1887

Abstract

is a metabolically versatile bacterium and also an important opportunistic pathogen. It has a remarkable genomic structure since the genetic information encoding its pathogenicity-related traits belongs to its core-genome while both environmental and clinical isolates are part of the same population with a highly conserved genomic sequence. Unexpectedly, considering the high level of sequence identity and homologue gene number shared between different isolates, the presence of specific essential genes of the two type strains PAO1 and PA14 has been reported to be highly variable. Here we report the detailed bioinformatics analysis of the essential genes of PAO1 and PA14 that have been previously experimentally identified and show that the reported gene variability was owed to sequencing and annotation inconsistencies, but that in fact they are highly conserved. This bioinformatics analysis led us to the definition of 348 general essential genes. In addition we show that 342 of these 348 essential genes are conserved in a nitrogen-fixing, cyst-forming, soil bacterium. These results support the hypothesis of having a polyphyletic origin with a Pseudomonads genomic backbone, and are a challenge to the accepted theory of bacterial evolution.

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2019-09-01
2024-03-28
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References

  1. Moradali MF, Ghods S, Rehm BHA. Pseudomonas aeruginosa Lifestyle: A Paradigm for Adaptation, Survival, and Persistence. Front Cell Infect Microbiol 2017; 7:39 [View Article]
    [Google Scholar]
  2. Wiens JR, Vasil AI, Schurr MJ, Vasil ML. Iron-regulated expression of alginate production, mucoid phenotype, and biofilm formation by Pseudomonas aeruginosa . MBio 2014; 5:1–12 [View Article]
    [Google Scholar]
  3. Lister PD, Wolter DJ, Hanson ND. Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin Microbiol Rev 2009; 22:582–610 [View Article]
    [Google Scholar]
  4. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P et al. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 2000; 406:959–964 [View Article]
    [Google Scholar]
  5. Mosquera-Rendón J, Rada-Bravo AM, Cárdenas-Brito S, Corredor M, Restrepo-Pineda E et al. Pangenome-wide and molecular evolution analyses of the Pseudomonas aeruginosa species. BMC Genomics 2016; 17:1–14 [View Article]
    [Google Scholar]
  6. Klockgether J, Cramer N, Wiehlmann L, Davenport CF, Tümmler B. Pseudomonas aeruginosa genomic structure and diversity. Front Microbiol 2011; 2:1–18 [View Article]
    [Google Scholar]
  7. Valot B, Guyeux C, Rolland JY, Mazouzi K, Bertrand X et al. What it takes to be a Pseudomonas aeruginosa? The core genome of the opportunistic pathogen updated. PLoS One 2015; 10:126468 [View Article]
    [Google Scholar]
  8. Rouli L, Merhej V, Fournier P-E, Raoult D. The bacterial pangenome as a new tool for analysing pathogenic bacteria. New Microbes New Infect 2015; 7:72–85 [View Article]
    [Google Scholar]
  9. Luo H, Lin Y, Gao F, Zhang C-T, Zhang R. Deg 10, an update of the database of essential genes that includes both protein-coding genes and noncoding genomic elements. Nucleic Acids Res 2014; 42:D574–D580 [View Article]
    [Google Scholar]
  10. Luo H, Gao F, Lin Y. Evolutionary conservation analysis between the essential and nonessential genes in bacterial genomes. Sci Rep 2015; 5:1–8 [View Article]
    [Google Scholar]
  11. Acevedo-Rocha CG, Fang G, Schmidt M, Ussery DW, Danchin A. From essential to persistent genes: a functional approach to constructing synthetic life. Trends in Genetics 2013; 29:273–279 [View Article]
    [Google Scholar]
  12. Juhas M, Reuß DR, Zhu B, Commichau FM. Bacillus subtilis and Escherichia coli essential genes and minimal cell factories after one decade of genome engineering. Microbiology 2014; 160:2341–2351 [View Article]
    [Google Scholar]
  13. Gallagher LA, Shendure J, Manoil C. Genome-scale identification of resistance functions in Pseudomonas aeruginosa using Tn-seq. MBio 2011; 2:1–8 [View Article]
