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CryoEM structure of the type IVa pilus secretin required for natural competence in Vibrio cholerae
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Abstract
Natural transformation is the process by which bacteria take up genetic material from their environment and integrate it into their genome by homologous recombination. It represents one mode of horizontal gene transfer and contributes to the spread of traits like antibiotic resistance. In Vibrio cholerae , a type IVa pilus (T4aP) is thought to facilitate natural transformation by extending from the cell surface, binding to exogenous DNA, and retracting to thread this DNA through the outer membrane secretin, PilQ. Here, we use a functional tagged allele of VcPilQ purified from native V. cholerae cells to determine the cryoEM structure of the VcPilQ secretin in amphipol to ~2.7 Å. We use bioinformatics to examine the domain architecture and gene neighborhood of T4aP secretins in Proteobacteria in comparison with VcPilQ. This structure highlights differences in the architecture of the T4aP secretin from the type II and type III secretion system secretins. Based on our cryoEM structure, we design a series of mutants to reversibly regulate VcPilQ gate dynamics. These experiments support the idea of VcPilQ as a potential druggable target and provide insight into the channel that DNA likely traverses to promote the spread of antibiotic resistance via horizontal gene transfer by natural transformation.
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Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566
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Research works printed but not linked: 139
- von Wintersdorff, C. J. H. et al. Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Front. Microbiol. 7, 173 (2016). · DOI · Paper page
- Blokesch, M. In and out—contribution of natural transformation to the shuffling of large genomic regions. Curr. Opin. Microbiol. 38, 22–29 (2017). · DOI
- Berry, J.-L. & Pelicic, V. Exceptionally widespread nanomachines composed of type IV pilins: the prokaryotic Swiss Army knives. FEMS Microbiol. Rev. 39, 134–154 (2015). · DOI
- Piepenbrink, K. H. DNA uptake by type IV filaments. Front. Mol. Biosci. 6, 1 (2019). · DOI
- Maiden, M. C. J. Horizontal genetic exchange, evolution, and spread of antibiotic resistance in bacteria. Clin. Infect. Dis. 27, S12–S20 (1998). · DOI
- Domingues, S. et al. Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. PLoS Pathog. 8, e1002837 (2012). · DOI
- Blokesch, M. & Schoolnik, G. K. Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathog. 3, e81 (2007). · DOI
- Miller, M. C., Keymer, D. P., Avelar, A., Boehm, A. B. & Schoolnik, G. K. Detection and transformation of genome segments that differ within a coastal population of Vibrio cholerae strains. Appl. Environ. Microbiol. 73, 3695–3704 (2007). · DOI
- Croucher, N. J. et al. Rapid pneumococcal evolution in response to clinical interventions. Science 331, 430–434 (2011). · DOI
- Hu, D. et al. Origins of the current seventh cholera pandemic. Proc. Natl. Acad. Sci. U.S.A. 113, E7730–E7739 (2016).
