1887

Microbial Genomics logo

Volume 4, Issue 8

Taxonogenomics reveal multiple novel genomospecies associated with clinical isolates of Stenotrophomonas maltophilia Open Access

Abstract

Stenotrophomonas maltophilia has evolved as one of the leading multidrug-resistant pathogens responsible for a variety of nosocomial infections especially in highly debilitated patients. As information on the genomic and intraspecies diversity of this clinically important pathogen is limited, we sequenced the whole genome of 27 clinical isolates from hospitalized patients. Phylogenomic analysis along with the genomes of type strains suggested that the clinical isolates are distributed over the Stenotrophomonas maltophilia complex (Smc) within the genus Stenotrophomonas. Further genome-based taxonomy coupled with the genomes of type strains of the genus Stenotrophomonas allowed us to identify five cryptic genomospecies, which are associated with the clinical isolates of S. maltophilia and are potentially novel species. These isolates share a very small core genome that implies a high level of genetic diversity within the isolates. Recombination analysis of core genomes revealed that the impact of recombination is more than mutation in the diversification of clinical S. maltophilia isolates. Distribution analysis of well-characterized antibiotic-resistance and efflux pump genes of S. maltophilia across multiple novel genomospecies provided insights into its antibiotic-resistant ability. This study supports the existence of multiple cryptic species within the Smc besides S. maltophilia, which are associated with human infections, and highlights the importance of genome-based approaches to delineate bacterial species. This data will aid in improving clinical diagnosis and for understanding species-specific clinical manifestations of infection due to Stenotrophomonas species.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): genomospecies , phylogenomics , resistome , Stenotrophomonas maltophilia and taxonogenomics
© 2018 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000207
2018-08-07
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/mgen/4/8/mgen000207.html?itemId=/content/journal/mgen/10.1099/mgen.0.000207&mimeType=html&fmt=ahah

