1887

Microbial Genomics logo

Volume 7, Issue 4

Genomics reveals the novel species placement of industrial contaminant isolates incorrectly identified as Open Access

Abstract

The complex (Bcc) is a closely related group of bacteria, composed of at least 20 different species, the accurate identification of which is essential in the context of infectious diseases. In industry, they can contaminate non-food products, including home and personal care products and cosmetics. The Bcc are problematic contaminants due to their ubiquitous presence and intrinsic antimicrobial resistance, which enables them to occasionally overcome preservation systems in non-sterile products. and are amongst the Bcc bacteria encountered most frequently as industrial contaminants, but their identification is not straightforward. Both species were historically established as a part of a group known collectively as taxon K, based upon analysis of the gene and multilocus sequence typing (MLST). Here, we deploy a straightforward genomics-based workflow for accurate Bcc classification using average nucleotide identity (ANI) and core-gene analysis. The workflow was used to examine a panel of 23 taxon K industrial strains, which, based on MLST, comprised 13 4 and 6 unclassified Bcc strains. Our genomic identification showed that the strains retained their classification, whilst the remaining strains were reclassified as sp. nov. Incorrect taxonomic identification of industrial contaminants is a problematic issue. Application and testing of our genomic workflow allowed the correct classification of 23 Bcc industrial strains, and also indicated that sp. nov. may have greater importance than as a contaminant species. Our study illustrates how the non-food manufacturing industry can harness whole-genome sequencing to better understand antimicrobial-resistant bacteria affecting their products.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Burkholderia , classification , contamination , industrial microbiology , phylogenomics and taxon K
Funding
This study was supported by the:
  • Biotechnology and Biological Sciences Research Council (Award BB/M009122/1)
    • Principle Award Recipient: EdwardCunningham-Oakes
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000564
2021-04-23
2024-05-07
Loading full text...

Full text loading...

/deliver/fulltext/mgen/7/4/mgen000564.html?itemId=/content/journal/mgen/10.1099/mgen.0.000564&mimeType=html&fmt=ahah

