Convergent Evolution of Hyperswarming Leads to Impaired Biofilm Formation in Pathogenic Bacteria

Cell Reports - Tập 4 - Trang 697-708 - 2013
Dave van Ditmarsch1, Kerry E. Boyle1, Hassan Sakhtah2, Jennifer E. Oyler1, Carey D. Nadell3, Éric Déziel4, Lars E.P. Dietrich2, Joao B. Xavier1
1Program in Computational Biology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10065, USA
2Department of Biological Sciences, Columbia University, 1108 Fairchild Center, 1212 Amsterdam Avenue, Mail Code 2418, New York, NY 10027, USA
3Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA
4INRS-Institut Armand-Frappier, 531 Boulevard des Prairies, Laval, QC H7V 1B7, Canada

Tài liệu tham khảo

Balaban, 2011, Polar flagellar biosynthesis and a regulator of flagellar number influence spatial parameters of cell division in Campylobacter jejuni, PLoS Pathog., 7, e1002420, 10.1371/journal.ppat.1002420 Baraquet, 2012, The FleQ protein from Pseudomonas aeruginosa functions as both a repressor and an activator to control gene expression from the pel operon promoter in response to c-di-GMP, Nucleic Acids Res., 40, 7207, 10.1093/nar/gks384 Bennett, 2007, An experimental test of evolutionary trade-offs during temperature adaptation, Proc. Natl. Acad. Sci. USA, 104, 8649, 10.1073/pnas.0702117104 Blount, 2008, Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli, Proc. Natl. Acad. Sci. USA, 105, 7899, 10.1073/pnas.0803151105 Boles, 2005, Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms, Mol. Microbiol., 57, 1210, 10.1111/j.1365-2958.2005.04743.x Boyle, 2013, Exploiting social evolution in biofilms, Curr. Opin. Microbiol., 16, 207, 10.1016/j.mib.2013.01.003 Breidenstein, 2012, The Lon protease is essential for full virulence in Pseudomonas aeruginosa, PLoS One, 7, e49123, 10.1371/journal.pone.0049123 Caiazza, 2005, Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa, J. Bacteriol., 187, 7351, 10.1128/JB.187.21.7351-7361.2005 Caiazza, 2007, Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14, J. Bacteriol., 189, 3603, 10.1128/JB.01685-06 Cattoir, 2013, Transcriptional response of mucoid Pseudomonas aeruginosa to human respiratory mucus, MBio, 3, e00410 Chou, 2012, Optimization of gene expression through divergent mutational paths, Cell Rep., 1, 133, 10.1016/j.celrep.2011.12.003 Chou, 2011, Diminishing returns epistasis among beneficial mutations decelerates adaptation, Science, 332, 1190, 10.1126/science.1203799 Christin, 2010, Causes and evolutionary significance of genetic convergence, Trends Genet., 26, 400, 10.1016/j.tig.2010.06.005 Costerton, 1999, Bacterial biofilms: a common cause of persistent infections, Science, 284, 1318, 10.1126/science.284.5418.1318 Dasgupta, 2001, Interaction of the antiactivator FleN with the transcriptional activator FleQ regulates flagellar number in Pseudomonas aeruginosa, J. Bacteriol., 183, 6636, 10.1128/JB.183.22.6636-6644.2001 Dasgupta, 2000, fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa, J. Bacteriol., 182, 357, 10.1128/JB.182.2.357-364.2000 Dasgupta, 2003, A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa, Mol. Microbiol., 50, 809, 10.1046/j.1365-2958.2003.03740.x David, 2011, Rapid evolutionary innovation during an Archaean genetic expansion, Nature, 469, 93, 10.1038/nature09649 Deziel, 1996, Biosurfactant production by a soil pseudomonas strain growing on polycyclic aromatic hydrocarbons, Appl. Environ. Microbiol., 62, 1908, 10.1128/AEM.62.6.1908-1912.1996 Déziel, 2003, rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids, Microbiology, 149, 2005, 10.1099/mic.0.26154-0 Dietrich, 2006, The co-evolution of life and Earth, Curr. Biol., 16, R395, 10.1016/j.cub.2006.05.017 Ensminger, 2012, Experimental evolution of Legionella pneumophila in mouse macrophages leads to strains with altered determinants of environmental survival, PLoS Pathog., 8, e1002731, 10.1371/journal.ppat.1002731 Herring, 2006, Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale, Nat. Genet., 38, 1406, 10.1038/ng1906 Heydorn, 2000, Quantification of biofilm structures by the novel computer program COMSTAT, Microbiology, 146, 2395, 10.1099/00221287-146-10-2395 Hibbing, 2010, Bacterial competition: surviving and thriving in the microbial jungle, Nat. Rev. Microbiol., 