- Sun, Y., Bernardy, E. E., Hammer, B. K. & Miyashiro, T. Competence and natural transformation in vibrios. Mol. Microbiol. 89, 583–595 (2013). · DOI
- Takemura, A. F., Chien, D. M. & Polz, M. F. Associations and dynamics of Vibrionaceae in the environment, from the genus to the population level. Front. Microbiol. 5, 38 (2014). · DOI
- Wittman, R. J. & Flick, G. J. Microbial contamination of shellfish: prevalence, risk to human health, and control strategies. Annu. Rev. Public Health 16, 123–140 (1995). · DOI
- Butt, A. A., Aldridge, K. E. & Sanders, C. V. Infections related to the ingestion of seafood Part I: viral and bacterial infections. Lancet Infect. Dis. 4, 201–212 (2004). · DOI
- Pelicic, V. Type IV pili: e pluribus unum? Mol. Microbiol. 68, 827–837 (2008). · DOI
- Craig, L., Forest, K. T. & Maier, B. Type IV pili: dynamics, biophysics and functional consequences. Nat. Rev. Microbiol. 17, 429–440 (2019). · DOI
- Burrows, L. L. Pseudomonas aeruginosa twitching motility: Type IV Pili in action. Annu. Rev. Microbiol. 66, 493–520 (2012). · DOI
- Hospenthal, M. K., Costa, T. R. & Waksman, G. A comprehensive guide to pilus biogenesis in gram-negative bacteria. Nat. Rev. Microbiol. 15, 365–379 (2017). · DOI
- Maier, B. & Wong, G. C. L. How bacteria use type IV pili machinery on surfaces. Trends Microbiol. 23, 775–788 (2015). · DOI
- Proft, T. & Baker, E. Pili in gram-negative and gram-positive bacteria—structure, assembly and their role in disease. Cell. Mol. Life Sci. 66, 613–635 (2009). · DOI
- Aagesen, A. M. & Häse, C. C. Sequence analyses of type IV pili from Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio vulnificus. Microb. Ecol. 64, 509–524 (2012). · DOI
- Simpson, C. A., Podicheti, R., Rusch, D. B., Dalia, A. B. & van Kessel, J. C. Diversity in natural transformation frequencies and regulation across Vibrio species. mBio 10, e02788-19 (2019). · DOI
- Meibom, K. L., Blokesch, M., Dolganov, N. A., Wu, C. -Y. & Schoolnik, G. K. Chitin induces natural competence in Vibrio cholerae. Science 310, 1824–1827 (2005). · DOI
- Gulig, P. A., Tucker, M. S., Thiaville, P. C., Joseph, J. L. & Brown, R. N. USER friendly cloning coupled with chitin-based natural transformation enables rapid mutagenesis of Vibrio vulnificus. AEM 75, 4936–4949 (2009). · DOI
- Chen, Y., Dai, J., Morris, J. G. & Johnson, J. A. Genetic analysis of the capsule polysaccharide (K antigen) and exopolysaccharide genes in pandemic Vibrio parahaemolyticus O3:K6. BMC Microbiol. 10, 274 (2010). · DOI
- Neiman, J., Guo, Y. & Rowe-Magnus, D. A. Chitin-induced carbotype conversion in Vibrio vulnificus. Infect. Immun. 79, 3195–3203 (2011). · DOI
- Yamamoto, S. et al. Regulation of natural competence by the orphan two-component system sensor kinase ChiS involves a non-canonical transmembrane regulator in Vibrio cholerae. Mol. Microbiol. 91, 326–347 (2014). · DOI
- Dalia, A. B., Lazinski, D. W. & Camilli, A. Identification of a membrane-bound transcriptional regulator that links chitin and natural competence in Vibrio cholerae. mBio 5, e01028-13 (2014). · DOI
- Meibom, K. L. et al. The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. U.S.A. 101, 2524–2529 (2004). · DOI
- Seitz, P. & Blokesch, M. DNA-uptake machinery of naturally competent Vibrio cholerae. Proc. Natl. Acad. Sci. U.S.A. 110, 17987–17992 (2013). · DOI
- Ellison, C. K. et al. Retraction of DNA-bound type IV competence pili initiates DNA uptake during natural transformation in Vibrio cholerae. Nat. Microbiol. 3, 773–780 (2018). · DOI
- Sandkvist, M. Biology of type II secretion. Mol. Microbiol. 40, 271–283 (2001). · DOI
- Korotkov, K. V., Gonen, T. & Hol, W. G. Secretins: dynamic channels for protein transport across membranes. Trends Biochem. Scie. 36, 433–443 (2011). · DOI
- Majewski, D. D., Worrall, L. J. & Strynadka, N. C. Secretins revealed: structural insights into the giant gated outer membrane portals of bacteria. Curr. Opin. Struct. Biol. 51, 61–72 (2018). · DOI
