{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T22:14:27Z","timestamp":1790979267134,"version":"4.1.0"},"reference-count":63,"publisher":"Microbiology Society","issue":"12","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2006,12,1]]},"abstract":"<jats:p><jats:italic>Neisseria meningitidis<\/jats:italic>is the causative agent of epidemic meningococcal meningitis and septicaemia. Type IV pili are surface organelles that mediate a variety of functions, including adhesion, twitching motility, and competence for DNA binding and uptake in transformation. The secretin PilQ is required for type IV pilus expression at the cell surface, and forms a dodecameric cage-like macromolecular complex in the meningococcal outer membrane. PilQ-null mutants are devoid of surface pili, and prevailing evidence suggests that the PilQ complex facilitates extrusion and retraction of type IV pili across the outer membrane. Defining the orientation of the meningococcal PilQ complex in the membrane is a prerequisite for understanding the structure\u2013function relationships of this important protein in pilus biology. In order to begin to define the topology of the PilQ complex in the outer membrane, polyhistidine insertions in N- and C-terminal regions of PilQ were constructed, and their subcellular locations examined. Notably, the insertion epitopes at residues 205 and 678 were located within the periplasm, whereas residue 656 was exposed at the outer surface of the outer membrane. Using electron microscopy with Ni-NTA gold labelling, it was demonstrated that the insertion at residue 205 within the N-terminus mapped to a site on the arm-like features of the 3D structure of the PilQ multimer. Interestingly, mutation of the same region gave rise to an increase in vancomycin permeability through the PilQ complex. The results yield novel information on the PilQ N-terminal location and function in the periplasm, and reveal a complex organization of the membrane-spanning secretin<jats:italic>in vivo<\/jats:italic>.<\/jats:p>","DOI":"10.1099\/mic.0.2006\/000315-0","type":"journal-article","created":{"date-parts":[[2006,12,12]],"date-time":"2006-12-12T08:28:10Z","timestamp":1165912090000},"page":"3751-3764","source":"Crossref","is-referenced-by-count":31,"title":["Topology of the outer-membrane secretin PilQ from Neisseria meningitidis"],"prefix":"10.1099","volume":"152","author":[{"given":"Stephan A.","family":"Frye","sequence":"first","affiliation":[{"name":"Centre for Molecular Biology and Neuroscience and Institute of Microbiology, Rikshospitalet-Radiumhospitalet Medical Centre, Norway"},{"name":"Centre for Molecular Biology and Neuroscience and Institute of Microbiology, University of Oslo, Norway"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Reza","family":"Assalkhou","sequence":"additional","affiliation":[{"name":"Centre for Molecular Biology and Neuroscience and Institute of Microbiology, University of Oslo, Norway"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard F.","family":"Collins","sequence":"additional","affiliation":[{"name":"Faculty of Life Sciences, The University of Manchester, Sackville Street, PO Box 88, Manchester M60 1QD, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert C.","family":"Ford","sequence":"additional","affiliation":[{"name":"Faculty of Life Sciences, The University of Manchester, Sackville Street, PO Box 88, Manchester M60 1QD, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christoffer","family":"Petersson","sequence":"additional","affiliation":[{"name":"Division of Medical Microbiology, Department of Molecular and Clinical Medicine, Faculty of Health Sciences, Link\u00f6ping University, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeremy P.","family":"Derrick","sequence":"additional","affiliation":[{"name":"Faculty of Life Sciences, The University of Manchester, Sackville Street, PO Box 88, Manchester M60 1QD, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tone","family":"T\u00f8njum","sequence":"additional","affiliation":[{"name":"Centre for Molecular Biology and Neuroscience and Institute of Microbiology, Rikshospitalet-Radiumhospitalet Medical Centre, Norway"},{"name":"Centre for Molecular Biology and Neuroscience and Institute of Microbiology, University of Oslo, Norway"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"345","reference":[{"key":"R1","first-page":"44","article-title":"Electron microscopy","volume-title":"Methods for General and Molecular Microbiology","author":"Beveridge","year":"1994"},{"key":"R2","doi-asserted-by":"crossref","first-page":"1905","DOI":"10.1084\/jem.20050112","article-title":"A