8, 15, 10.1038/nrmicro2259 Jensen, 2007, Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa, Microbiology, 153, 1329, 10.1099/mic.0.2006/003863-0 Kasting, 2002, Life and the evolution of Earth’s atmosphere, Science, 296, 1066, 10.1126/science.1071184 Kazmierczak, 2013, Spatial and numerical regulation of flagellar biosynthesis in polarly flagellated bacteria, Mol. Microbiol., 88, 655, 10.1111/mmi.12221 Kearns, 2010, A field guide to bacterial swarming motility, Nat. Rev. Microbiol., 8, 634, 10.1038/nrmicro2405 Köhler, 2000, Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili, J. Bacteriol., 182, 5990, 10.1128/JB.182.21.5990-5996.2000 Kolter, 2006, Microbial sciences: the superficial life of microbes, Nature, 441, 300, 10.1038/441300a Kuchma, 2007, BifA, a cyclic-Di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14, J. Bacteriol., 189, 8165, 10.1128/JB.00586-07 Kuchma, 2010, Cyclic-di-GMP-mediated repression of swarming motility by Pseudomonas aeruginosa: the pilY1 gene and its impact on surface-associated behaviors, J. Bacteriol., 192, 2950, 10.1128/JB.01642-09 Kusumoto, 2006, Regulation of polar flagellar number by the flhF and flhG genes in Vibrio alginolyticus, J. Biochem., 139, 113, 10.1093/jb/mvj010 Lai, 2009, Swarming motility: a multicellular behaviour conferring antimicrobial resistance, Environ. Microbiol., 11, 126, 10.1111/j.1462-2920.2008.01747.x Lambertsen, 2004, Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins, Environ. Microbiol., 6, 726, 10.1111/j.1462-2920.2004.00605.x Lanzer, 1988, Promoters largely determine the efficiency of repressor action, Proc. Natl. Acad. Sci. USA, 85, 8973, 10.1073/pnas.85.23.8973 Lee, 2007, A cyclic-di-GMP receptor required for bacterial exopolysaccharide production, Mol. Microbiol., 65, 1474, 10.1111/j.1365-2958.2007.05879.x Lenski, 1993, Evolutionary response of Escherichia coli to thermal stress, Am. Nat., 142, S47, 10.1086/285522 Lenski, 1991, Long-term experimental evolution in Escherichia coli. 1. Adaptation and divergence during 2,000 generations, Am. Nat., 138, 1315, 10.1086/285289 Lequette, 2005, Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms, J. Bacteriol., 187, 37, 10.1128/JB.187.1.37-44.2005 Lieberman, 2011, Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes, Nat. Genet., 43, 1275, 10.1038/ng.997 Maynard, 2010, A forward-genetic screen and dynamic analysis of lambda phage host-dependencies reveals an extensive interaction network and a new anti-viral strategy, PLoS Genet., 6, e1001017, 10.1371/journal.pgen.1001017 McKenna, 2010, The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data, Genome Res., 20, 1297, 10.1101/gr.107524.110 Mitri, 2011, Social evolution in multispecies biofilms, Proc. Natl. Acad. Sci. USA, 108, 10839, 10.1073/pnas.1100292108 Morris, 2011, Imaging and analysis of Pseudomonas aeruginosa swarming and rhamnolipid production, Appl. Environ. Microbiol., 77, 8310, 10.1128/AEM.06644-11 Murray, 2006, FlhF is required for swimming and swarming in Pseudomonas aeruginosa, J. Bacteriol., 188, 6995, 10.1128/JB.00790-06 Murray, 2010, Swarming motility, secretion of type 3 effectors and biofilm formation phenotypes exhibited within a large cohort of Pseudomonas aeruginosa clinical isolates, J. Med. Microbiol., 59, 511, 10.1099/jmm.0.017715-0 Nadell, 2011, A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms, Proc. Natl. Acad. Sci. USA, 108, 14181, 10.1073/pnas.1111147108 Nadell, 2010, Emergence of spatial structure in cell groups and the evolution of cooperation, PLoS Comput. Biol., 6, e1000716, 10.1371/journal.pcbi.1000716 Oliver, 2000, High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection, Science, 288, 1251, 10.1126/science.288.5469.1251 O’Toole, 1998, Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development, Mol. Microbiol., 30, 295, 10.1046/j.1365-2958.1998.01062.x Pandza, 2000, The G-protein FlhF has a role in polar flagellar placement and general stress response induction in Pseudomonas putida, Mol. Microbiol., 36, 414, 10.1046/j.1365-2958.2000.01859.x Perfeito, 2007, Adaptive mutations in bacteria: high rate and small effects, Science, 317, 813, 10.1126/science.1142284 Rashid, 2000, Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa, Proc. Natl. Acad. Sci. USA, 