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Pseudomonas aeruginosa Pangenome: Core and Accessory Genes of a Highly Resourceful Opportunistic Pathogen

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Pseudomonas aeruginosa

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1386))

Abstract

In this chapter, we leverage a novel approach to assess the seamless population structure of Pseudomonas aeruginosa, using the full repertoire of genomes sequenced to date (GenBank, April 6, 2020). In order to assess the set of core functions that represents the species as well as the differences in these core functions among the phylogroups observed in the population structure analysis, we performed pangenome analyses at the species level and at the phylogroup level. The existence of the phylogroups described in the population structure analyses was supported by their different profiles of antibiotic-resistant determinants. Finally, we utilized a presence/absence matrix of protein families from the entire species to evaluate if P. aeruginosa phylogroups can be differentiated according to their accessory genomic content. Our analysis shows that the core genome of P. aeruginosa is approximately 62% of the average gene content for the species, and it is highly enriched with pathways related to the metabolism of carbohydrates and amino acids as well as cellular processes and cell maintenance. The analysis of the accessory genome of P. aeruginosa performed in this chapter confirmed not only the existence of the three phylogroups previously described in the population structure analysis, but also of 29 genetic substructures (subgroups) within the main phylogroups. Our work illustrates the utility of populations genomics pipelines to better understand highly complex bacterial species such as P. aeruginosa.

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References

  • Abram KZ, Udaondo Z (2018) Towards a better metabolic engineering reference: the microbial chassis. J Microbial Biotechnol 13:17–18

    Article  Google Scholar 

  • Abram K, Udaondo Z, Bleker C, Wanchai V, Wassenaar TM, Robeson MS, Ussery DW (2021) Mash-based analyses of Escherichia coli genomes reveal 14 distinct phylogroups. Commun Biol 4:1–12

    Article  Google Scholar 

  • Acar Kirit H, Lagator M, Bollback JP (2020) Experimental determination of evolutionary barriers to horizontal gene transfer. BMC Microbiol 20:326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Achtman M, den Broeck FV, Cooper KK, Lemey P, Parker CT, Zhou Z, The A.S Group (2021) Genomic population structure associated with repeated escape of Salmonella enterica ATCC14028s from the laboratory into nature. PLoS Genet 17:e1009820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aendekerk S, Diggle SP, Song Z, Høiby N, Cornelis P, Williams P, Cámara M (2005) The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication. Microbiology (Reading) 151:1113–1125

    Article  CAS  Google Scholar 

  • Aguilar-Rodea P, Zúñiga G, Rodríguez-Espino BA, Olivares Cervantes AL, Gamiño Arroyo AE, Moreno-Espinosa S et al (2017) Identification of extensive drug resistant Pseudomonas aeruginosa strains: new clone ST1725 and high-risk clone ST233. PLoS One 12:e0172882

    Article  PubMed  PubMed Central  Google Scholar 

  • Aherfi S, Pagnier I, Fournous G, Raoult D, La Scola B, Colson P (2013) Complete genome sequence of Cannes 8 virus, a new member of the proposed family “Marseilleviridae”. Virus Genes 47:550–555

    Article  CAS  PubMed  Google Scholar 

  • Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M, Edalatmand A et al (2020) CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 48:D517–D525

    CAS  PubMed  Google Scholar 

  • Alvarez-Ortega C, Wiegand I, Olivares J, Hancock REW, Martínez JL (2011) The intrinsic resistome of Pseudomonas aeruginosa to β-lactams. Virulence 2:144–146

    Article  PubMed  Google Scholar 

  • Andam C, Challagundla L, Azarian T, Hanage W, Robinson D (2017) Population structure of pathogenic bacteria. Genet Evol Infect Dis 51–70

    Google Scholar 

  • Arai H (2011) Regulation and function of versatile aerobic and anaerobic respiratory metabolism in Pseudomonas aeruginosa. Front Microbiol 2

    Google Scholar 

  • Argimón S, Abudahab K, Goater RJE, Fedosejev A, Bhai J, Glasner C, Feil EJ, Holden MTG, Yeats CA, Grundmann H, Spratt BG, Aanensen DM (2016) Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microb Genom 2(11):e000093. https://doi.org/10.1099/mgen.0.000093

