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Volume 9, Issue 1

Leveraging comparative genomics to uncover alien genes in bacterial genomes Open Access

Abstract

A significant challenge in bacterial genomics is to catalogue genes acquired through the evolutionary process of horizontal gene transfer (HGT). Both comparative genomics and sequence composition-based methods have often been invoked to quantify horizontally acquired genes in bacterial genomes. Comparative genomics methods rely on completely sequenced genomes and therefore the confidence in their predictions increases as the databases become more enriched in completely sequenced genomes. Recent developments including in microbial genome sequencing call for reassessment of alien genes based on information-rich resources currently available. We revisited the comparative genomics approach and developed a new algorithm for alien gene detection. Our algorithm compared favourably with the existing comparative genomics-based methods and is capable of detecting both recent and ancient transfers. It can be used as a standalone tool or in concert with other complementary algorithms for comprehensively cataloguing alien genes in bacterial genomes.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): comparative genomics , horizontal gene transfer and phyletic pattern analysis
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2023-01-27
2024-04-25
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References

  1. Ochiai K, Yamanaka T, Kimura K, Sawada O. Inheritance of drug resistance (and its transfer) between shigella strains and between shigella and E. coli strains. Hihon Iji Shimpor 1959; 1861:34
     [Google Scholar]
  2. Zinder ND, Lederberg J. Genetic exchange in Salmonella. J Bacteriol 1952; 64:679–699 [View Article]
     [Google Scholar]
  3. Lederberg J, Tatum EL. Gene recombination in Escherichia coli. Nature 1946; 158:558 [View Article]
     [Google Scholar]
  4. Avery OT, Macleod CM, McCarty M. Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J Exp Med 1944; 79:137–158 [View Article]
     [Google Scholar]
  5. Doolittle WF. Uprooting the tree of life. Sci Am 2000; 282:90–95 [View Article] [PubMed]
     [Google Scholar]
  6. Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature 2000; 405:299–304 [View Article] [PubMed]
     [Google Scholar]
  7. Arnold BJ, Huang IT, Hanage WP. Horizontal gene transfer and adaptive evolution in bacteria. Nat Rev Microbiol 2022; 20:206–218 [View Article] [PubMed]
     [Google Scholar]
  8. Hall JPJ, Brockhurst MA, Harrison E. Sampling the mobile gene pool: innovation via horizontal gene transfer in bacteria. Philos Trans R Soc Lond B Biol Sci 2017; 372:20160424 [View Article] [PubMed]
     [Google Scholar]
  9. Koonin EV. Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions. F1000Res 2016; 5:F1000 Faculty Rev-1805 [View Article] [PubMed]
     [Google Scholar]
  10. Soucy SM, Huang J, Gogarten JP. Horizontal gene transfer: building the web of life. Nat Rev Genet 2015; 16:472–482 [View Article] [PubMed]
     [Google Scholar]
  11. Doolittle WF. Phylogenetic classification and the universal tree. Science 1999; 284:2124–2129 [View Article] [PubMed]
     [Google Scholar]
  12. Azad RK, Lawrence JG. Detecting laterally transferred genes. Methods Mol Biol 2012; 855:281–308 [View Article]
     [Google Scholar]
  13. Jani M, Azad RK. IslandCafe: compositional anomaly and feature enrichment assessment for delineation of genomic Islands. G3 (Bethesda) 2019; 9:3273–3285 [View Article]
     [Google Scholar]
  14. Ravenhall M, Škunca N, Lassalle F, Dessimoz C. Inferring horizontal gene transfer. PLOS Comput Biol 2015; 11:e1004095 [View Article] [PubMed]
     [Google Scholar]
  15. Sheinman M, Arkhipova K, Arndt PF, Dutilh BE, Hermsen R et al. Identical sequences found in distant genomes reveal frequent horizontal transfer across the bacterial domain. Elife 2021; 10:e62719 [View Article] [PubMed]
     [Google Scholar]
  16. Bapteste E, Boucher Y, Leigh J, Doolittle WF. Phylogenetic reconstruction and lateral gene transfer. Trends Microbiol 2004; 12:406–411 [View Article] [PubMed]
     [Google Scholar]
  17. Lerat E, Daubin V, Moran NA. From gene trees to organismal phylogeny in prokaryotes: the case of the gamma-proteobacteria. PLoS Biol 2003; 1:E19 [View Article]
     [Google Scholar]
