now well accepted, and examples of N-and O-glycosylation and of attachment of glycosylphosphatidylinositol anchors can now be found in the literature (1, 2). However, in contrast to eukaryotic glycosylation systems, prokaryotic systems display considerable diversity in the structure of the respective glycans and the proximal monosaccharide linkage. As a consequence there is considerable interest in determining the structural and genetic basis of glycan production among these diverse prokaryotic systems.The archaeal flagellum is a unique motility structure that is distinct from the well characterized bacterial flagellum (3). In contrast to bacterial flagellar assembly where newly synthesized flagellin is incorporated at the distal tip of the filament, it is believed that mature archaeal flagellin is incorporated at the base of the filament. In recent studies, the assembly of archaeal flagellum has been shown to more closely resemble a second bacterial motility system, the type IV pilus, where the structural protein pilin is synthesized with an unusual signal peptide and a hydrophobic N terminus. In Archaea, signal peptidases have been shown to cleave a signal peptide of the preflagellin proteins to produce mature flagellin, which is then incorporated into the filament (4). Flagellated archaeal species have one to five flagellin genes organized into a fla locus (3). The marine archaeon Methanococcus voltae has four flagellin structural genes organized in two transcriptional units: one unit contains flaA, whereas the second unit contains flaB1, flaB...

show abstract

Section: Methodsmentioning

confidence: 99%

Identification and Characterization of the Unique N-Linked Glycan Common to the Flagellins and S-layer Glycoprotein of Methanococcus voltae

Voisin

Houliston

Kelly

et al. 2005

Journal of Biological Chemistry

Self Cite

131

144

View full text Add to dashboard Cite

show abstract

“…Eubacterial flagellin filaments disassemble to monomers under very acid conditions, and at somewhat acid pH eubacterial flagella undergo a remarkable phase transition to an abnormal, less efficient, curly form (Kamiya et al, 1982). Replacing an ancestral flagellin polymer by recruiting an acidstable glycoprotein from pili, which the shaft resembles (Faguy et al, 1994), would have enabled archaebacterial flagella to function in highly acid conditions, while retaining the same basal rotary motor. As archaebacterial flagella operate well in neutral conditions, there would be no selective advantage in replacing them by flagellin in secondary mesophiles.…”

Section: Secondary Hyperthermophily and Acidophily And The Origin Of mentioning

confidence: 99%

“…Because of their novel lipids, thermophilic archaebacteria can control their pH and use proton gradients as energy sources, unlike eubacterial thermophiles (Albers et al, 2000). I now argue that secondary acidophily gives a simple adaptive explanation to the otherwise puzzling fact that archaebacterial flagellar shafts lack classical flagellins but are built of unrelated proteins (Faguy et al, 1994). Eubacterial flagellin filaments disassemble to monomers under very acid conditions, and at somewhat acid pH eubacterial flagella undergo a remarkable phase transition to an abnormal, less efficient, curly form (Kamiya et al, 1982).…”

mentioning

confidence: 99%

The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification.

Cavalier‐Smith¹

2002

International Journal of Systematic and Evolutionary Microbiology

418

590

View full text Add to dashboard Cite

Prokaryotes constitute a single kingdom, Bacteria, here divided into two new subkingdoms : Negibacteria, with a cell envelope of two distinct genetic membranes, and Unibacteria, comprising the new phyla Archaebacteria and Posibacteria, with only one. Other new bacterial taxa are established in a revised higher-level classification that recognizes only eight phyla and 29 classes. Morphological, palaeontological and molecular data are integrated into a unified picture of large-scale bacterial cell evolution despite occasional lateral gene transfers. Archaebacteria and eukaryotes comprise the clade neomura, with many common characters, notably obligately co-translational secretion of N-linked glycoproteins, signal recognition particle with 7S RNA and translationarrest domain, protein-spliced tRNA introns, eight-subunit chaperonin, prefoldin, core histones, small nucleolar ribonucleoproteins (snoRNPs), exosomes and similar replication, repair, transcription and translation machinery. Eubacteria (posibacteria and negibacteria) are paraphyletic, neomura having arisen from Posibacteria within the new subphylum Actinobacteria (possibly from the new class Arabobacteria, from which eukaryotic cholesterol biosynthesis probably came). Replacement of eubacterial peptidoglycan by glycoproteins and adaptation to thermophily are the keys to neomuran origins. All 19 common neomuran character suites probably arose essentially simultaneously during the radical modification of an actinobacterium. At least 11 were arguably adaptations to thermophily. Most unique archaebacterial characters (prenyl ether lipids ; flagellar shaft of glycoprotein, not flagellin ; DNA-binding protein 10b ; specially modified tRNA ; absence of Hsp90) were subsequent secondary adaptations to hyperthermophily and/or hyperacidity. The insertional origin of protein-spliced tRNA introns and an insertion in proton-pumping ATPase also support the origin of neomura from eubacteria. Molecular co-evolution between histones and DNA-handling proteins, and in novel protein initiation and secretion machineries, caused quantum evolutionary shifts in their properties in stem neomura. Proteasomes probably arose in the immediate common ancestor of neomura and Actinobacteria. Major gene losses (e.g. peptidoglycan synthesis, hsp90, secA) and genomic reduction were central to the origin of archaebacteria. Ancestral archaebacteria were probably heterotrophic, anaerobic, sulphur-dependent hyperthermoacidophiles ; methanogenesis and halophily are secondarily derived. Multiple lateral gene transfers from eubacteria helped secondary archaebacterial adaptations to mesophily and genome re-expansion. The origin from a drastically altered actinobacterium of neomura, and the immediately subsequent simultaneous origins of archaebacteria and eukaryotes, are the most extreme and important cases of T. Cavalier-Smith quantum evolution since cells began. All three strikingly exemplify De Beer's principle of mosaic evolution : the fact that, during major evolutionary transformations, some org...

show abstract

“…In bacteria, this residue is usually a phenylalanine. Faguy et al (1994) first noted the occurrence of type IV pilin-like signal peptides in archaea by examining Methanococcus voltae flagellins. All archaeal flagellins exhibit a short, positively charged signal peptide of 4-18 residues (Fig.…”

Section: Class 2: Lipoprotein Signal Peptidesmentioning

confidence: 99%

Signal peptides of secreted proteins of the archaeon Sulfolobus solfataricus : a genomic survey

Albers

Driessen

2002

Archives of Microbiology

View full text Add to dashboard Cite

Signal peptides of secreted proteins of the archaeon Sulfolobus solfataricus: a genomic survey Albers, S.V.; Driessen, A.J.M. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim.Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 23-03-2019Abstract Analysis of the recently completed genome sequence of the thermoacidophilic archaeon Sulfolobus solfataricus reveals that about 4.2% of its proteome consists of putative secretory proteins with signal peptides. This includes members of the four major classes of signal peptides: secretory signal peptides, twin-arginine signal peptides, possible lipoprotein precursors, and type IV pilin signal peptides. The latter group is surprisingly large compared to the size of the groups in other organisms and seems to be used predominately for a subset of extracellular substrate-binding proteins.

show abstract

Molecular analysis of archaeal flagellins: similarity to the type IV pilin – transport superfamily widespread in bacteria

Cited by 89 publications

References 32 publications

Identification and Characterization of the Unique N-Linked Glycan Common to the Flagellins and S-layer Glycoprotein of Methanococcus voltae

Identification and Characterization of the Unique N-Linked Glycan Common to the Flagellins and S-layer Glycoprotein of Methanococcus voltae

The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification.

Signal peptides of secreted proteins of the archaeon Sulfolobus solfataricus : a genomic survey

Contact Info

Product

Resources

About