chromosomally integrated bacteriophage in invasive meningococci","volume":"201","author":"Bille","year":"2005","journal-title":"J Exp Med"},{"key":"R3","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1046\/j.1365-2958.1998.00677.x","article-title":"Formation of oligomeric rings by XcpQ and PilQ, which are involved in protein transport across the outer membrane of Pseudomonas aeruginosa","volume":"27","author":"Bitter","year":"1998","journal-title":"Mol Microbiol"},{"key":"R4","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal Biochem"},{"key":"R5","first-page":"155","article-title":"Uses of pili in gonorrhoea control: role of bacterial pili in disease, purification and properties of gonococcal pili, and progress in the development of a gonococcal pilus vaccine for gonorrhoeae","volume-title":"Immunobiology of Neisseria gonorrhoeae","author":"Brinton","year":"1978"},{"key":"R6","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1111\/j.1365-2958.2004.04364.x","article-title":"Type IV pilus biogenesis in Neisseria meningitidis : PilW is involved in a step occurring after pilus assembly, essential for fibre stability and function","volume":"55","author":"Carbonnelle","year":"2005","journal-title":"Mol Microbiol"},{"key":"R7","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1128\/JB.186.3.730-739.2004","article-title":"A mutant form of the Neisseria gonorrhoeae pilus secretin protein PilQ allows increased entry of heme and antimicrobial compounds","volume":"186","author":"Chen","year":"2004","journal-title":"J Bacteriol"},{"key":"R8","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1016\/S1570-9639(02)00467-3","article-title":"Expression and localization of alpha- and beta-carbonic anhydrase in Helicobacter pylori","volume":"1601","author":"Chirica","year":"2002","journal-title":"Biochim Biophys Acta"},{"key":"R9","doi-asserted-by":"crossref","first-page":"3825","DOI":"10.1128\/JB.183.13.3825-3832.2001","article-title":"Analysis of the PilQ secretin from Neisseria meningitidis by transmission electron microscopy reveals a dodecameric quaternary structure","volume":"183","author":"Collins","year":"2001","journal-title":"J Bacteriol"},{"key":"R10","doi-asserted-by":"crossref","first-page":"2611","DOI":"10.1128\/JB.185.8.2611-2617.2003","article-title":"Three-dimensional structure of the Neisseria meningitidis secretin PilQ determined from negative-stain transmission electron microscopy","volume":"185","author":"Collins","year":"2003","journal-title":"J Bacteriol"},{"key":"R11","doi-asserted-by":"crossref","first-page":"39750","DOI":"10.1074\/jbc.M405971200","article-title":"Structure of the Neisseria meningitidis outer membrane PilQ secretin complex at 12\u2005A\u030a resolution","volume":"279","author":"Collins","year":"2004","journal-title":"J Biol Chem"},{"key":"R12","doi-asserted-by":"crossref","first-page":"18923","DOI":"10.1074\/jbc.M411603200","article-title":"Interaction with type IV pili induces structural changes in the bacterial outer membrane secretin PilQ","volume":"280","author":"Collins","year":"2005","journal-title":"J Biol Chem"},{"key":"R13","doi-asserted-by":"crossref","first-page":"2144","DOI":"10.1074\/jbc.M508078200","article-title":"Periplasmic protein\u2013protein contacts in the inner membrane protein Wzc form a tetrameric complex required for the assembly of Escherichia coli group 1 capsules","volume":"281","author":"Collins","year":"2006","journal-title":"J Biol Chem"},{"key":"R14","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1007\/978-94-009-1383-7_107","article-title":"Antibodies to outer-membrane protein\u2013macromolecular complex (OMP-MC) are bactericidal for serum-resistant gonococci","volume-title":"Gonococci and Meningococci","author":"Corbett","year":"1988"},{"key":"R15","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1093\/bioinformatics\/14.10.892","article-title":"JPred: a consensus secondary structure prediction server","volume":"14","author":"Cuff","year":"1998","journal-title":"Bioinformatics"},{"key":"R16","doi-asserted-by":"crossref","first-page":"978","DOI":"10.1006\/jmbi.1996.0866","article-title":"Module swaps between related translocator proteins pIV(f1), pIV(IKe) and PulD: identification of a specificity domain","volume":"266","author":"Daefler","year":"1997","journal-title":"J Mol Biol"},{"key":"R17","doi-asserted-by":"crossref","first-page":"872","DOI":"10.1128\/IAI.10.4.872-876.1974","article-title":"Ultrastructure of pili and annular structures on the cell wall surface of