References

  1. Depoorter E, Bull MJ, Peeters C, Coenye T, Vandamme P et al. Burkholderia: an update on taxonomy and biotechnological potential as antibiotic producers. Appl Microbiol Biotechnol 2016; 100:5215–5229 [View Article][PubMed]
     [Google Scholar]
  2. Eberl L, Vandamme P. Members of the genus Burkholderia: good and bad guys. F1000Res 2016; 5:1007 26 05 2016 [View Article][PubMed]
     [Google Scholar]
  3. Zlosnik JEA, Zhou G, Brant R, Henry DA, Hird TJ et al. Burkholderia species infections in patients with cystic fibrosis in British Columbia, Canada. 30 years' experience. Ann Am Thorac Soc 2015; 12:70–78 [View Article][PubMed]
     [Google Scholar]
  4. Jacobs JL, Fasi AC, Ramette A, Smith JJ, Hammerschmidt R et al. Identification and onion pathogenicity of Burkholderia cepacia complex isolates from the onion rhizosphere and onion field soil. Appl Environ Microbiol 2008; 74:3121–3129 [View Article][PubMed]
     [Google Scholar]
  5. Mullins AJ, Murray JAH, Bull MJ, Jenner M, Jones C et al. Genome mining identifies cepacin as a plant-protective metabolite of the biopesticidal bacterium Burkholderia ambifaria . Nat Microbiol 2019; 4:996–1005 [View Article][PubMed]
     [Google Scholar]
  6. Cunningham-Oakes E, Weiser R, Pointon T, Mahenthiralingam E. Understanding the challenges of non-food industrial product contamination. FEMS Microbiol Lett 2020; 23:fnaa010
     [Google Scholar]
  7. Tavares M, Kozak M, Balola A, Coutinho CP, Godinho CP et al. Adaptation and survival of Burkholderia cepacia and B. contaminans during long-term incubation in saline solutions containing benzalkonium chloride. Front Bioeng Biotechnol 2020; 8:630 [View Article][PubMed]
     [Google Scholar]
  8. Vandamme P, Holmes B, Vancanneyt M, Coenye T, Hoste B et al. Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multivorans sp. nov. Int J Syst Bacteriol 1997; 47:1188–1200 [View Article][PubMed]
     [Google Scholar]
  9. Henry D, Campbell M, McGimpsey C, Clarke A, Louden L et al. Comparison of isolation media for recovery of Burkholderia cepacia complex from respiratory secretions of patients with cystic fibrosis. J Clin Microbiol 1999; 37:1004–1007 [View Article][PubMed]
     [Google Scholar]
  10. Mahenthiralingam E, Bischof J, Byrne SK, Radomski C, Davies JE. DNA-based diagnostic approaches for identification of Burkholderia cepacia Genomovars I and III DNA-based diagnostic approaches for identification of Burkholderia cepacia complex, Burkholderia vietnamiensis . J Clin Microbiol 2000; 38:3165–3173
     [Google Scholar]
  11. Mahenthiralingam E, Baldwin A, Drevinek P, Vanlaere E, Vandamme P et al. Multilocus sequence typing breathes life into a microbial metagenome. PLoS One 2006; 1:e17 [View Article][PubMed]
     [Google Scholar]
  12. Lipuma JJ. The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 2010; 23:299–323 [View Article][PubMed]
     [Google Scholar]
  13. Baldwin A, Mahenthiralingam E, Thickett KM, Honeybourne D, Maiden MCJ et al. Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex. J Clin Microbiol 2005; 43:4665–4673 [View Article][PubMed]
     [Google Scholar]
  14. Maiden MCJ, 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]
  15. Baldwin A, Mahenthiralingam E, Drevinek P, Pope C, Waine DJ. Elucidating global epidemiology of Burkholderia multivorans in cases of cystic fibrosis by multilocus sequence typing. J Clin Microbiol
     [Google Scholar]
  16. Fila L, Dřevínek P. Burkholderia cepacia complex in cystic fibrosis in the post-epidemic period: multilocus sequence typing-based approach. Folia Microbiol 2017; 62:509–514 [View Article][PubMed]
     [Google Scholar]
  17. Rose H, Baldwin A, Dowson CG, Mahenthiralingam E. Biocide susceptibility of the Burkholderia cepacia complex. J Antimicrob Chemother 2009; 63:502–510 [View Article][PubMed]
     [Google Scholar]
  18. Ferone M, Gowen A, Fanning S, Scannell AGM. Microbial detection and identification methods: bench top assays to omics approaches. Compr Rev Food Sci Food Saf 2020; 19:3106–3129 [View Article][PubMed]
     [Google Scholar]
  19. Griffith C. Surface sampling and the detection of contamination. Handbook of Hygiene Control in the Food Industry, 2nd ed. 2016
     [Google Scholar]
  20. Webster G, Newberry CJ, Fry JC, Weightman AJ. Assessment of bacterial community structure in the deep sub-seafloor biosphere by 16S rDNA-based techniques: a cautionary tale. J Microbiol Methods
     [Google Scholar]
  21. Caulfield T, Evans J, McGuire A, McCabe C, Bubela T et al. Reflections on the cost of "Low-Cost" whole genome sequencing: framing the health policy debate. PLoS Biol 2013; 11:e1001699–12 [View Article]
     [Google Scholar]
  22. Wallner A, King E, Ngonkeu ELM, Moulin L, Béna G. Genomic analyses of Burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans. BMC Genomics 2019; 20: [View Article]
     [Google Scholar]
  23. Vandamme P, Holmes B, Coenye T, Goris J, Mahenthiralingam E. Burkholderia cenocepacia sp. nov. - A new twist to an old story. Res Microbiol
     [Google Scholar]
  24. Dalmastri C, Baldwin A, Tabacchioni S, Bevivino A, Mahenthiralingam E et al. Investigating Burkholderia cepacia complex populations recovered from Italian maize rhizosphere by multilocus sequence typing. Environ Microbiol 2007; 9:1632-9 [View Article][PubMed]
     [Google Scholar]
  25. Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E. Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol
     [Google Scholar]
  26. Rushton L, Sass A, Baldwin A, Dowson CG, Donoghue D et al. Key role for efflux in the preservative susceptibility and adaptive resistance of Burkholderia cepacia complex bacteria. Antimicrob Agents Chemother 2013; 57:2972–2980 [View Article][PubMed]
     [Google Scholar]
  27. Depoorter E, De Canck E, Peeters C, Wieme AD, Cnockaert M et al. Burkholderia cepacia complex Taxon K: where to split?. Front Microbiol 2020; 11:1594 [View Article][PubMed]
     [Google Scholar]
  28. Bull MJ, Marchesi JR, Vandamme P, Plummer S, Mahenthiralingam E. Minimum taxonomic criteria for bacterial genome sequence depositions and announcements. J Microbiol Methods .
  29. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9: [View Article]
     [Google Scholar]
  30. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol
     [Google Scholar]
  31. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article][PubMed]
     [Google Scholar]
  32. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 2014; 15:R46 [View Article][PubMed]
     [Google Scholar]
  33. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A
     [Google Scholar]
  34. Page AJ, Alikhan N-F, Carleton HA, Seemann T, Keane JA et al. Comparison of classical multi-locus sequence typing software for next-generation sequencing data. Microbial Genomics 2017; 3: [View Article]
     [Google Scholar]
  35. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
     [Google Scholar]
  36. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article][PubMed]
     [Google Scholar]
  37. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
     [Google Scholar]
  38. Hancock JM, Zvelebil MJ, Cummings MP. FigTree. In: Dictionary of Bioinformatics and Computational Biology 2004
     [Google Scholar]
  39. Schöler U, Schöler U. Inkscape. In: Inkscape 2014
     [Google Scholar]
  40. Leong LEX, Lagana D, Carter GP, Wang Q, Smith K et al. Burkholderia lata infections from intrinsically contaminated chlorhexidine Mouthwash, Australia, 2016. Emerg Infect Dis 2018; 24:2109–2111 [View Article][PubMed]
     [Google Scholar]
  41. Caputo A, Fournier P-E, Raoult D. Genome and pan-genome analysis to classify emerging bacteria. Biol Direct 2019; 14:Figure legends [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000564
Loading
Genomics reveals the novel species placement of industrial contaminant isolates incorrectly identified as Burkholderia lata
M Gen 7, 000564 (2021); https://doi.org/10.1099/mgen.0.000564
/content/journal/mgen/10.1099/mgen.0.000564
/content/journal/mgen/10.1099/mgen.0.000564
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

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