97, 4885, 10.1073/pnas.060030097 Schniederberend, 2013, The GTPase activity of FlhF is dispensable for flagellar localization, but not motility, in Pseudomonas aeruginosa, J. Bacteriol., 195, 1051, 10.1128/JB.02013-12 Shanks, 2006, Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria, Appl. Environ. Microbiol., 72, 5027, 10.1128/AEM.00682-06 Shoval, 2012, Evolutionary trade-offs, Pareto optimality, and the geometry of phenotype space, Science, 336, 1157, 10.1126/science.1217405 Shrout, 2006, The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional, Mol. Microbiol., 62, 1264, 10.1111/j.1365-2958.2006.05421.x Smidt, 2004, Anaerobic microbial dehalogenation, Annu. Rev. Microbiol., 58, 43, 10.1146/annurev.micro.58.030603.123600 Smith, 2006, Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients, Proc. Natl. Acad. Sci. USA, 103, 8487, 10.1073/pnas.0602138103 Snitkin, 2012, Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing, Sci. Transl. Med., 4, 10.1126/scitranslmed.3004129 Takahashi, 2008, Swarming of Pseudomonas aeruginosa PAO1 without differentiation into elongated hyperflagellates on hard agar minimal medium, FEMS Microbiol. Lett., 280, 169, 10.1111/j.1574-6968.2007.01057.x Taubes, 2008, The bacteria fight back, Science, 321, 356, 10.1126/science.321.5887.356 Taylor, 2011, Selection experiments reveal trade-offs between swimming and twitching motilities in Pseudomonas aeruginosa, Evolution, 65, 3060, 10.1111/j.1558-5646.2011.01376.x Tenaillon, 2012, The molecular diversity of adaptive convergence, Science, 335, 457, 10.1126/science.1212986 Tremblay, 2008, Improving the reproducibility of Pseudomonas aeruginosa swarming motility assays, J. Basic Microbiol., 48, 509, 10.1002/jobm.200800030 Tremblay, 2010, Gene expression in Pseudomonas aeruginosa swarming motility, BMC Genomics, 11, 587, 10.1186/1471-2164-11-587 Tremblay, 2007, Self-produced extracellular stimuli modulate the Pseudomonas aeruginosa swarming motility behaviour, Environ. Microbiol., 9, 2622, 10.1111/j.1462-2920.2007.01396.x van Ditmarsch, 2011, High-resolution time series of Pseudomonas aeruginosa gene expression and rhamnolipid secretion through growth curve synchronization, BMC Microbiol., 11, 140, 10.1186/1471-2180-11-140 Weigand, 2012, General and inducible hypermutation facilitate parallel adaptation in Pseudomonas aeruginosa despite divergent mutation spectra, Proc. Natl. Acad. Sci. USA, 109, 13680, 10.1073/pnas.1205357109 Winsor, 2011, Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes, Nucleic Acids Res., 39, D596, 10.1093/nar/gkq869 Woods, 2006, Tests of parallel molecular evolution in a long-term experiment with Escherichia coli, Proc. Natl. Acad. Sci. USA, 103, 9107, 10.1073/pnas.0602917103 Wyckoff, 2002, Static growth of mucoid Pseudomonas aeruginosa selects for non-mucoid variants that have acquired flagellum-dependent motility, Microbiology, 148, 3423, 10.1099/00221287-148-11-3423 Xavier, 2007, Cooperation and conflict in microbial biofilms, Proc. Natl. Acad. Sci. USA, 104, 876, 10.1073/pnas.0607651104 Xavier, 2009, Social evolution of spatial patterns in bacterial biofilms: when conflict drives disorder, Am. Nat., 174, 1, 10.1086/599297 Xavier, 2011, A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa, Mol. Microbiol., 79, 166, 10.1111/j.1365-2958.2010.07436.x Xie, 2011, Statistical image analysis reveals features affecting fates of Myxococcus xanthus developmental aggregates, Proc. Natl. Acad. Sci. USA, 108, 5915, 10.1073/pnas.1018383108 Yang, 2011, Evolutionary dynamics of bacteria in a human host environment, Proc. Natl. Acad. Sci. USA, 108, 7481, 10.1073/pnas.1018249108 Yeung, 2009, Swarming of Pseudomonas aeruginosa is controlled by a broad spectrum of transcriptional regulators, including MetR, J. Bacteriol., 191, 5592, 10.1128/JB.00157-09 Yeung, 2011, The sensor kinase CbrA is a global regulator that modulates metabolism, virulence, and antibiotic resistance in Pseudomonas aeruginosa, J. Bacteriol., 193, 918, 10.1128/JB.00911-10 Yeung, 2012, Mucin promotes rapid surface motility in Pseudomonas aeruginosa, MBio, 3, 10.1128/mBio.00073-12 Zhen, 2012, Parallel molecular evolution in an herbivore community, Science, 337, 1634, 10.1126/science.1226630