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Corynebacterium guaraldiae sp. nov.: a new species of Corynebacterium from human infections

  • Clinical Microbiology - Research Paper
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Abstract

Non-diphtheria Corynebacterium species (NDC) belonging to the human skin and mucosa microbiota are frequently neglected as contaminants. However, reports of human infections by Corynebacterium spp. have increased considerably in recent years. In this study, a group of six NDC isolates of urine (n = 5) and sebaceous cyst (n = 1) from two South American countries were identified at genus level or misidentified based on API® Coryne and genetic/molecular analyses. The 16S rRNA (99.09–99.56%) and rpoB (96.18–97.14%) gene sequence similarities of the isolates were higher when compared with Corynebacterium aurimucosum DSM 44532 T. Multilocus sequence analysis (MLSA) indicated that these six NDC isolates compose a distinctive phylogenetic clade. Genome-based taxonomic analysis with the whole-genome sequences was able to separate these six isolates from other known Corynebacterium type strains. Average nucleotide identity (ANI), average amino acid identity (AAI), and digital DNA–DNA hybridization (dDDH) values between closely related type strains and the six isolates were considerably lower than the currently recommended threshold values for species circumscription. Phylogenetic and genomic taxonomy analyses indicated these microorganisms as a novel Corynebacterium species, for which we formally propose the name Corynebacterium guaraldiae sp. nov. with isolate 13T (= CBAS 827T = CCBH 35012T) as type strain.

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References

  1. Bernard K (2012) The genus Corynebacterium and other medically relevant coryneform-like bacteria. J Clin Microbiol Published online. https://doi.org/10.1128/JCM.00796-12

    Article  Google Scholar 

  2. Parte AC, SardàCarbasse J, Meier-Kolthoff JP, Reimer LC, Göker M (2020) List of prokaryotic names with standing in nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 70(11):5607–5612. https://doi.org/10.1099/ijsem.0.004332

    Article  PubMed  PubMed Central  Google Scholar 

  3. Ramos JN, Souza C, Faria YV et al (2019) Bloodstream and catheter-related infections due to different clones of multidrug-resistant and biofilm producer Corynebacterium striatum. BMC Infect Dis 19(1):672. https://doi.org/10.1186/s12879-019-4294-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Nudel K, Zhao X, Basu S et al (2018) Genomics of Corynebacterium striatum, an emerging multidrug-resistant pathogen of immunocompromised patients. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis 24(9):1016.e7-1016.e13. https://doi.org/10.1016/j.cmi.2017.12.024

    Article  CAS  Google Scholar 

  5. Sokol-Leszczynska B, Leszczynski P, Lachowicz D et al (2019) Corynebacterium coyleae as potential urinary tract pathogen. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol 38(7):1339–1342. https://doi.org/10.1007/s10096-019-03565-4

    Article  CAS  Google Scholar 

  6. Yatera K, Mukae H (2020) Corynebacterium species as one of the major causative pathogens of bacterial pneumonia. Respir Investig 58(3):131–133. https://doi.org/10.1016/j.resinv.2020.01.008

    Article  PubMed  Google Scholar 

  7. Zasada AA, Mosiej E (2018) Contemporary microbiology and identification of Corynebacteria spp. causing infections in human. Lett Appl Microbiol 66(6):472–483. https://doi.org/10.1111/lam.12883

    Article  CAS  PubMed  Google Scholar 

  8. Bao R, Gao X, Hu B, Zhou Z (2017) Matrix-assisted laser desorption ionization time-of-flight mass spectrometry: a powerful tool for identification of Corynebacterium species. J Thorac Dis 9(9):3239–3245. https://doi.org/10.21037/jtd.2017.09.69

    Article  PubMed  PubMed Central  Google Scholar 

  9. Barberis C, Almuzara M, Join-Lambert O, Ramírez MS, Famiglietti A, Vay C (2014) Comparison of the Bruker MALDI-TOF mass spectrometry system and conventional phenotypic methods for identification of Gram-positive rods. PLoS ONE 9(9):1–6. https://doi.org/10.1371/journal.pone.0106303