    Article  PubMed  PubMed Central  Google Scholar 

  • Azarian T, Huang I-T, Hanage WP (2020) Structure and dynamics of bacterial populations: pangenome ecology. In: Tettelin H, Medini D (eds) The pangenome: diversity, dynamics and evolution of genomes. Springer, Cham

    Google Scholar 

  • Azimi S, Kafil HS, Baghi HB, Shokrian S, Najaf K, Asgharzadeh M et al (2016) Presence of exoY, exoS, exoU and exoT genes, antibiotic resistance and biofilm production among Pseudomonas aeruginosa isolates in Northwest Iran. GMS Hyg Infect Control 11:Doc04

    PubMed  PubMed Central  Google Scholar 

  • Beharry Z, Palzkill T (2005) Functional analysis of active site residues of the fosfomycin resistance enzyme FosA from Pseudomonas aeruginosa. J Biol Chem 280:17786–17791

    Article  CAS  PubMed  Google Scholar 

  • Bell SC, Mall MA, Gutierrez H, Macek M, Madge S, Davies JC et al (2020) The future of cystic fibrosis care: a global perspective. Lancet Respir Med 8:65–124

    Article  CAS  PubMed  Google Scholar 

  • Botelho J, Grosso F, Peixe L (2019) Antibiotic resistance in Pseudomonas aeruginosa – Mechanisms, epidemiology and evolution. Drug Resist Updat 44:100640

    Article  PubMed  Google Scholar 

  • Cao J, Schneeberger K, Ossowski S, Günther T, Bender S, Fitz J et al (2011) Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 43:956–963

    Article  CAS  PubMed  Google Scholar 

  • Castañeda-Montes FJ, Avitia M, Sepúlveda-Robles O, Cruz-Sánchez V, Kameyama L, Guarneros G, Escalante AE (2018) Population structure of Pseudomonas aeruginosa through a MLST approach and antibiotic resistance profiling of a Mexican clinical collection. Infect Genet Evol 65:43–54

    Article  PubMed  Google Scholar 

  • Clark ST, Diaz Caballero J, Cheang M, Coburn B, Wang PW, Donaldson SL et al (2015) Phenotypic diversity within a Pseudomonas aeruginosa population infecting an adult with cystic fibrosis. Sci Rep 5:10932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coradini ALV, Hull CB, Ehrenreich IM (2020) Building genomes to understand biology. Nat Commun 11:6177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cox G, Wright GD (2013) Intrinsic antibiotic resistance: mechanisms, origins, challenges and solutions. Int J Med Microbiol 303:287–292

    Article  CAS  PubMed  Google Scholar 

  • Croucher NJ, Coupland PG, Stevenson AE, Callendrello A, Bentley SD, Hanage WP (2014) Diversification of bacterial genome content through distinct mechanisms over different timescales. Nat Commun 5:5471

    Article  PubMed  Google Scholar 

  • Danchin EGJ, Arguel M-J, Campan-Fournier A, Perfus-Barbeoch L, Magliano M, Rosso M-N et al (2013) Identification of novel target genes for safer and more specific control of root-knot nematodes from a pan-genome mining. PLoS Pathog 9:e1003745

    Article  PubMed  PubMed Central  Google Scholar 

  • D’Auria G, Jiménez-Hernández N, Peris-Bondia F, Moya A, Latorre A (2010) Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genomics 11:181

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis JJ, Wattam AR, Aziz RK, Brettin T, Butler R, Butler RM, Chlenski P, Conrad N, Dickerman A, Dietrich EM, Gabbard JL, Gerdes S, Guard A, Kenyon RW, Machi D, Mao C, Murphy-Olson D, Nguyen M, Nordberg EK, Olsen GJ, Olson RD, Overbeek JC, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomas C, VanOeffelen M, Vonstein V, Warren AS, Xia F, Xie D, Yoo H, Stevens R (2020) The PATRIC bioinformatics resource center: expanding data and analysis capabilities. Nucleic Acids Res 48(D1):D606–D612. https://doi.org/10.1093/nar/gkz943

    Article  CAS  PubMed  Google Scholar 

  • Del Barrio-Tofiño E, López-Causapé C, Oliver A (2020) Pseudomonas aeruginosa epidemic high-risk clones and their association with horizontally-acquired β-lactamases: 2020 update. Int J Antimicrob Agents 56:106196