- Genin, S. & Boucher, C. A. A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Molec. Gen. Genet. 243, 112–118 (1994). · DOI
- Green, E. R. & Mecsas, J. Bacterial secretion systems—an overview. Microbiol. Spectr. 4, 215–239 (2016). · DOI
- Adams, D. W., Stutzmann, S., Stoudmann, C. & Blokesch, M. DNA-uptake pili of Vibrio cholerae are required for chitin colonization and capable of kin recognition via sequence-specific self-interaction. Nat. Microbiol. 4, 1545–1557 (2019). · DOI
- Burkhardt, J., Vonck, J., Langer, J. D., Salzer, R. & Averhoff, B. Unusual N-terminal ααβαββα fold of PilQ from Thermus thermophilus mediates ring formation and is essential for piliation. J. Biol. Chem. 287, 8484–8494 (2012). · DOI
- Collins, R. F., Davidsen, L., Derrick, J. P., Ford, R. C. & Tønjum, T. Analysis of the PilQ Secretin from Neisseria meningitidis by transmission electron microscopy reveals a dodecameric quaternary structure. J. Bacteriol. 183, 3825–3832 (2001). · DOI
- Collins, R. F. et al. Three-dimensional structure of the Neisseria meningitidis secretin PilQ determined from negative-stain transmission electron microscopy. J. Bacteriol. 185, 2611–2617 (2003). · DOI
- Collins, R. F. et al. Structure of the Neisseria meningitidis outer membrane PilQ secretin complex at 12 Å resolution. J. Biol. Chem. 279, 39750–39756 (2004). · DOI
- Collins, R. F. et al. Interaction with type IV Pili induces structural changes in the bacterial outer membrane secretin PilQ. J. Biol. Chem. 280, 18923–18930 (2005). · DOI
- Burkhardt, J., Vonck, J. & Averhoff, B. Structure and function of PilQ, a secretin of the DNA transporter from the thermophilic bacterium Thermus thermophilus HB27. J. Biol. Chem. 286, 9977–9984 (2011). · DOI
- Balasingham, S. V. et al. Interactions between the lipoprotein PilP and the Secretin PilQ in Neisseria meningitidis. J. Bacteriol. 189, 5716–5727 (2007). · DOI
- Berry, J.-L. et al. Structure and assembly of a trans-periplasmic channel for type IV Pili in Neisseria meningitidis. PLOS Pathog. 8, e1002923 (2012). · DOI
- Koo, J., Lamers, R. P., Rubinstein, J. L., Burrows, L. L. & Howell, L. P. Structure of the Pseudomonas aeruginosa type IVa pilus secretin at 7.4 Å. Structure 24, 1778–1787 (2016). · DOI
- D’Imprima, E. et al. Cryo-EM structure of the bifunctional secretin complex of Thermus thermophilus. eLife 6, e30483 (2017). · DOI
- Bitter, W., Koster, M., Latijnhouwers, M., Cock, H. & Tommassen, J. Formation of oligomeric rings by XcpQ and PilQ, which are involved in protein transport across the outer membrane of Pseudomonas aeruginosa. Mol. Microbiol. 27, 209–219 (1998). · DOI
- Chang, Y. -W. et al. Architecture of the type IVa pilus machine. Science 351, aad2001 (2016). · DOI
- Chang, Y. -W. et al. Architecture of the Vibrio cholerae toxin-coregulated pilus machine revealed by electron cryotomography. Nat. Microbiol. 2, 16269 (2017). · DOI
- Gold, V. A., Salzer, R., Averhoff, B. & Kühlbrandt, W. Structure of a type IV pilus machinery in the open and closed state. eLife 4, e07380 (2015). · DOI
- Jain, S. et al. Structural characterization of outer membrane components of the type IV pili system in pathogenic Neisseria. PLoS ONE 6, e16624 (2011). · DOI
- Tarry, M. et al. The extra-membranous domains of the competence protein HofQ show dna binding, flexibility and a shared fold with type I KH domains. J. Mol. Biol. 409, 642–653 (2011). · DOI
- Lieberman, J. A. et al. Outer membrane targeting, ultrastructure, and single molecule localization of the enteropathogenic Escherichia coli type IV pilus secretin BfpB. J. Bacteriol. 194, 1646–1658 (2012). · DOI
- Yan, Z., Yin, M., Xu, D., Zhu, Y. & Li, X. Structural insights into the secretin translocation channel in the type II secretion system. Nat. Struct. Mol. Biol. 24, 177–183 (2017). · DOI
- Hay, I. D., Belousoff, M. J., Dunstan, R. A., Bamert, R. S. & Lithgow, T. Structure and membrane topography of the vibrio-type secretin complex from the type 2 secretion system of enteropathogenic. Escherichia coli. J. Bacteriol. 200, e00521–17 (2018).