  18. Gogarten MB, Gogarten JP, Olendzenski LC. Horizontal Gene Transfer. In Testing Phylogenetic Methods to Identify Gene Transfer Totowa, NJ: HumanaPress; 2009 pp 227–240 [View Article]
     [Google Scholar]
  19. Gophna U, Charlebois RL, Doolittle WF. Ancient lateral gene transfer in the evolution of Bdellovibrio bacteriovorus. Trends Microbiol 2006; 14:64–69 [View Article] [PubMed]
     [Google Scholar]
  20. Zhu Q, Kosoy M, Dittmar K. HGTector: an automated method facilitating genome-wide discovery of putative horizontal gene transfers. BMC Genomics 2014; 15:717 [View Article] [PubMed]
     [Google Scholar]
  21. Podell S, Gaasterland T. DarkHorse: a method for genome-wide prediction of horizontal gene transfer. Genome Biol 2007; 8:R16 [View Article] [PubMed]
     [Google Scholar]
  22. Podell S, Gaasterland T, Allen EE. A database of phylogenetically atypical genes in archaeal and bacterial genomes, identified using the DarkHorse algorithm. BMC Bioinformatics 2008; 9:419 [View Article] [PubMed]
     [Google Scholar]
  23. Langille MGI, Hsiao WWL, Brinkman FSL. Evaluation of genomic island predictors using a comparative genomics approach. BMC Bioinformatics 2008; 9:329 [View Article] [PubMed]
     [Google Scholar]
  24. Ibtehaz N, Ahmed I, Ahmed MS, Rahman MS, Azad RK et al. SSG-LUGIA: single sequence based genome level unsupervised genomic Island prediction algorithm. Brief Bioinform 2021; 22:bbab116 [View Article]
     [Google Scholar]
  25. Vernikos GS, Parkhill J. Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 2006; 22:2196–2203 [View Article] [PubMed]
     [Google Scholar]
  26. Wei W, Gao F, Du M-Z, Hua H-L, Wang J et al. Zisland Explorer: detect genomic islands by combining homogeneity and heterogeneity properties. Brief Bioinform 2017; 18:357–366 [View Article] [PubMed]
     [Google Scholar]
  27. Azad RK, Lawrence JG. Detecting laterally transferred genes. Methods Mol Biol 2012; 855:281–308 [View Article]
     [Google Scholar]
  28. Azad RK, Lawrence JG. Detecting laterally transferred genes: use of entropic clustering methods and genome position. Nucleic Acids Res 2007; 35:4629–4639 [View Article] [PubMed]
     [Google Scholar]
  29. Azad RK, Lawrence JG. Use of artificial genomes in assessing methods for atypical gene detection. PLoS Comput Biol 2005; 1:e56 [View Article] [PubMed]
     [Google Scholar]
  30. Bertelli C, Brinkman FSL. Improved genomic island predictions with IslandPath-DIMOB. Bioinformatics 2018; 34:2161–2167 [View Article] [PubMed]
     [Google Scholar]
  31. 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] [PubMed]
     [Google Scholar]
  32. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT et al. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 2005; 187:2426–2438 [View Article] [PubMed]
     [Google Scholar]
  33. Hiramatsu K, Ito T, Tsubakishita S, Sasaki T, Takeuchi F et al. Genomic basis for methicillin resistance in Staphylococcus aureus. Infect Chemother 2013; 45:117–136 [View Article]
     [Google Scholar]
  34. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH et al. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 2006; 367:731–739 [View Article] [PubMed]
     [Google Scholar]
  35. Ou H-Y, Chen L-L, Lonnen J, Chaudhuri RR, Thani AB et al. A novel strategy for the identification of genomic islands by comparative analysis of the contents and contexts of tRNA sites in closely related bacteria. Nucleic Acids Res 2006; 34:e3 [View Article]
     [Google Scholar]
  36. Arvey AJ, Azad RK, Raval A, Lawrence JG. Detection of genomic islands via segmental genome heterogeneity. Nucleic Acids Res 2009; 37:5255–5266 [View Article] [PubMed]
     [Google Scholar]
  37. Jani M, Mathee K, Azad RK. Identification of novel genomic Islands in Liverpool epidemic strain of Pseudomonas aeruginosa using segmentation and clustering. Front Microbiol 2016; 7:1210 [View Article]
     [Google Scholar]
  38. Sahl JW, Johnson JK, Harris AD, Phillippy AM, Hsiao WW et al. Genomic comparison of multi-drug resistant invasive and colonizing Acinetobacter baumannii isolated from diverse human body sites reveals genomic plasticity. BMC Genomics 2011; 12:1–12 [View Article] [PubMed]
     [Google Scholar]
  39. Gross R, Guzman CA, Sebaihia M, dos Santos VAPM, Pieper DH et al. The missing link: Bordetella petrii is endowed with both the metabolic versatility of environmental bacteria and virulence traits of pathogenic Bordetellae. BMC Genomics 2008; 9:449 [View Article]