Neisseria meningitidis","volume":"10","author":"Devoe","year":"1974","journal-title":"Infect Immun"},{"key":"R18","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1111\/j.1365-2958.1995.18050975.x","article-title":"The product of the pilQ gene is essential for the biogenesis of type IV pili in Neisseria gonorrhoeae","volume":"18","author":"Drake","year":"1995","journal-title":"Mol Microbiol"},{"key":"R19","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1046\/j.1365-2958.1997.2511618.x","article-title":"PilP, a pilus biogenesis lipoprotein in Neisseria gonorrhoeae , affects expression of PilQ as a high-molecular-mass multimer","volume":"23","author":"Drake","year":"1997","journal-title":"Mol Microbiol"},{"key":"R20","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1128\/IAI.5.1.98-102.1972","article-title":"Classification of Neisseria meningitidis group B into distinct serotypes. I. Serological typing by a microbactericidal method","volume":"5","author":"Frasch","year":"1972","journal-title":"Infect Immun"},{"key":"R21","first-page":"525","article-title":"Electron microscopical and cultural features of Neisseria meningitidis competence variants","volume":"[B] 81","author":"Fr\u00f8holm","year":"1973","journal-title":"Acta Pathol Microbiol Scand"},{"key":"R22","doi-asserted-by":"crossref","first-page":"1215","DOI":"10.1111\/j.1365-2958.1990.tb00697.x","article-title":"Generation of capsule-deficient Neisseria meningitidis strains by homologous recombination","volume":"4","author":"Frosch","year":"1990","journal-title":"Mol Microbiol"},{"key":"R23","doi-asserted-by":"crossref","first-page":"3443","DOI":"10.1242\/jcs.108.11.3443","article-title":"Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes","volume":"108","author":"Fujimoto","year":"1995","journal-title":"J Cell Sci"},{"key":"R24","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1007\/BF00283883","article-title":"A superfamily of proteins involved in different secretion pathways in Gram-negative bacteria: modular structure and specificity of the N-terminal domain","volume":"243","author":"Genin","year":"1994","journal-title":"Mol Gen Genet"},{"key":"R25","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1093\/protein\/10.5.497","article-title":"Identification of membrane spanning beta strands in bacterial porins","volume":"10","author":"Gromiha","year":"1997","journal-title":"Protein Eng"},{"key":"R26","doi-asserted-by":"crossref","first-page":"7212","DOI":"10.1128\/JB.181.23.7212-7220.1999","article-title":"Genetic dissection of the outer membrane secretin PulD: are there distinct domains for multimerization and secretion specificity?","volume":"181","author":"Guilvout","year":"1999","journal-title":"J Bacteriol"},{"key":"R27","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1128\/IAI.43.3.839-845.1984","article-title":"Conservation of peptide structure of outer membrane protein-macromolecular complex from Neisseria gonorrhoeae","volume":"43","author":"Hansen","year":"(1984","journal-title":"Infect Immun"},{"key":"R28","doi-asserted-by":"crossref","first-page":"967","DOI":"10.1046\/j.1365-2958.1996.01539.x","article-title":"The secretin-specific, chaperone-like protein of the general secretory pathway: separation of proteolytic protection and piloting functions","volume":"22","author":"Hardie","year":"1996","journal-title":"Mol Microbiol"},{"key":"R29","doi-asserted-by":"crossref","DOI":"10.1017\/S1551929500060016","volume-title":"Negative Staining and Cryoelectron Microscopy","author":"Harris","year":"1997"},{"key":"R30","doi-asserted-by":"crossref","first-page":"10798","DOI":"10.1073\/pnas.0402397101","article-title":"Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili","volume":"101","author":"Hegge","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R31","first-page":"445","article-title":"Studies on bacterial surface translocation. 2.Correlation of twitching motility and fimbriation in colony variants of Moraxella nonliquefaciens , M. bovis , and M. kingii","volume":"80","author":"Henrichsen","year":"1972","journal-title":"Acta Pathol Microbiol Scand [B]"},{"key":"R32","first-page":"528","article-title":"Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction","volume":"8","author":"Horton","year":"1990","journal-title":"Biotechniques"},{"key":"R33","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1111\/j.1365-2958.1994.tb00435.x","article-title":"Sequence changes in the pilus subunit lead to tropism variation of Neisseria gonorrhoeae to human tissue","volume":"13","author":"Jo\u0308nsson","year":"1994","journal-title":"Mol