    Article  PubMed  Google Scholar 

  • de Sales RO, Migliorini LB, Puga R, Kocsis B, Severino P (2020) A core genome multilocus sequence typing scheme for Pseudomonas aeruginosa. Front Microbiol 11:1049

    Article  PubMed  PubMed Central  Google Scholar 

  • Dolan SK, Kohlstedt M, Trigg S, Vallejo Ramirez P, Kaminski CF, Wittmann C, Welch M (2020) Contextual flexibility in Pseudomonas aeruginosa central carbon metabolism during growth in single carbon sources. mBio 11:e02684–e02619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dortet L, Lombardi C, Cretin F, Dessen A, Filloux A (2018) Pore-forming activity of the Pseudomonas aeruginosa type III secretion system translocon alters the host epigenome. Nat Microbiol 3:378–386

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • Elnegery AA, Mowafy WK, Zahra TA, Abou El-Khier NT (2021) Study of quorum-sensing LasR and RhlR genes and their dependent virulence factors in Pseudomonas aeruginosa isolates from infected burn wounds. Access Microbiol 3:000211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eschbach M, Schreiber K, Trunk K, Buer J, Jahn D, Schobert M (2004) Long-term anaerobic survival of the opportunistic pathogen Pseudomonas aeruginosa via pyruvate fermentation. J Bacteriol 186:4596–4604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang Y, Li Z, Liu J, Shu C, Wang X, Zhang X et al (2011) A pangenomic study of Bacillus thuringiensis. J Genet Genomics 38:567–576

    Article  CAS  PubMed  Google Scholar 

  • Finnan S, Morrissey JP, O’Gara F, Boyd EF (2004) Genome diversity of Pseudomonas aeruginosa isolates from cystic fibrosis patients and the hospital environment. J Clin Microbiol 42:5783–5792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer S, Dethlefsen S, Klockgether J, Tümmler B (2020) Phenotypic and genomic comparison of the two most common ExoU-positive Pseudomonas aeruginosa clones, PA14 and ST235. mSystems 5:e01007–e01020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freschi L, Jeukens J, Kukavica-Ibrulj I, Boyle B, Dupont M-J, Laroche J et al (2015) Clinical utilization of genomics data produced by the international Pseudomonas aeruginosa consortium. Front Microbiol 6:1036

    Article  PubMed  PubMed Central  Google Scholar 

  • Freschi L, Bertelli C, Jeukens J, Moore MP, Kukavica-Ibrulj I, Emond-Rheault J-G et al (2018) Genomic characterisation of an international Pseudomonas aeruginosa reference panel indicates that the two major groups draw upon distinct mobile gene pools. FEMS Microbiol Lett 365

    Google Scholar 

  • Freschi L, Vincent AT, Jeukens J, Emond-Rheault J-G, Kukavica-Ibrulj I, Dupont M-J et al (2019) The Pseudomonas aeruginosa pan-genome provides new insights on its population structure, horizontal gene transfer, and pathogenicity. Genome Biol Evol 11:109–120

    Article  CAS  PubMed  Google Scholar 

  • Frimmersdorf E, Horatzek S, Pelnikevich A, Wiehlmann L, Schomburg D (2010) How Pseudomonas aeruginosa adapts to various environments: a metabolomic approach. Environ Microbiol 12:1734–1747

    Article  CAS  PubMed  Google Scholar 

  • Gatzeva-Topalova PZ, May AP, Sousa MC (2005) Structure and mechanism of ArnA: conformational change implies ordered dehydrogenase mechanism in key enzyme for polymyxin resistance. Structure 13:929–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gene Ontology Consortium (2019) The gene ontology resource: 20 years and still going strong. Nucleic Acids Res 47:D330–D338

    Article  Google Scholar 

  • González-Ittig RE, Carletto-Körber FPM, Vera NS, Jiménez MG, Cornejo LS (2017) Population genetic structure and demographic history of Streptococcus mutans (Bacteria: Streptococcaceae). Biol J Linn Soc 120:705–716

    Google Scholar 

  • Hall BG, Ehrlich GD, Hu FZ (2010) Pan-genome analysis provides much higher strain typing resolution than multi-locus sequence typing. Microbiology 156:1060–1068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall CW, Hinz AJ, Gagnon LB-P, Zhang L, Nadeau J-P, Copeland S et al (2018) Pseudomonas aeruginosa biofilm antibiotic resistance gene ndvB expression requires the RpoS stationary-phase sigma factor. Appl Environ Microbiol 84