References

  1. Hauben L, Vauterin L, Moore ER, Hoste B, Swings J. Genomic diversity of the genus Stenotrophomonas. Int J Syst Bacteriol 1999; 49:1749–1760 [View Article][PubMed]
     [Google Scholar]
  2. Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L et al. The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 2009; 7:514–525 [View Article][PubMed]
     [Google Scholar]
  3. Mukherjee P, Roy P. Genomic potential of Stenotrophomonas maltophilia in bioremediation with an assessment of its multifaceted role in our environment. Front Microbiol 2016; 7:967 [View Article][PubMed]
     [Google Scholar]
  4. Berg G, Martinez JL. Friends or foes: can we make a distinction between beneficial and harmful strains of the Stenotrophomonas maltophilia complex?. Front Microbiol 2015; 6:241 [View Article][PubMed]
     [Google Scholar]
  5. Brooke JS. Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev 2012; 25:2–41 [View Article][PubMed]
     [Google Scholar]
  6. Looney WJ, Narita M, Mühlemann K. Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis 2009; 9:312–323 [View Article][PubMed]
     [Google Scholar]
  7. Chang YT, Lin CY, Chen YH, Hsueh PR. Update on infections caused by Stenotrophomonas maltophilia with particular attention to resistance mechanisms and therapeutic options. Front Microbiol 2015; 6:893 [View Article][PubMed]
     [Google Scholar]
  8. Denton M, Kerr KG. Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev 1998; 11:57–80[PubMed]
     [Google Scholar]
  9. Brooke JS. New strategies against Stenotrophomonas maltophilia: a serious worldwide intrinsically drug-resistant opportunistic pathogen. Expert Rev Anti Infect Ther 2014; 12:1–4 [View Article][PubMed]
     [Google Scholar]
  10. Anzai Y, Kim H, Park JY, Wakabayashi H, Oyaizu H. Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. Int J Syst Evol Microbiol 2000; 50:1563–1589 [View Article][PubMed]
     [Google Scholar]
  11. Svensson-Stadler LA, Mihaylova SA, Moore ER. Stenotrophomonas interspecies differentiation and identification by gyrB sequence analysis. FEMS Microbiol Lett 2012; 327:15–24 [View Article][PubMed]
     [Google Scholar]
  12. Rhee JY, Choi JY, Choi MJ, Song JH, Peck KR et al. Distinct groups and antimicrobial resistance of clinical Stenotrophomonas maltophilia complex isolates from Korea. J Med Microbiol 2013; 62:748–753 [View Article][PubMed]
     [Google Scholar]
  13. Patil PP, Midha S, Kumar S, Patil PB. Genome sequence of type strains of genus Stenotrophomonas. Front Microbiol 2016; 7:309 [View Article][PubMed]
     [Google Scholar]
  14. Pompilio A, Pomponio S, Crocetta V, Gherardi G, Verginelli F et al. Phenotypic and genotypic characterization of Stenotrophomonas maltophilia isolates from patients with cystic fibrosis: genome diversity, biofilm formation, and virulence. BMC Microbiol 2011; 11:159 [View Article][PubMed]
     [Google Scholar]
  15. Lin CW, Chiou CS, Chang YC, Yang TC. Comparison of pulsed-field gel electrophoresis and three rep-PCR methods for evaluating the genetic relatedness of Stenotrophomonas maltophilia isolates. Lett Appl Microbiol 2008; 47:393–398 [View Article][PubMed]
     [Google Scholar]
  16. Kaiser S, Biehler K, Jonas D. A Stenotrophomonas maltophilia multilocus sequence typing scheme for inferring population structure. J Bacteriol 2009; 191:2934–2943 [View Article][PubMed]
     [Google Scholar]
  17. Vidigal PG, Dittmer S, Steinmann E, Buer J, Rath PM et al. Adaptation of Stenotrophomonas maltophilia in cystic fibrosis: molecular diversity, mutation frequency and antibiotic resistance. Int J Med Microbiol 2014; 304:613–619 [View Article][PubMed]
     [Google Scholar]
  18. Ochoa-Sánchez LE, Vinuesa P. Evolutionary genetic analysis uncovers multiple species with distinct habitat preferences and antibiotic resistance phenotypes in the Stenotrophomonas maltophilia complex. Front Microbiol 2017; 8:1548 [View Article][PubMed]
     [Google Scholar]
  19. Rocco F, De Gregorio E, Colonna B, Di Nocera PP. Stenotrophomonas maltophilia genomes: a start-up comparison. Int J Med Microbiol 2009; 299:535–546 [View Article][PubMed]
     [Google Scholar]
  20. Esposito A, Pompilio A, Bettua C, Crocetta V, Giacobazzi E et al. Evolution of Stenotrophomonas maltophilia in cystic fibrosis lung over chronic infection: a genomic and phenotypic population study. Front Microbiol 2017; 8:1590 [View Article][PubMed]
     [Google Scholar]
  21. Chung H, Lieberman TD, Vargas SO, Flett KB, Mcadam AJ et al. Global and local selection acting on the pathogen Stenotrophomonas maltophilia in the human lung. Nat Commun 2017; 8:14078 [View Article][PubMed]
     [Google Scholar]
  22. Adamek M, Linke B, Schwartz T. Virulence genes in clinical and environmental Stenotrophomas maltophilia isolates: a genome sequencing and gene expression approach. Microb Pathog 2014; 67-68:20–30 [View Article][PubMed]
     [Google Scholar]
  23. Lira F, Berg G, Martínez JL. Double-face meets the bacterial world: the opportunistic pathogen Stenotrophomonas maltophilia. Front Microbiol 2017; 8:2190 [View Article][PubMed]
     [Google Scholar]
  24. Crossman LC, Gould VC, Dow JM, Vernikos GS, Okazaki A et al. The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol 2008; 9:R74 [View Article][PubMed]
     [Google Scholar]
  25. Sánchez MB. Antibiotic resistance in the opportunistic pathogen Stenotrophomonas maltophilia. Front Microbiol 2015; 6:658 [View Article][PubMed]
     [Google Scholar]
  26. Youenou B, Favre-Bonté S, Bodilis J, Brothier E, Dubost A et al. Comparative genomics of environmental and clinical Stenotrophomonas maltophilia strains with different antibiotic resistance profiles. Genome Biol Evol 2015; 7:2484–2505 [View Article][PubMed]
     [Google Scholar]
  27. Toleman MA, Bennett PM, Bennett DM, Jones RN, Walsh TR. Global emergence of trimethoprim/sulfamethoxazole resistance in Stenotrophomonas maltophilia mediated by acquisition of sul genes. Emerg Infect Dis 2007; 13:559–565 [View Article][PubMed]