    Article  CAS  Google Scholar 

  10. Khamis A, Raoult D, La Scola B (2005) Comparison between rpoB and 16S rRNA gene sequencing for molecular identification of 168 clinical isolates of Corynebacterium. J Clin Microbiol. 43(4):1934–1936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Chun J, Rainey FA (2014) Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 64(PART 2):316–324. https://doi.org/10.1099/ijs.0.054171-0

    Article  PubMed  Google Scholar 

  12. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, De Meyer S, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68(1):461–466. https://doi.org/10.1099/ijsem.0.002516

    Article  CAS  PubMed  Google Scholar 

  13. Theel ES, Schmitt BH, Hall L et al (2012) Formic acid-based direct, on-plate testing of yeast and Corynebacterium species by Bruker Biotyper matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol 50(9):3093–3095. https://doi.org/10.1128/JCM.01045-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Baio PVP, Mota HF, Freitas AD et al (2013) Clonal multidrug-resistant Corynebacterium striatum within a nosocomial environment, Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz Published online. https://doi.org/10.1590/s0074-02762013000100004

    Article  Google Scholar 

  15. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  16. Yoon S-H, Ha S-M, Kwon S et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67(5):1613–1617. https://doi.org/10.1099/ijsem.0.001755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882. https://doi.org/10.1093/nar/25.24.4876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Aziz RK, Bartels D, Best AA et al (2008) The RAST s erver: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Bolt F, Cassiday P, Tondella ML, Dezoysa A, Efstratiou A, Sing A, Zasada A, Bernard K, Guiso N, Badell E, Rosso ML, Baldwin A, Dowson C (2010) Multilocus sequence typing identifies evidence for recombination and two distinct lineages of Corynebacterium diphtheriae. J Clin Microbiol 48(11):4177–4185. https://doi.org/10.1128/JCM.00274-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120. https://doi.org/10.1007/BF01731581

    Article  CAS  PubMed  Google Scholar 

  22. Nei M, Kumar S. Molecular evolution and phylogenetics. (Oxford Press U, ed.).; 2000.

  23. Thompson CC, Chimetto L, Edwards RA, Swings J, Stackebrandt E, Thompson FL (2013) Microbial genomic taxonomy. BMC Genomics 14:913. https://doi.org/10.1186/1471-2164-14-913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. https://doi.org/10.1186/1471-2105-14-60

    Article  PubMed  PubMed Central  Google Scholar 

  25. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57(1):81–91. https://doi.org/10.1099/ijs.0.64483-0

    Article  CAS  PubMed  Google Scholar 

  26. Rodriguez-R LM, Konstantinidis KT (2014) Bypassing cultivation to identify bacterial species identify bacterial species. Microbe 9(3):111–118

    Google Scholar 

  27. Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10(1):2182. https://doi.org/10.1038/s41467-019-10210-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Atasayar E, Zimmermann O, Spröer C, Schumann P, Groß U (2017) Corynebacterium gottingense sp. nov., isolated from a clinical patient. Int J Syst Evol Microbiol 67(11):4494–4499. https://doi.org/10.1099/ijsem.0.002322

    Article  CAS  PubMed  Google Scholar 

  29. Diop K, Nguyen TT, Delerce J et al (2018) Corynebacterium fournierii sp. nov., isolated from the female genital tract of a patient with bacterial vaginosis. Antonie Van Leeuwenhoek 111(7):1165–1174. https://doi.org/10.1007/s10482-018-1022-z

    Article  CAS  PubMed  Google Scholar 

  30. Badell E, Hennart M, Rodrigues C et al (2020) Corynebacterium rouxii sp. nov., a novel member of the diphtheriae species complex. Res Microbiol. 171(3–4):122–127. https://doi.org/10.1016/j.resmic.2020.02.003

    Article  CAS  PubMed  Google Scholar 

  31. Dazas M, Badell E, Carmi-Leroy A, Criscuolo A, Brisse S (2018) Taxonomic status of Corynebacterium diphtheriae biovar Belfanti and proposal of Corynebacterium belfantii sp. nov. Int J Syst Evol Microbiol 68(12):3826–3831. https://doi.org/10.1099/ijsem.0.003069