    Google Scholar 

  • Han K, Li Z, Peng R, Zhu L, Zhou T, Wang L et al (2013) Extraordinary expansion of a Sorangium cellulosum genome from an alkaline milieu. Sci Rep 3:2101

    Article  PubMed  PubMed Central  Google Scholar 

  • Hancock REW, Speert DP (2000) Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug Resist Updat 3:247–255

    Article  CAS  PubMed  Google Scholar 

  • Harrison EM, Carter MEK, Luck S, Ou H-Y, He X, Deng Z et al (2010) Pathogenicity islands PAPI-1 and PAPI-2 contribute individually and synergistically to the virulence of Pseudomonas aeruginosa strain PA14. Infect Immun 78:1437–1446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hauser AR (2009) The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat Rev Microbiol 7:654–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hilker R, Munder A, Klockgether J, Losada PM, Chouvarine P, Cramer N et al (2015) Interclonal gradient of virulence in the Pseudomonas aeruginosa pangenome from disease and environment. Environ Microbiol 17:29–46

    Article  CAS  PubMed  Google Scholar 

  • Hirsch CN, Foerster JM, Johnson JM, Sekhon RS, Muttoni G, Vaillancourt B et al (2014) Insights into the maize pan-genome and pan-transcriptome. Plant Cell 26:121–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Høiby N, Ciofu O, Johansen HK, Song Z, Moser C, Jensen PØ et al (2011) The clinical impact of bacterial biofilms. Int J Oral Sci 3:55–65

    Article  PubMed  PubMed Central  Google Scholar 

  • Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S (2018) High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 9:1–8

    Article  Google Scholar 

  • Jeanvoine A, Meunier A, Puja H, Bertrand X, Valot B, Hocquet D (2019) Contamination of a hospital plumbing system by persister cells of a copper-tolerant high-risk clone of Pseudomonas aeruginosa. Water Res 157:579–586

    Article  CAS  PubMed  Google Scholar 

  • Jeukens J, Boyle B, Kukavica-Ibrulj I, Ouellet MM, Aaron SD, Charette SJ et al (2014) Comparative genomics of isolates of a Pseudomonas aeruginosa epidemic strain associated with chronic lung infections of cystic fibrosis patients. PLoS One 9:e87611

    Article  PubMed  PubMed Central  Google Scholar 

  • Kamali E, Jamali A, Ardebili A, Ezadi F, Mohebbi A (2020) Evaluation of antimicrobial resistance, biofilm forming potential, and the presence of biofilm-related genes among clinical isolates of Pseudomonas aeruginosa. BMC Res Notes 13:27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:D457–D462

    Article  CAS  PubMed  Google Scholar 

  • Kim HS, Park BK, Kim SK, Han SB, Lee JW, Lee D-G et al (2017) Clinical characteristics and outcomes of Pseudomonas aeruginosa bacteremia in febrile neutropenic children and adolescents with the impact of antibiotic resistance: a retrospective study. BMC Infect Dis 17:500

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim Y, Gu C, Kim HU, Lee SY (2020) Current status of pan-genome analysis for pathogenic bacteria. Curr Opin Biotechnol 63:54–62

    Article  PubMed  Google Scholar 

  • Kirch W (ed) (2008) Pearson’s correlation coefficient. In: Encyclopedia of public health. Springer, Dordrecht, pp 1090–1091

    Google Scholar 

  • Klockgether J, Cramer N, Wiehlmann L, Davenport C, Tümmler B (2011) Pseudomonas aeruginosa genomic structure and diversity. Front Microbiol 2:150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konstantinidis KT, Ramette A, Tiedje JM (2006) The bacterial species definition in the genomic era. Philos Trans R Soc B Biol Sci 361:1929–1940

    Article  Google Scholar 

  • Kos VN, Déraspe M, McLaughlin RE, Whiteaker JD, Roy PH, Alm RA et al (2015) The resistome of Pseudomonas aeruginosa in relationship to phenotypic susceptibility. Antimicrob Agents Chemother 59:427–436

    Article  PubMed  Google Scholar 

  • Kumar A, Munder A, Aravind R, Eapen SJ, Tümmler B, Raaijmakers JM (2013) Friend or foe: genetic and functional characterization of plant endophytic Pseudomonas aeruginosa. Environ Microbiol 15:764–779