Microbiol"},{"key":"R34","doi-asserted-by":"crossref","first-page":"1962","DOI":"10.1128\/JB.178.7.1962-1970.1996","article-title":"Essential role of a sodium dodecyl sulfate-resistant protein IV multimer in assembly-export of filamentous phage","volume":"178","author":"Linderoth","year":"1996","journal-title":"J Bacteriol"},{"key":"R35","first-page":"3165","article-title":"On the role of pili in transformation of Neisseria gonorrhoeae","volume":"130","author":"Mathis","year":"1984","journal-title":"J Gen Microbiol"},{"key":"R36","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1038\/35024105","article-title":"Pilus retraction powers bacterial twitching motility","volume":"407","author":"Merz","year":"2000","journal-title":"Nature"},{"key":"R37","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1016\/S0962-8924(99)01634-7","article-title":"Bacterial type II protein export and pilus biogenesis: more than just homologies?","volume":"9","author":"Nunn","year":"1999","journal-title":"Trends Cell Biol"},{"key":"R38","doi-asserted-by":"crossref","first-page":"3281","DOI":"10.1073\/pnas.88.8.3281","article-title":"Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase","volume":"88","author":"Nunn","year":"1991","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R39","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1016\/S0022-2836(02)01246-9","article-title":"Structure of the filamentous phage pIV multimer by cryo-electron microscopy","volume":"325","author":"Opalka","year":"2003","journal-title":"J Mol Biol"},{"key":"R40","doi-asserted-by":"crossref","first-page":"3051","DOI":"10.1099\/mic.0.26364-0","article-title":"Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella","volume":"149","author":"Peabody","year":"2003","journal-title":"Microbiology"},{"key":"R41","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1177\/002215540004800616","article-title":"A new method to visualize the Helicobacter pylori -associated Lewis(b)-binding adhesin utilizing SDS-digested freeze-fracture replica labeling","volume":"48","author":"Petersson","year":"2000","journal-title":"J Histochem Cytochem"},{"key":"R42","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1128\/MMBR.57.1.50-108.1993","article-title":"The complete general secretory pathway in Gram-negative bacteria","volume":"57","author":"Pugsley","year":"1993","journal-title":"Microbiol Rev"},{"key":"R43","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/373357a0","article-title":"Neisseria PilC protein identified as type-4 pilus tip-located adhesin","volume":"373","author":"Rudel","year":"1995","journal-title":"Nature"},{"key":"R44","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1111\/j.1365-2958.1994.tb01296.x","article-title":"Mutants at conserved positions in gene IV, a gene required for assembly and secretion of filamentous phages","volume":"14","author":"Russel","year":"1994","journal-title":"Mol Microbiol"},{"key":"R45","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/S0378-1119(96)00801-3","article-title":"Filamentous phage assembly: variation on a protein export theme","volume":"192","author":"Russel","year":"1997","journal-title":"Gene"},{"key":"R46","volume-title":"Molecular Cloning: a Laboratory Manual","author":"Sambrook","year":"1989"},{"key":"R47","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1016\/0003-2697(87)90587-2","article-title":"Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100\u2005kDa","volume":"166","author":"Scha\u0308gger","year":"1987","journal-title":"Anal Biochem"},{"key":"R48","doi-asserted-by":"crossref","first-page":"4848","DOI":"10.1128\/JB.183.16.4848-4859.2001","article-title":"Structure-function analysis of BfpB, a secretin-like protein encoded by the bundle-forming-pilus operon of enteropathogenic Escherichia coli","volume":"183","author":"Schmidt","year":"2001","journal-title":"J Bacteriol"},{"key":"R49","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1128\/JB.172.1.40-46.1990","article-title":"Shuttle mutagenesis of Neisseria gonorrhoeae : pilin null mutations lower DNA transformation competence","volume":"172","author":"Seifert","year":"1990","journal-title":"J Bacteriol"},{"key":"R50","doi-asserted-by":"crossref","first-page":"886","DOI":"10.1084\/jem.134.4.886","article-title":"Studies on gonococcus infection. I. Pili and zones of adhesion: their relation to gonococcal growth patterns","volume":"134","author":"Swanson","year":"1971","journal-title":"J Exp Med"},{"key":"R51","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1046\/j.1365-2958.1998.00910.x","article-title":"Structure