    Article  CAS  PubMed  Google Scholar 

  32. Jaén-Luchoro D, Gonzales-Siles L, Karlsson R et al (2020) Corynebacterium sanguinis sp. nov, a clinical and environmental associated corynebacterium. Syst Appl Microbiol 43(1):126039. https://doi.org/10.1016/j.syapm.2019.126039

    Article  CAS  PubMed  Google Scholar 

  33. Mcmullen AR, Anderson N, Wallace MA, Shupe A, Burnham CD (2017) When good bugs go bad: epidemiology and antimicrobial resistance profiles of pathogen. Antimicrob Agents Chemother 61(11):1–10

    Article  Google Scholar 

  34. Salem N, Salem L, Saber S, Ismail G (2015) Bluth MH Corynebacterium urealyticum: a comprehensive review of an understated organism. Infect Drug Resist 8:129–145. https://doi.org/10.2147/IDR.S74795

    Article  PubMed  PubMed Central  Google Scholar 

  35. Rocha DJP, Azevedo V, Brenig B et al (2020) Whole-genome sequencing reveals misidentification of a multidrug-resistant urine clinical isolate as Corynebacterium urealyticum. J Glob Antimicrob Resist 23:16–19. https://doi.org/10.1016/j.jgar.2020.07.020

    Article  PubMed  Google Scholar 

  36. Adderson EE, Boudreaux JW, Cummings JR et al (2008) Identification of clinical coryneform bacterial isolates: comparison of biochemical methods and sequence analysis of 16S rRNA and rpoB genes. J Clin Microbiol 46(3):921–927. https://doi.org/10.1128/JCM.01849-07

    Article  CAS  PubMed  Google Scholar 

  37. Rychert J (2019) Benefits and limitations of MALDI-TOF mass spectrometry for the identification of microorganisms. J Infect 2(4):1–5. https://doi.org/10.29245/2689-9981/2019/4.1142

    Article  Google Scholar 

  38. Alatoom AA, Cazanave CJ, Cunningham SA, Ihde SM, Patel R (2012) Identification of non-diphtheriae corynebacterium by use of matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol 50(1):160–163. https://doi.org/10.1128/JCM.05889-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Bizzini A, Jaton K, Romo D, Bille J, Prod’hom G, Greub G (2011) Matrix-assisted laser desorption ionization-time of flight mass spectrometry as an alternative to 16S rRNA gene sequencing for identification of difficult-to-identify bacterial strains. J Clin Microbiol 49(2):693–696. https://doi.org/10.1128/JCM.01463-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Stackebrandt E, Jonas E (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155

    Google Scholar 

  41. Khamis A, Raoult D, La Scola B (2004) rpoB gene sequencing for identification of Corynebacterium species. J Clin Microbiol 42(9):3925–3931. https://doi.org/10.1128/JCM.42.9.3925-3931.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We offer our deepest thanks to Raphael Hirata Jr. (In Memoriam), our eternal teacher and source of inspiration and to Rafael Sanches for his availability in advising on editing the image of this study. In addition, we thank CNPq for the research fellowship granted to LGCP.

Funding

This work was supported by Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior (CAPES) # 88882.450376/2019–01, and # 88882.315426/2019–01, Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) # E-26/202.087/2020, # E-26/210.889/2019, and # E-26/211.629/2015, Fundação Oswaldo Cruz (INOVA/FIOCRUZ) # 7481297331, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) # 309948/2018–5, and Secretaria de Ciencia y Técnica de la Universidad de Buenos Aires (UBACyT) # 20020170100109 BA.