    Article  CAS  PubMed  Google Scholar 

  • Kung VL, Ozer EA, Hauser AR (2010) The accessory genome of Pseudomonas aeruginosa. Microbiol Mol Biol Rev 74:621–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lahiri SD, Johnstone MR, Ross PL, McLaughlin RE, Olivier NB, Alm RA (2014) Avibactam and class C β-lactamases: mechanism of inhibition, conservation of the binding pocket, and implications for resistance. Antimicrob Agents Chemother 58:5704–5713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee I, Andam CP (2019) Pan-genome diversification and recombination in Cronobacter sakazakii, an opportunistic pathogen in neonates, and insights to its xerotolerant lifestyle. BMC Microbiol 19:article number 306

    Article  Google Scholar 

  • Lee DG, Urbach JM, Wu G, Liberati NT, Feinbaum RL, Miyata S et al (2006) Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol 7:R90

    Article  PubMed  PubMed Central  Google Scholar 

  • Li G, Lu S, Shen M, Le S, Shen W, Tan Y et al (2017) Characterization and interstrain transfer of prophage pp3 of Pseudomonas aeruginosa. PLoS One 12:e0174429

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin J, Cheng J, Wang Y, Shen X (2018) The Pseudomonas quinolone signal (PQS): not just for quorum sensing anymore. Front Cell Infect Microbiol 8:230

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu Q-F, Cao D-M, Su L-L, Li S-B, Ye G-B, Zhu X-Y, Wang J-P (2019) Genus-wide comparative genomics analysis of Neisseria to identify new genes associated with pathogenicity and niche adaptation of Neisseria pathogens. Int J Genomics 2019:e6015730

    Article  Google Scholar 

  • Maciel-Vergara G, Jensen AB, Eilenberg J (2018) Cannibalism as a possible entry route for opportunistic pathogenic bacteria to insect hosts, exemplified by Pseudomonas aeruginosa, a pathogen of the giant mealworm Zophobas morio. Insects 9:88

    Article  PubMed Central  Google Scholar 

  • Mah T-F, Pitts B, Pellock B, Walker GC, Stewart PS, O’Toole GA (2003) A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306–310

    Article  CAS  PubMed  Google Scholar 

  • Marttinen P, Croucher NJ, Gutmann MU, Corander J, Hanage WP (2015) Recombination produces coherent bacterial species clusters in both core and accessory genomes. Microb Genom 1:e000038

    PubMed  PubMed Central  Google Scholar 

  • McPhee JB, Lewenza S, Hancock REW (2003) Cationic antimicrobial peptides activate a two-component regulatory system, PmrA-PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol Microbiol 50:205–217

    Article  CAS  PubMed  Google Scholar 

  • Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R (2005) The microbial pan-genome. Curr Opin Genet Dev 15:589–594

    Article  CAS  PubMed  Google Scholar 

  • Mikkelsen H, Duck Z, Lilley KS, Welch M (2007) Interrelationships between colonies, biofilms, and planktonic cells of Pseudomonas aeruginosa. J Bacteriol 189:2411–2416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mikkelsen H, McMullan R, Filloux A (2011) The Pseudomonas aeruginosa reference strain PA14 displays increased virulence due to a mutation in ladS. PLoS One 6:e29113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mira A (2010) The bacterial pan-genome: a new paradigm in microbiology. Int Microbiol 45–57

    Google Scholar 

  • Molina-Santiago C, Udaondo Z, Ramos J-L (2015) Draft whole-genome sequence of the antibiotic-producing soil isolate Pseudomonas sp. strain 250J. Environ Microbiol Rep 7:288–292

    Article  CAS  PubMed  Google Scholar 

  • Moore MP, Lamont IL, Williams D, Paterson S, Kukavica-Ibrulj I, Tucker NP et al (2021) Transmission, adaptation and geographical spread of the Pseudomonas aeruginosa Liverpool epidemic strain. Microb Genom 7

    Google Scholar 

  • Morita Y, Tomida J, Kawamura Y (2012) Primary mechanisms mediating aminoglycoside resistance in the multidrug-resistant Pseudomonas aeruginosa clinical isolate PA7. Microbiology 158:1071–1083