- Yin, M., Yan, Z. & Li, X. Structural insight into the assembly of the type II secretion system pilotin–secretin complex from enterotoxigenic Escherichia coli. Nat. Microbiol. 3, 581–587 (2018). · DOI
- Hay, I. D., Belousoff, M. J. & Lithgow, T. Structural basis of type 2 secretion system engagement between the inner and outer bacterial membranes. mBio 8, e01344-17 (2017). · DOI
- Chernyatina, A. A. & Low, H. H. Core architecture of a bacterial type II secretion system. Nat. Commun. 10, 1–10 (2019). · DOI
- Howard, P. S. et al. Structure and assembly of pilotin-dependent and -independent secretins of the type II secretion system. PLOS Pathog. 15, e1007731 (2019). · DOI
- Worrall, L. et al. Near-atomic-resolution cryo-EM analysis of the Salmonella T3S injectisome basal body. Nature 540, 597 (2016). · DOI
- McCallum, M., Tammam, S., Rubinstein, J. L., Burrows, L. L. & Howell, P. L. TsaP binds PilQ and is involved in cyclic di-GMP signaling. Preprint at https://www.biorxiv.org/content/10.1101/2020.05.29.123786v1 (2020). · DOI
- Lo Scrudato, M. & Blokesch, M. A transcriptional regulator linking quorum sensing and chitin induction to render Vibrio cholerae naturally transformable. Nucleic Acids Res. 41, 3644–3658 (2013). · DOI
- Dalia, A. B., McDonough, E. & Camilli, A. Multiplex genome editing by natural transformation. Proc. Natl. Acad. Sci. U.S.A. 111, 8937–8942 (2014). · DOI
- Chami, M. et al. Structural insights into the secretin PulD and its trypsin-resistant core. J. Biol. Chem. 280, 37732–37741 (2005). · DOI
- Guilvout, I., Nickerson, N. N., Chami, M. & Pugsley, A. P. Multimerization-defective variants of dodecameric secretin PulD. Res. Microbiol. 162, 180–190 (2011). · DOI
- Tan, Y. et al. Addressing preferred specimen orientation in single-particle cryo-EM through tilting. Nat. Methods 14, 793–796 (2017). · DOI
- Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nat. Methods 11, 63–65 (2014). · DOI
- Rocaboy, M. et al. The crystal structure of the cell division amidase AmiC reveals the fold of the AMIN domain, a new peptidoglycan binding domain. Mol. Microbiol. 90, 267–277 (2013). · DOI
- de Souza, R. F., Anantharaman, V., de Souza, S. J., Aravind, L. & Gueiros-Filho, F. J. AMIN domains have a predicted role in localization of diverse periplasmic protein complexes. Bioinformatics 24, 2423–2426 (2008). · DOI
- Ghosal, D. et al. In vivo structure of the Legionella type II secretion system by electron cryotomography. Nat. Microbiol. 4, 2101–2108 (2019). · DOI
- Dombkowski, A. A. Disulfide by design: a computational method for the rational design of disulfide bonds in proteins. Bioinformatics 19, 1852–1853 (2003). · DOI
- Craig, D. B. & Dombkowski, A. A. Disulfide by Design 2.0: a web-based tool for disulfide engineering in proteins. BMC Bioinform. 14, 346 (2013). · DOI
- Dombkowski, A. A., Sultana, K. Z. & Craig, D. B. Protein disulfide engineering. FEBS Lett. 588, 206–212 (2014). · DOI
- Ellison, C. K., Dalia, T. N., Dalia, A. B. & Brun, Y. V. Real-time microscopy and physical perturbation of bacterial pili using maleimide-conjugated molecules. Nat. Protoc. 14, 1–17 (2019). · DOI
- Ellison, C. K. et al. Obstruction of pilus retraction stimulates bacterial surface sensing. Science 358, 535–538 (2017). · DOI