and function of repetitive sequence elements associated with a highly polymorphic domain of the Neisseria meningitidis PilQ protein","volume":"29","author":"Tonjum","year":"1998","journal-title":"Mol Microbiol"},{"key":"R52","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1111\/j.1365-2958.1995.tb02410.x","article-title":"Identification and characterization of pilG , a highly conserved pilus-assembly gene in pathogenic Neisseria","volume":"16","author":"T\u00f8njum","year":"1995","journal-title":"Mol Microbiol"},{"key":"R53","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/S0378-1119(97)00018-8","article-title":"The pilus colonization factor of pathogenic neisserial species: organelle biogenesis and structure\/function relationships \u2013 a review","volume":"192","author":"T\u00f8njum","year":"1997","journal-title":"Gene"},{"key":"R54","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1046\/j.1365-2958.1998.00910.x","article-title":"Structure and function of repetitive sequence elements associated with a highly polymorphic domain of the Neisseria meningitidis PilQ protein","volume":"29","author":"T\u00f8njum","year":"1998","journal-title":"Mol Microbiol"},{"key":"R55","doi-asserted-by":"crossref","first-page":"2653","DOI":"10.1128\/IAI.57.9.2653-2659.1989","article-title":"Cloning and DNA sequence of the omc gene encoding the outer membrane protein\u2013macromolecular complex from Neisseria gonorrhoeae","volume":"57","author":"Tsai","year":"(1989","journal-title":"Infect Immun"},{"key":"R56","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1128\/jcm.3.2.172-174.1976","article-title":"Simple disk-plate method for the biochemical confirmation of pathogenic Neisseria","volume":"3","author":"Valu","year":"1976","journal-title":"J Clin Microbiol"},{"key":"R57","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1042\/bst0270498","article-title":"Glycans in meningococcal pathogenesis","volume":"27","author":"Virji","year":"1999","journal-title":"Biochem Soc Trans"},{"key":"R58","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1126\/science.1078973","article-title":"Role of a highly conserved bacterial protein in outer membrane protein assembly","volume":"299","author":"Voulhoux","year":"2003","journal-title":"Science"},{"key":"R59","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1128\/JB.181.1.24-33.1999","article-title":"The Myxococcus xanthus pilQ ( sglA ) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility, and development","volume":"181","author":"Wall","year":"1999","journal-title":"J Bacteriol"},{"key":"R60","doi-asserted-by":"crossref","first-page":"15276","DOI":"10.1073\/pnas.261574998","article-title":"Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence","volume":"98","author":"Winther-Larsen","year":"2001","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R61","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1046\/j.1365-2958.1998.00935.x","article-title":"PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae","volume":"29","author":"Wolfgang","year":"1998","journal-title":"Mol Microbiol"},{"key":"R62","doi-asserted-by":"crossref","first-page":"1345","DOI":"10.1046\/j.1365-2958.1999.01269.x","article-title":"The comP locus of Neisseria gonorrhoeae encodes a type IV prepilin that is dispensable for pilus biogenesis but essential for natural transformation","volume":"31","author":"Wolfgang","year":"1999","journal-title":"Mol Microbiol"},{"key":"R63","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1111\/j.1365-2958.2005.04752.x","article-title":"The penC mutation conferring antibiotic resistance in Neisseria gonorrhoeae arises from a mutation in the PilQ secretin that interferes with multimer stability","volume":"57","author":"Zhao","year":"2005","journal-title":"Mol Microbiol"}],"container-title":["Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/micro\/10.1099\/mic.0.2006\/000315-0?crawler=true","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,8,5]],"date-time":"2021-08-05T21:06:42Z","timestamp":1628197602000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/micro\/10.1099\/mic.0.2006\/000315-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2006,12,1]]},"references-count":63,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2006,12,1]]}},"URL":"https:\/\/doi.org\/10.1099\/mic.0.2006\/000315-0","relation":{},"ISSN":["1350-0872","1465-2080"],"issn-type":[{"value":"1350-0872","type":"print"},{"value":"1465-2080","type":"electronic"}],"subject":[],"published":{"date-parts":[[2006,12,1]]}}}