    Article  CAS  PubMed  Google Scholar 

  • Mosquera-Rendón J, Rada-Bravo AM, Cárdenas-Brito S, Corredor M, Restrepo-Pineda E, Benítez-Páez A (2016) Pangenome-wide and molecular evolution analyses of the Pseudomonas aeruginosa species. BMC Genomics 17:45

    Article  PubMed  PubMed Central  Google Scholar 

  • Mulet X, Cabot G, Ocampo-Sosa AA, Domínguez MA, Zamorano L, Juan C et al (2013) Biological markers of Pseudomonas aeruginosa epidemic high-risk clones. Antimicrob Agents Chemother 57:5527–5535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller C, Plésiat P, Jeannot K (2011) A two-component regulatory system interconnects resistance to polymyxins, aminoglycosides, fluoroquinolones, and β-lactams in Pseudomonas aeruginosa. Antimicrob Agents Chemother 55:1211–1221

    Article  CAS  PubMed  Google Scholar 

  • Oliver A, Mulet X, López-Causapé C, Juan C (2015) The increasing threat of Pseudomonas aeruginosa high-risk clones. Drug Resist Updat 21–22:41–59

    Article  PubMed  Google Scholar 

  • Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH, Koren S, Phillippy AM (2016) Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 17

    Google Scholar 

  • Ozer EA, Nnah E, Didelot X, Whitaker RJ, Hauser AR (2019) The population structure of Pseudomonas aeruginosa is characterized by genetic isolation of exoU+ and exoS+ lineages. Genome Biol Evol 11:1780–1796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pachori P, Gothalwal R, Gandhi P (2019) Emergence of antibiotic resistance Pseudomonas aeruginosa in intensive care unit; a critical review. Genes Dis 6:109–119

    Article  PubMed  PubMed Central  Google Scholar 

  • Papazian L, Klompas M, Luyt C-E (2020) Ventilator-associated pneumonia in adults: a narrative review. Intensive Care Med 46:888–906

    Article  PubMed  PubMed Central  Google Scholar 

  • Park J, Zhang Y, Buboltz AM, Zhang X, Schuster SC, Ahuja U et al (2012) Comparative genomics of the classical Bordetella subspecies: the evolution and exchange of virulence-associated diversity amongst closely related pathogens. BMC Genomics 13:545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park C, Shin B, Park W (2020) Protective role of bacterial alkanesulfonate monooxygenase under oxidative stress. Appl Environ Microbiol 86:e00692-20

    Article  PubMed  PubMed Central  Google Scholar 

  • Pearson WR (2013) An introduction to sequence similarity (“homology”) searching. Curr Protoc Bioinformatics 3

    Google Scholar 

  • Pirnay J-P, Bilocq F, Pot B, Cornelis P, Zizi M, Eldere JV et al (2009) Pseudomonas aeruginosa population structure revisited. PLoS One 4:e7740

    Article  PubMed  PubMed Central  Google Scholar 

  • Pohl S, Klockgether J, Eckweiler D, Khaledi A, Schniederjans M, Chouvarine P et al (2014) The extensive set of accessory Pseudomonas aeruginosa genomic components. FEMS Microbiol Lett 356:235–241

    Article  CAS  PubMed  Google Scholar 

  • Porter SS, Chang PL, Conow CA, Dunham JP, Friesen ML (2017) Association mapping reveals novel serpentine adaptation gene clusters in a population of symbiotic Mesorhizobium. ISME J 11:248–262

    Article  CAS  PubMed  Google Scholar 

  • Ramos J-L (ed) (2004) Pseudomonas: volume 3 biosynthesis of macromolecules and molecular metabolism. Springer, New York

    Google Scholar 

  • Rampioni G, Falcone M, Heeb S, Frangipani E, Fletcher MP, Dubern J-F et al (2016) Unravelling the genome-wide contributions of specific 2-Alkyl-4-quinolones and PqsE to quorum sensing in Pseudomonas aeruginosa. PLoS Pathog 12:e1006029

    Article  PubMed  PubMed Central  Google Scholar 

  • Rasmussen TB, Danielsen M, Valina O, Garrigues C, Johansen E, Pedersen MB (2008) Streptococcus thermophilus core genome: comparative genome hybridization study of 47 strains. Appl Environ Microbiol 74:4703–4710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ripp S, Ogunseitan OA, Miller RV (1994) Transduction of a freshwater microbial community by a new Pseudomonas aeruginosa generalized transducing phage, UT1. Mol Ecol 3:121–126