- Denise, R., Abby, S. S. & Rocha, E. P. C. Diversification of the type IV filament superfamily into machines for adhesion, protein secretion, DNA uptake, and motility. PLOS Biol. 17, e3000390 (2019). · DOI
- Craig, L., Pique, M. E. & Tainer, J. A. Type IV pilus structure and bacterial pathogenicity. Nat. Rev. Microbiol. 2, 363 (2004). · DOI
- Plant, L. J. & Jonsson, A.-B. Type IV pili of Neisseria gonorrhoeae influence the activation of human CD4+ T cells. Infect. Immun. 74, 442–448 (2006). · DOI
- Friedrich, A., Prust, C., Hartsch, T., Henne, A. & Averhoff, B. Molecular analyses of the natural transformation machinery and identification of pilus structures in the extremely thermophilic bacterium Thermus thermophilus strain HB27. Appl. Environ. Microbiol. 68, 745–755 (2002). · DOI
- Martin, P. R., Hobbs, M., Free, P. D., Jeske, Y. & Mattick, J. S. Characterization of pilQ, a new gene required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa. Mol. Microbiol. 9, 857–868 (1993). · DOI
- Parkhill, J. et al. Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 404, 502–506 (2000). · DOI
- Mattick, J. S., Whitchurch, C. B. & Alm, R. A. The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa—a review. Gene 179, 147–155 (1996). · DOI
- Ropp, P. A. & Nicholas, R. A. Cloning and characterization of the ponA gene encoding penicillin-binding protein 1 from Neisseria gonorrhoeae and Neisseria meningitidis. J. Bacteriol. 179, 2783–2787 (1997). · DOI
- Wall, D., Kolenbrander, P. E. & Kaiser, D. The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility, and development. J. Bacteriol. 181, 24–33 (1999). · DOI
- Palchevskiy, V. & Finkel, S. E. Escherichia coli competence gene homologs are essential for competitive fitness and the use of DNA as a nutrient. J. Bacteriol. 188, 3902–3910 (2006). · DOI
- Sauvage, E., Kerff, F., Terrak, M., Ayala, J. A. & Charlier, P. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol. Rev. 32, 234–258 (2008). · DOI
- Merz, A. J., So, M. & Sheetz, M. P. Pilus retraction powers bacterial twitching motility. Nature 407, 98–102 (2000). · DOI
- Skerker, J. M. & Berg, H. C. Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. U.S.A. 98, 6901–6904 (2001). · DOI
- Wolfgang, M. et al. PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol. Microbiol. 29, 321–330 (1998). · DOI
- Salleh, M. Z. et al. Structure and properties of a natural competence-associated pilin suggest a unique pilus tip-associated DNA receptor. mBio 10, e00614–e00619 (2019). · DOI
- Craig, L. et al. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol. Cell 23, 651–662 (2006). · DOI
- Neuhaus, A. et al. Cryo-electron microscopy reveals two distinct type IV pili assembled by the same bacterium. Nat. Commun. 11, 2231 (2020). · DOI
- Kruse, K., Salzer, R., Joos, F. & Averhoff, B. Functional dissection of the three N-terminal general secretory pathway domains and the Walker motifs of the traffic ATPase PilF from Thermus thermophilus. Extremophiles 22, 461–471 (2018). · DOI
- Seitz, P. et al. ComEA is essential for the transfer of external DNA into the periplasm in naturally transformable Vibrio cholerae cells. PLOS Genet. 10, e1004066 (2014). · DOI