    [Google Scholar]
  14. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E et al. Comprehensive transposon mutant library of Pseudomonas aeruginosa . Proc Natl Acad Sci U S A 2003; 100:14339–14344 [View Article]
    [Google Scholar]
  15. Liberati NT, Urbach JM, Miyata S, Lee DG, Drenkard E et al. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci U S A 2006; 103:2833–2838 [View Article]
    [Google Scholar]
  16. Skurnik D, Roux D, Aschard H, Cattoir V, Yoder-Himes D et al. A comprehensive analysis of in vitro and in vivo genetic fitness of Pseudomonas aeruginosa using high-throughput sequencing of transposon libraries. PLoS Pathog 2013; 9:e1003582 [View Article]
    [Google Scholar]
  17. Rusmini R, Vecchietti D, Macchi R, Vidal-Aroca F, Bertoni G. A shotgun antisense approach to the identification of novel essential genes in Pseudomonas aeruginosa . BMC Microbiol 2014; 14:24–29 [View Article]
    [Google Scholar]
  18. Turner KH, Wessel AK, Palmer GC, Murray JL, Whiteley M. Essential genome of Pseudomonas aeruginosa in cystic fibrosis sputum. Proc Natl Acad Sci U S A 2015; 112:4110–4115 [View Article]
    [Google Scholar]
  19. Lee SA, Gallagher LA, Thongdee M, Staudinger BJ, Lippman S et al. General and condition-specific essential functions of Pseudomonas aeruginosa . Proc Natl Acad Sci U S A 2015; 112:5189–5194 [View Article]
    [Google Scholar]
  20. Charlebois RL, Doolittle WF. Computing prokaryotic gene ubiquity: rescuing the core from extinction. Genome Res 2004; 14:2469–2477 [View Article]
    [Google Scholar]
  21. Özen AI, Ussery DW. Defining the Pseudomonas genus: where do we draw the line with Azotobacter?. Microb Ecol 2012; 63:239–248 [View Article]
    [Google Scholar]
  22. Rediers H, Vanderleyden J, De Mot R. Azotobacter vinelandii: a Pseudomonas in disguise?. Microbiology 2004; 150:1117–1119 [View Article]
    [Google Scholar]
  23. González-Casanova A, Aguirre-von-Wobeser E, Espín G, Servín-González L, Kurt N et al. Strong seed-bank effects in bacterial evolution. J Theor Biol 2014; 356:62–70 [View Article]
    [Google Scholar]
  24. Lex A, Gehlenborg N, Strobelt H, Vuillemot R, Pfister H. Upset: visualization of intersecting sets. IEEE Trans Vis Comput Graph 2014; 20:1983–1992 [View Article]
    [Google Scholar]
  25. Tatusov RL, Koonin EV, Lipman DJ. A genomic perspective on protein families. Science 1997; 278:631–637 [View Article]
    [Google Scholar]
  26. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped blast and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article]
    [Google Scholar]
  27. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004; 14:1394–1403 [View Article]
    [Google Scholar]
  28. Whitfield C, Trent MS. Biosynthesis and export of bacterial lipopolysaccharides. Annu Rev Biochem 2014; 83:99–128 [View Article]
    [Google Scholar]
  29. Setubal JC, dos Santos P, Goldman BS, Ertesvåg H, Espin G et al. Genome sequence of Azotobacter vinelandii, an obligate aerobe specialized to support diverse anaerobic metabolic processes. J Bacteriol 2009; 191:4534–4545 [View Article]
    [Google Scholar]
  30. Matsui H, Sano Y, Ishihara H, Shinomiya T. Regulation of pyocin genes in Pseudomonas aeruginosa by positive (prtN) and negative (prtR) regulatory genes. J Bacteriol 1993; 175:1257–1263 [View Article]
    [Google Scholar]
  31. Bertelli C, Laird MR, Williams KP, Lau BY, Hoad G et al. IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res 2017; 45:W30–W35 [View Article]
    [Google Scholar]
  32. Mira A, Pushker R, Legault BA, Moreira D, Rodríguez-Valera F. Evolutionary relationships of Fusobacterium nucleatum based on phylogenetic analysis and comparative genomics. BMC Evol Biol 2004; 4:50–17 [View Article]
    [Google Scholar]
  33. Zhaxybayeva O, Swithers KS, Lapierre P, Fournier GP, Bickhart DM et al. On the chimeric nature, thermophilic origin, and phylogenetic placement of the Thermotogales. Proc Natl Acad Sci U S A 2009; 106:5865–5870 [View Article]
    [Google Scholar]
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