    Article  CAS  PubMed  Google Scholar 

  • Rossi E, Falcone M, Molin S, Johansen HK (2018) High-resolution in situ transcriptomics of Pseudomonas aeruginosa unveils genotype independent patho-phenotypes in cystic fibrosis lungs. Nat Commun 9:3459

    Article  PubMed  PubMed Central  Google Scholar 

  • Rossolini GM, Mantengoli E (2005) Treatment and control of severe infections caused by multiresistant Pseudomonas aeruginosa. Clin Microbiol Infect 11:17–32

    Article  CAS  PubMed  Google Scholar 

  • Roy PH, Tetu SG, Larouche A, Elbourne L, Tremblay S, Ren Q et al (2010) Complete genome sequence of the multiresistant taxonomic outlier Pseudomonas aeruginosa PA7. PLoS One 5:e8842

    Article  PubMed  PubMed Central  Google Scholar 

  • Rubio-Gómez JM, Santiago CM, Udaondo Z, Garitaonaindia MT, Krell T, Ramos J-L, Daddaoua A (2020) Full transcriptomic response of Pseudomonas aeruginosa to an inulin-derived fructooligosaccharide. Front Microbiol 11:202

    Article  PubMed  PubMed Central  Google Scholar 

  • Saxena S, Banerjee G, Garg R, Singh M (2014) Comparative study of biofilm formation in Pseudomonas aeruginosa isolates from patients of lower respiratory tract infection. J Clin Diagn Res 8:DC09–DC11

    PubMed  PubMed Central  Google Scholar 

  • Scaccabarozzi L, Leoni L, Ballarini A, Barberio A, Locatelli C, Casula A et al (2015) Pseudomonas aeruginosa in dairy goats: genotypic and phenotypic comparison of intramammary and environmental isolates. PLoS One 10:e0142973

    Article  PubMed  PubMed Central  Google Scholar 

  • Schick A, Kassen R (2018) Rapid diversification of Pseudomonas aeruginosa in cystic fibrosis lung-like conditions. PNAS 115:10714–10719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schreiber K, Boes N, Eschbach M, Jaensch L, Wehland J, Bjarnsholt T et al (2006) Anaerobic survival of Pseudomonas aeruginosa by pyruvate fermentation requires an Usp-type stress protein. J Bacteriol 188:659–668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069

    Article  CAS  PubMed  Google Scholar 

  • Selezska K, Kazmierczak M, Müsken M, Garbe J, Schobert M, Häussler S et al (2012) Pseudomonas aeruginosa population structure revisited under environmental focus: impact of water quality and phage pressure. Environ Microbiol 14:1952–1967

    Article  CAS  PubMed  Google Scholar 

  • Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ et al (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959–964

    Article  CAS  PubMed  Google Scholar 

  • Subedi D, Vijay AK, Kohli GS, Rice SA, Willcox M (2018) Comparative genomics of clinical strains of Pseudomonas aeruginosa strains isolated from different geographic sites. Sci Rep 8:15668

    Article  PubMed  PubMed Central  Google Scholar 

  • Swingley WD, Chen M, Cheung PC, Conrad AL, Dejesa LC, Hao J et al (2008) Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina. PNAS 105:2005–2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tariq MA, Everest FLC, Cowley LA, Wright R, Holt GS, Ingram H et al (2019) Temperate bacteriophages from chronic Pseudomonas aeruginosa lung infections show disease-specific changes in host range and modulate antimicrobial susceptibility. mSystems 4:e00191-18

    Article  PubMed  PubMed Central  Google Scholar 

  • Templeton AR (2006) Population genetics and microevolutionary theory. Wiley, Hoboken, NJ

    Book  Google Scholar 

  • Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL et al (2005) Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. PNAS 102:13950–13955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treepong P, Kos VN, Guyeux C, Blanc DS, Bertrand X, Valot B, Hocquet D (2018) Global emergence of the widespread Pseudomonas aeruginosa ST235 clone. Clin Microbiol Infect 24:258–266

    Article  CAS  PubMed  Google Scholar 

  • Udaondo Z, Molina L, Daniels C, Gómez MJ, Molina-Henares MA, Matilla MA et al (2013) Metabolic potential of the organic-solvent tolerant Pseudomonas putida DOT-T1E deduced from its annotated genome. J Microbial Biotechnol 6:598–611