- Kolappan, S. et al. Structure of the Neisseria meningitidis type IV pilus. Nat. Commun. 7, 13015 (2016). · DOI
- Wang, F. et al. Cryoelectron microscopy reconstructions of the Pseudomonas aeruginosa and Neisseria gonorrhoeae type IV pili at sub-nanometer resolution. Structure 25, 1423–1435.e4 (2017). · DOI
- Bardiaux, B. et al. Structure and assembly of the enterohemorrhagic Escherichia coli type 4 pilus. Structure 27, 1082–1093.e5 (2019). · DOI
- Pugsley, A. P. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57, 50–108 (1993). · DOI
- Russel, M. Macromolecular assembly and secretion across the bacterial cell envelope: type II protein secretion systems. J. Mol. Biol. 279, 485–499 (1998). · DOI
- Wehbi, H. et al. The peptidoglycan-binding protein FimV promotes assembly of the Pseudomonas aeruginosa iype IV pilus secretin. J. Bacteriol. 193, 540–550 (2011). · DOI
- Siewering, K. et al. Peptidoglycan-binding protein TsaP functions in surface assembly of type IV pili. Proc. Natl. Acad. Sci. U.S.A. 111, E953–E961 (2014). · DOI
- Carter, T. et al. The type IVa pilus machinery is recruited to sites of future cell division. mBio 8, e02103–e02116 (2017). · DOI
- Miller, V. L., DiRita, V. J. & Mekalanos, J. J. Identification of toxS, a regulatory gene whose product enhances toxR-mediated activation of the cholera toxin promoter. J. Bacteriol. 171, 1288–1293 (1989). · DOI
- Dalia, A. B. Natural cotransformation and multiplex genome editing by natural transformation (MuGENT) of Vibrio cholerae. in Vibrio Cholerae: Methods and Protocols (ed. Sikora, A. E.) 53–64 (Springer, 2018). · DOI
- Zhu, J. et al. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. U.S.A. 99, 3129–3134 (2002). · DOI
- Dalia, T. N., Chlebek, J. L. & Dalia, A. B. A modular chromosomally integrated toolkit for ectopic gene expression in Vibrio cholerae. Sci. Rep. 10, 15398 (2020). · DOI
- Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36–51 (2005). · DOI
- Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017). · DOI
- Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216–221 (2015). · DOI
- Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017). · DOI · Paper page
- Kimanius, D., Forsberg, B. O. O., Scheres, S. H. & Lindahl, E. Accelerated cryo-EM structure determination with parallelisation using GPUs in RELION-2. eLife 5, e18722 (2016). · DOI
- Zivanov, J. et al. New tools for automated high-resolution cryo-EM structure determination in RELION-3. eLife 7, e42166 (2018). · DOI
- Zivanov, J., Nakane, T. & Scheres, S. H. W. Estimation of high-order aberrations and anisotropic magnification from cryo-EM datasets in RELION-3.1. IUCrJ 7, 253–267 (2020). · DOI
- Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Cryst. D 62, 1002–1011 (2006). · DOI
- Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of coot. Acta Cryst. D 66, 486–501 (2010). · DOI · Paper page
- Roy, A., Kucukural, A. & Zhang, Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725–738 (2010). · DOI
- Yang, J. et al. The I-TASSER suite: protein structure and function prediction. Nat. Methods 12, 7–8 (2015). · DOI · Paper page
- Zhang, Y. I-TASSER server for protein 3D structure prediction. BMC Bioinform. 9, 40 (2008).
- Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Cryst. D 66, 213–221 (2010). · DOI · Paper page
- Barad, B. A. et al. EMRinger: side chain-directed model and map validation for 3D cryo-electron microscopy. https://doi.org/10.1038/nmeth.3541 (2015). · DOI · Paper page
- Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Cryst. D 66, 12–21 (2010). · DOI · Paper page
- Hu, J. et al. Cryo-EM analysis of the T3S injectisome reveals the structure of the needle and open secretin. Nat. Commun. 9, 1–11 (2018). · DOI · Paper page
- Pettersen, E. F. et al. UCSF chimera—a visualization system for exploratory research and analysis. J. Computational Chem. 25, 1605–1612 (2004). · DOI
- Meng, E. C., Pettersen, E. F., Couch, G. S., Huang, C. C. & Ferrin, T. E. Tools for integrated sequence-structure analysis with UCSF chimera. BMC Bioinform. 7, 339 (2006).
- Lomize, M. A., Pogozheva, I. D., Joo, H., Mosberg, H. I. & Lomize, A. L. OPM database and PPM web server: resources for positioning of proteins in membranes. Nucleic Acids Res. 40, D370–D376 (2012). · DOI
- Cox, J. et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794–1805 (2011). · DOI
- Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008). · DOI · Paper page
- Gumerov, V. M., Ortega, D. R., Adebali, O., Ulrich, L. E. & Zhulin, I. B. MiST 3.0: an updated microbial signal transduction database with an emphasis on chemosensory systems. Nucleic Acids Res. 48, D459–D464 (2020). · DOI
- El-Gebali, S. et al. The Pfam protein families database in 2019. Nucleic Acids Res. 47, D427–D432 (2019). · DOI · Paper page
- Finn, R. D., Clements, J. & Eddy, S. R. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39, W29–W37 (2011). · DOI · Paper page
- Li, W., Jaroszewski, L. & Godzik, A. Clustering of highly homologous sequences to reduce the size of large protein databases. Bioinformatics 17, 282–283 (2001). · DOI
- Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinform. 10, 1–9 (2009). · DOI · Paper page
- Katoh, K. & Toh, H. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 9, 286–298 (2008). · DOI
- Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. & Barton, G. J. Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009). · DOI
- Gumerov, V. M. & Zhulin, I. B. TREND: a platform for exploring protein function in prokaryotes based on phylogenetic, domain architecture and gene neighborhood analyses. Nucleic Acids Res. 48, W72–W76 (2020). · DOI
- Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014). · DOI · Paper page
- Adebali, O., Ortega, D. R. & Zhulin, I. B. CDvist: a webserver for identification and visualization of conserved domains in protein sequences. Bioinformatics 31, 1475–1477 (2015). · DOI
- Jurrus, E. et al. Improvements to the APBS biomolecular solvation software suite. Protein Sci. 27, 112–128 (2018). · DOI
Metadata
- Authors
- Weaver, S. J., Ortega, D. R., Sazinsky, M. H., Dalia, T. N., Dalia, A. B., & Jensen, G. J.
- Affiliations
- California Institute of Technology (US)
- Pomona College (US)
- Indiana University Bloomington (US)
- Corresponding author
- Jensen, Grant J.
- ORCID
- Venue
- Nature Communications
- Published
- 2020-10-08
- Volume
- 11
- Issue
- 1
- Pages
- 5080-5080
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC7545093
- OpenAlex
- W3092186467
- Cited by
- 37
- References
- 1
- Citations by year
- 2026: 7 · 2025: 6 · 2024: 5 · 2023: 7 · 2022: 6 · 2021: 4 · 2020: 2
- FWCI
- 1.94
- Type
- journal article
- Language
- en
- Update notices
- correction (2020-10-27)
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion, cc-by-nc-nd)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- U.S. Department of Health & Human Services | National Institutes of Health (R35GM128674, AI127401)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
- Keywords
- Vibrio cholerae, natural competence, natural transformation, horizontal gene transfer, DNA uptake, antibiotic resistance spread, druggable targets, Proteobacteria
- MeSH terms
- Protein Domains, Cysteine, Membrane Proteins, Models, Molecular, Mutation, Phylogeny, Fimbriae, Bacterial, Secretin, Transformation, Bacterial, Vibrio cholerae, Cryoelectron Microscopy, Bacterial Secretion Systems
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