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Authors and Affiliations

  1. Laboratory of Diphtheria and Corynebacteria of Clinical Relevance, Department of Microbiology, Immunology and Parasitology, State University of Rio de Janeiro, Rio de Janeiro, Brazil

    Lincoln de Oliveira Sant’Anna, Louisy Sanches dos Santos, Juliana Nunes Ramos & Ana Luíza Mattos-Guaraldi

  2. Hermes Pardini Institute, Vespasiano, Brazil

    Max Roberto Batista Araújo

  3. Department of Biotechnology, Institute of Health Sciences, Federal University of Bahia, Salvador, Brazil

    Danilo Jobim Passos Gil da Rocha & Luis Gustavo Carvalho Pacheco

  4. Interdisciplinary Laboratory of Medical Research, Oswaldo Cruz Institute, Oswaldo Cruz Foundation, Rio de Janeiro, Brazil

    Juliana Nunes Ramos & Verônica Viana Vieira

  5. Army Chemical and Pharmaceutical Laboratory, Ministry of Defense, Brasília, Brazil

    Paulo Victor Pereira Baio

  6. Richet Laboratory, Rio de Janeiro, Brazil

    Pedro Fernandez Del Peloso & Cassiana da Costa Ferreira Leite

  7. Professur Fuer Mikrobiologie, Friedrich-Alexander-Universität Erlagen-Nürnberg, Erlangen, Germany

    Renata Stavrakakis Peixoto & Andreas Burkovski

  8. Faculty of Pharmacy and Biochemistry and Bacteriology, Department of Clinical Biochemistry, University of Buenos Aires, Autonomous City of Buenos Aires, Buenos Aires, Argentina

    Marisa Almuzara, Carlos Vay & Claudia Barberis

  9. Faculty of Health and Life Sciences, Northumbria University, Newcastle Upon Tyne, UK

    Vartul Sangal

  10. Virus Bioinformatics Laboratory, Center of Biotechnology and Genetics, Department of Biological Sciences, State University of Santa Cruz, Ilhéus, Brazil

    Eric Roberto Guimarães Rocha Aguiar

Authors
  1. Lincoln de Oliveira Sant’Anna
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  2. Louisy Sanches dos Santos
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  3. Max Roberto Batista Araújo
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Contributions

LOS: Data curation; Formal analysis; Writing-original draft; Writing-review and editing; Investigation; Visualization. LSS: Data curation; Formal analysis; Writing-review and editing. MRBA: Writing-original draft; Investigation; Visualization. DJPR: Data curation; Formal analysis; Methodology. JNR: Data curation; Formal analysis; Writing-review and editing. PVPB: Data curation; Formal analysis; Writing-review and editing. PFDP: Writing-review and editing; Investigation; Resources. CCFL: Writing-review and editing; Investigation. RPS: Writing-original draft; Investigation. MA: Writing-review and editing; Investigation; Validation. CV: Data curation; Formal analysis; Writing-review and editing; Investigation; Methodology; Resources. CB: Data curation; Formal analysis; Writing-review and editing; Investigation; Methodology. VS: Data curation; Formal analysis; Writing-review and editing; Resources; Visualization; Validation. AB: Data curation; Formal analysis; Writing-review and editing; Resources; Visualization; Validation; Funding acquisition. ERGRA: Data curation; Formal analysis; Methodology. ALMG: Conceptualization; Writing-review and editing; Resources; Visualization; Funding acquisition. LGCP: Conceptualization; Data curation; Formal analysis; Writing-review and editing; Investigation; Methodology; Resources; Visualization; Validation; Funding acquisition; Project administration. VVV: Conceptualization; Data curation; Formal analysis; Writing-review and editing; Investigation; Methodology; Resources; Visualization; Validation; Funding acquisition; Project administration; Supervision.

Corresponding author

Correspondence to Lincoln de Oliveira Sant’Anna.

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Ethical approval

This study was approved by Research Ethics Committee of Hospital Universitário Pedro Ernesto (CEP/HUPE– CAAE: 25847614.8.0000.5259).

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The authors declare no competing interests.

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de Oliveira Sant’Anna, L., dos Santos, L.S., Araújo, M.R.B. et al. Corynebacterium guaraldiae sp. nov.: a new species of Corynebacterium from human infections. Braz J Microbiol 54, 779–790 (2023). https://doi.org/10.1007/s42770-023-00938-y

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