    Article  Google Scholar 

  • Udaondo Z, Molina L, Segura A, Duque E, Ramos JL (2016) Analysis of the core genome and pangenome of Pseudomonas putida. Environ Microbiol 18:3268–3283

    Article  CAS  PubMed  Google Scholar 

  • Udaondo Z, Duque E, Ramos J-L (2017) The pangenome of the genus Clostridium. Environ Microbiol 19:2588–2603

    Article  CAS  PubMed  Google Scholar 

  • Udaondo Z, Ramos J-L, Segura A, Krell T, Daddaoua A (2018) Regulation of carbohydrate degradation pathways in Pseudomonas involves a versatile set of transcriptional regulators. J Microbial Biotechnol 11:442–454

    Article  CAS  Google Scholar 

  • UniProt Consortium (2019) UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res 47:D506–D515

    Article  Google Scholar 

  • Valot B, Guyeux C, Rolland JY, Mazouzi K, Bertrand X, Hocquet D (2015) What it takes to be a Pseudomonas aeruginosa? The core genome of the opportunistic pathogen updated. PLoS One 10:e0126468

    Article  PubMed  PubMed Central  Google Scholar 

  • van Belkum A, Soriaga LB, LaFave MC, Akella S, Veyrieras J-B, Barbu EM et al (2015) Phylogenetic distribution of CRISPR-Cas systems in antibiotic-resistant Pseudomonas aeruginosa. mBio 6:e01796–e01715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vior NM, Lacret R, Chandra G, Dorai-Raj S, Trick M, Truman AW (2018) Discovery and biosynthesis of the antibiotic bicyclomycin in distantly related bacterial classes. Appl Environ Microbiol 84:e02828-17

    Article  PubMed  PubMed Central  Google Scholar 

  • Walker TS, Bais HP, Déziel E, Schweizer HP, Rahme LG, Fall R, Vivanco JM (2004) Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol 134:320–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White PA, Stokes HW, Bunny KL, Hall RM (1999) Characterisation of a chloramphenicol acetyltransferase determinant found in the chromosome of Pseudomonas aeruginosa. FEMS Microbiol Lett 175:27–35

    Article  CAS  PubMed  Google Scholar 

  • Wiehlmann L, Wagner G, Cramer N, Siebert B, Gudowius P, Morales G et al (2007) Population structure of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 104:8101–8106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willenbrock H, Hallin PF, Wassenaar TM, Ussery DW (2007) Characterization of probiotic Escherichia coli isolates with a novel pan-genome microarray. Genome Biol 8:R267

    Article  PubMed  PubMed Central  Google Scholar 

  • Williams JG, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:6531–6535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng L, Jin S (2003) aph(3′)-IIb, a gene encoding an aminoglycoside-modifying enzyme, is under the positive control of surrogate regulator HpaA. Antimicrob Agents Chemother 47:3867–3876

    Google Scholar 

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Acknowledgments

This work was supported by the University of Arkansas for Medical Sciences (UAMS) College of Medicine Barton Pilot Grant FY19 program (AWD00052801), the UAMS Translational Research Institute (UL1 TR003107) through the NIH National Center for Advancing Translational Sciences, and the National Science Foundation under Award No. OIA-1946391. The content is solely the responsibility of the authors and does not necessarily represent the official views of the funding agencies.

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  1. Department of Biomedical Informatics, University of Arkansas for Medical Sciences, Little Rock, AR, USA

    Kaleb Z. Abram, Se-Ran Jun & Zulema Udaondo

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  1. Kaleb Z. Abram
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  2. Se-Ran Jun
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  3. Zulema Udaondo
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Correspondence to Zulema Udaondo .

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  1. Department of Life Sciences, Imperial College London, London, West Sussex, UK

    Alain Filloux

  2. Department of Environmental Protection, Consejo Superior de Investigaciones Científicas, Granada, Spain

    Juan-Luis Ramos

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Abram, K.Z., Jun, SR., Udaondo, Z. (2022). Pseudomonas aeruginosa Pangenome: Core and Accessory Genes of a Highly Resourceful Opportunistic Pathogen. In: Filloux, A., Ramos, JL. (eds) Pseudomonas aeruginosa. Advances in Experimental Medicine and Biology, vol 1386. Springer, Cham. https://doi.org/10.1007/978-3-031-08491-1_1

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