     [Google Scholar]
  28. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article][PubMed]
     [Google Scholar]
  29. Tatusova T, Dicuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article][PubMed]
     [Google Scholar]
  30. Lagesen K, Hallin P, Rødland EA, Staerfeldt HH, Rognes T et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108 [View Article][PubMed]
     [Google Scholar]
  31. Kerepesi C, Bánky D, Grolmusz V. AmphoraNet: the webserver implementation of the AMPHORA2 metagenomic workflow suite. Gene 2014; 533:538–540 [View Article][PubMed]
     [Google Scholar]
  32. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article][PubMed]
     [Google Scholar]
  33. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 2013; 4:2304 [View Article][PubMed]
     [Google Scholar]
  34. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26:2460–2461 [View Article][PubMed]
     [Google Scholar]
  35. Price MN, Dehal PS, Arkin AP. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article][PubMed]
     [Google Scholar]
  36. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [View Article][PubMed]
     [Google Scholar]
  37. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 2014; 64:316–324 [View Article][PubMed]
     [Google Scholar]
  38. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article][PubMed]
     [Google Scholar]
  39. Auch AF, Klenk HP, Göker M. Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci 2010; 2:142–148 [View Article][PubMed]
     [Google Scholar]
  40. Zhao Y, Wu J, Yang J, Sun S, Xiao J et al. PGAP: pan-genomes analysis pipeline. Bioinformatics 2012; 28:416–418 [View Article][PubMed]
     [Google Scholar]
  41. Zhao Y, Jia X, Yang J, Ling Y, Zhang Z et al. PanGP: a tool for quickly analyzing bacterial pan-genome profile. Bioinformatics 2014; 30:1297–1299 [View Article][PubMed]
     [Google Scholar]
  42. Darling AC, 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]
  43. Guindon S, Delsuc F, Dufayard JF, Gascuel O. Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol 2009; 537:113–137 [View Article][PubMed]
     [Google Scholar]
  44. Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput Biol 2015; 11:e1004041 [View Article][PubMed]
     [Google Scholar]
  45. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article][PubMed]
     [Google Scholar]
  46. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article][PubMed]
     [Google Scholar]
  47. Li XZ, Zhang L, McKay GA, Poole K. Role of the acetyltransferase AAC(6')-Iz modifying enzyme in aminoglycoside resistance in Stenotrophomonas maltophilia. J Antimicrob Chemother 2003; 51:803–811 [View Article][PubMed]
     [Google Scholar]
  48. Okazaki A, Avison MB. Aph(3')-IIc, an aminoglycoside resistance determinant from Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2007; 51:359–360 [View Article][PubMed]
     [Google Scholar]
  49. Liaw SJ, Lee YL, Hsueh PR. Multidrug resistance in clinical isolates of Stenotrophomonas maltophilia: roles of integrons, efflux pumps, phosphoglucomutase (SpgM), and melanin and biofilm formation. Int J Antimicrob Agents 2010; 35:126–130 [View Article][PubMed]
     [Google Scholar]
  50. Al-Hamad A, Upton M, Burnie J. Molecular cloning and characterization of SmrA, a novel ABC multidrug efflux pump from Stenotrophomonas maltophilia. J Antimicrob Chemother 2009; 64:731–734 [View Article][PubMed]
     [Google Scholar]
  51. Lin YT, Huang YW, Liou RS, Chang YC, Yang TC. MacABCsm, an ABC-type tripartite efflux pump of Stenotrophomonas maltophilia involved in drug resistance, oxidative and envelope stress tolerances and biofilm formation. J Antimicrob Chemother 2014; 69:3221–3226 [View Article][PubMed]
     [Google Scholar]
  52. Hu RM, Liao ST, Huang CC, Huang YW, Yang TC. An inducible fusaric acid tripartite efflux pump contributes to the fusaric acid resistance in Stenotrophomonas maltophilia. PLoS One 2012; 7:e51053 [View Article][PubMed]
     [Google Scholar]
  53. Coenye T, Vanlaere E, Falsen E, Vandamme P. Stenotrophomonas africana Drancourt et al. 1997 is a later synonym of Stenotrophomonas maltophilia (Hugh 1981) Palleroni and Bradbury 1993. Int J Syst Evol Microbiol 2004; 54:1235–1237 [View Article][PubMed]
     [Google Scholar]
  54. Drancourt M, Bollet C, Raoult D. Stenotrophomonas africana sp. nov., an opportunistic human pathogen in Africa. Int J Syst Evol Microbiol 1997; 47:160–163
     [Google Scholar]
  55. Maiden MC, Jansen van Rensburg MJ, Bray JE, Earle SG, Ford SA et al. MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 2013; 11:728–736 [View Article][PubMed]
     [Google Scholar]
  56. Adegoke AA, Stenström TA, Okoh AI. Stenotrophomonas maltophilia as an emerging ubiquitous pathogen: looking beyond contemporary antibiotic therapy. Front Microbiol 2017; 8:2276 [View Article][PubMed]
     [Google Scholar]
  57. Falagas ME, Valkimadi PE, Huang YT, Matthaiou DK, Hsueh PR. Therapeutic options for Stenotrophomonas maltophilia infections beyond co-trimoxazole: a systematic review. J Antimicrob Chemother 2008; 62:889–894 [View Article][PubMed]
     [Google Scholar]
  58. Kaur P, Gautam V, Tewari R. Distribution of class 1 integrons, sul1 and sul2 genes among clinical isolates of Stenotrophomonas maltophilia from a Tertiary Care Hospital in North India. Microb Drug Resist 2015; 21:380–385 [View Article][PubMed]
     [Google Scholar]
  59. Ruppé E, Cherkaoui A, Lazarevic V, Emonet S, Schrenzel J. Establishing genotype-to-phenotype relationships in bacteria causing hospital-acquired pneumonia: a prelude to the application of clinical metagenomics. Antibiotics 2017; 6:30 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000207
Loading
Taxonogenomics reveal multiple novel genomospecies associated with clinical isolates of Stenotrophomonas maltophilia
M Gen 4, e000207 (2018); https://doi.org/10.1099/mgen.0.000207
/content/journal/mgen/10.1099/mgen.0.000207
/content/journal/mgen/10.1099/mgen.0.000207
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error