     [Google Scholar]
  40. Lechner M, Schmitt K, Bauer S, Hot D, Hubans C et al. Genomic island excisions in Bordetella petrii. BMC Microbiol 2009; 9:141 [View Article]
     [Google Scholar]
  41. Holden MTG, Seth-Smith HMB, Crossman LC, Sebaihia M, Bentley SD et al. The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol 2009; 191:261–277 [View Article] [PubMed]
     [Google Scholar]
  42. Holden MTG, Titball RW, Peacock SJ, Cerdeño-Tárraga AM, Atkins T et al. Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci U S A 2004; 101:14240–14245 [View Article] [PubMed]
     [Google Scholar]
  43. Cerdeño-Tárraga AM, Efstratiou A, Dover LG, Holden MTG, Pallen M et al. The complete genome sequence and analysis of Corynebacterium diphtheriae NCTC13129. Nucleic Acids Res 2003; 31:6516–6523 [View Article] [PubMed]
     [Google Scholar]
  44. Uchiumi T, Ohwada T, Itakura M, Mitsui H, Nukui N et al. Expression islands clustered on the symbiosis island of the Mesorhizobium loti genome. J Bacteriol 2004; 186:2439–2448 [View Article] [PubMed]
     [Google Scholar]
  45. Pearson MM, Sebaihia M, Churcher C, Quail MA, Seshasayee AS et al. Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J Bacteriol 2008; 190:4027–4037 [View Article] [PubMed]
     [Google Scholar]
  46. Holden MTG, Heather Z, Paillot R, Steward KF, Webb K et al. Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens. PLoS Pathog 2009; 5:e1000346 [View Article] [PubMed]
     [Google Scholar]
  47. Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 2000; 406:477–483 [View Article] [PubMed]
     [Google Scholar]
  48. Bertelli C, Tilley KE, Brinkman FSL. Microbial genomic island discovery, visualization and analysis. Brief Bioinform 2019; 20:1685–1698 [View Article] [PubMed]
     [Google Scholar]
  49. 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] [PubMed]
     [Google Scholar]
  50. Pevsner J. Bioinformatics and functional genomics, Third edition. Chichester, West Sussex, UK ; Hoboken, New Jersey: John Wiley and Sons, Inc; 2015
     [Google Scholar]
  51. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011; 39:W29–37 [View Article] [PubMed]
     [Google Scholar]
  52. Eddy S. HMMER user’s guide. biological sequence analysis using profile hidden Markov models 2003
     [Google Scholar]
  53. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 2016; 44:D279–85 [View Article] [PubMed]
     [Google Scholar]
  54. Jani M, Azad RK. IslandCafe: compositional anomaly and feature enrichment assessment for delineation of genomic Islands. G3 (Bethesda) 2019; 9:3273–3285 [View Article]
     [Google Scholar]
  55. Hsiao WWL, Ung K, Aeschliman D, Bryan J, Finlay BB et al. Evidence of a large novel gene pool associated with prokaryotic genomic islands. PLoS Genet 2005; 1:e62 [View Article] [PubMed]
     [Google Scholar]
  56. Grant JR, Stothard P. The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Research 2008; 36:W181–W184 [View Article]
     [Google Scholar]
  57. Qi J, Luo H, Hao B. CVTree: a phylogenetic tree reconstruction tool based on whole genomes. Nucleic Acids Res 2004; 32:W45–7 [View Article] [PubMed]
     [Google Scholar]
  58. Jani M, Sengupta S, Hu K, Azad RK. Deciphering pathogenicity and antibiotic resistance islands in methicillin-resistant Staphylococcus aureus genomes. Open Biol 2017; 7:170094 [View Article] [PubMed]
     [Google Scholar]
  59. Song W, Wemheuer B, Zhang S, Steensen K, Thomas T. MetaCHIP: community-level horizontal gene transfer identification through the combination of best-match and phylogenetic approaches. Microbiome 2019; 7:1–14 [View Article]
     [Google Scholar]
  60. Song W, Steensen K, Thomas T. HgtSIM: a simulator for horizontal gene transfer (HGT) in microbial communities. PeerJ 2017; 5:e4015 [View Article] [PubMed]
     [Google Scholar]
  61. Lawrence JG, Ochman H. Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci U S A 1998; 95:9413–9417 [View Article] [PubMed]
     [Google Scholar]
  62. Lawrence JG, Roth JR. Genomic flux: genome evolution by gene loss and acquisition. Organization of the prokaryotic genome 1999263–289
     [Google Scholar]
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Leveraging comparative genomics to uncover alien genes in bacterial genomes
M Gen 9, 000939 (2023); https://doi.org/10.1099/mgen.0.000939
/content/journal/mgen/10.1099/mgen.0.000939
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