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Volume 167, Issue 7

, resident member of the urogenital microbiota? Free

Abstract

is a Gram-positive species previously isolated from human urine. Although other species from the same genus have been associated with urinary tract infections, is currently believed to be a non-pathogenic member of the urogenital microbiota. Prior to our study, only two isolates were described in the literature, and very little is known about the species. Here, we describe UFMG-H7, the first strain of this species isolated from the urine of healthy cattle. The genome for this isolate was produced and compared to the two other publicly available as well as other genome assemblies. Our in-depth genomic analysis identified four additional publicly available genome assemblies that are representatives of the species, also isolated from the human urogenital tract. Although none of the strains have been associated with symptoms or disease, numerous genes associated with virulence factors are encoded. In contrast to related species and species from the bovine vaginal tract, all strains examined code for the SpaD-type pili suggesting adherence is essential for its persistence within the urinary tract. As the other strains analysed were isolated from the human urogenital tract, our results suggest that this species may be specific to this niche.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bovine microbiome , Corynebacterium phoceense , urinary microbiome and urogenital microbiome
Funding
This study was supported by the:
  • National Science Foundation (Award 1661357)
    • Principle Award Recipient: CatherinePutonti
  • Loyola University Chicago
    • Principle Award Recipient: LauraMaskeri
  • Loyola University Chicago
    • Principle Award Recipient: AdrianaEne
  • CAPES-PROEX
    • Principle Award Recipient: SilviaGiannattasio-Ferraz
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico
    • Principle Award Recipient: EdelF Barbosa-Stancioli
© 2021 The Authors
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2021-07-16
2024-04-19
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References

  1. Fouts DE, Pieper R, Szpakowski S, Pohl H, Knoblach S et al. Integrated next-generation sequencing of 16S rDNA and metaproteomics differentiate the healthy urine microbiome from asymptomatic bacteriuria in neuropathic bladder associated with spinal cord injury. J Transl Med 2012; 10:174 [View Article] [PubMed]
     [Google Scholar]
  2. Pearce MM, Hilt EE, Rosenfeld AB, Zilliox MJ, Thomas-White K et al. The female urinary microbiome: A comparison of women with and without urgency urinary incontinence. MBio 2014; 5:e01283–14 [View Article] [PubMed]
     [Google Scholar]
  3. Hilt EE, McKinley K, Pearce MM, Rosenfeld AB, Zilliox MJ et al. Urine is not sterile: Use of enhanced urine culture techniques to detect resident bacterial flora in the adult female bladder. J Clin Microbiol 2014; 52:871–876 [View Article] [PubMed]
     [Google Scholar]
  4. Thomas-White K, Forster SC, Kumar N, Van Kuiken M, Putonti C et al. Culturing of female bladder bacteria reveals an interconnected urogenital microbiota. Nat Commun 2018; 9:1557 [View Article] [PubMed]
     [Google Scholar]
  5. Kline KA, Lewis AL. Gram-positive uropathogens, polymicrobial urinary tract infection, and the emerging microbiota of the urinary tract. Microbiol Spectr 2016; 4: [View Article] [PubMed]
     [Google Scholar]
  6. Bailiff NL, Westropp JL, Jang SS, Ling GV. Corynebacterium urealyticum urinary tract infection in dogs and cats: 7 cases (1996-2003. J Am Vet Med Assoc 2005; 226:1676–1680 [View Article] [PubMed]
     [Google Scholar]
  7. Briscoe KA, Barrs VR, Lindsay S, Hoffmann KL, Cockwill KR et al. Encrusting cystitis in a cat secondary to Corynebacterium urealyticum infection. J Feline Med Surg 2010; 12:972–977 [View Article] [PubMed]
     [Google Scholar]
  8. Suarez ML, Espino L, Vila M, Santamarina G. Urinary tract infection caused by Corynebacterium urealyticum in a dog. J Small Anim Pract 2002; 43:299–302 [View Article] [PubMed]
     [Google Scholar]
  9. Nicolet J, Fey H. Antibody coated bacteria in urine sediment from cattle infected with Corynebacterium renale. Vet Rec 1979; 105:301–303 [View Article] [PubMed]
     [Google Scholar]
  10. Rebhun WC, Dill SG, Perdrizet JA, Hatfield CE. Pyelonephritis in cows: 15 cases (1982-1986). J Am Vet Med Assoc 1989; 194:953–955
     [Google Scholar]
  11. Wallace LL, Bouchard G, Nicholson W, Turk J, Sweeney CL. Polypoid cystitis, pyelonephritis, and obstructive uropathy in a cow. J Am Vet Med Assoc 1990; 197:1181–1183
     [Google Scholar]
  12. Yeruham I, Elad D, Avidar Y, Goshen T, Asis E. Four-year survey of urinary tract infections in calves in Israel. Vet Rec 2004; 154:204–206 [View Article] [PubMed]
     [Google Scholar]
  13. Yeruham I, Elad D, Avidar Y, Goshen T. A herd level analysis of urinary tract infection in dairy cattle. Vet J 2006; 171:172–176 [View Article] [PubMed]
     [Google Scholar]
  14. Braun U, Nuss K, Wehbrink D, Rauch S, Pospischil A. Clinical and ultrasonographic findings, diagnosis and treatment of pyelonephritis in 17 cows. Vet J 2008; 175:240–248 [View Article] [PubMed]
     [Google Scholar]
  15. Niang EHA, CI L, Morand A, Ndongo S, Raoult D et al. Corynebacterium urinapleomorphum sp. nov., a new bacterial species isolated from human urine sample. New Microbes New Infect 2019; 31:100576
     [Google Scholar]
  16. Cresci M, Ibrahima Lo C, Khelaifia S, Mouelhi D, Delerce J et al. Corynebacterium phoceense sp. nov., strain MC1T a new bacterial species isolated from human urine. New Microbes New Infect 2016; 14:73–82 [View Article] [PubMed]
     [Google Scholar]
  17. Intanoo M, Kongkeitkajorn MB, Pattarajinda V, Bernard JK, Callaway TR et al. Isolation and screening of aflatoxin-detoxifying yeast and bacteria from ruminal fluids to reduce aflatoxin B 1 contamination in dairy cattle feed. J Appl Microbiol 2018; 125:1603–1613 [View Article]
     [Google Scholar]
  18. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
     [Google Scholar]
  19. 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]
  20. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article] [PubMed]
     [Google Scholar]
  21. Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG et al. Anvi’o: an advanced analysis and visualization platform for’ omics data. PeerJ 2015; 3:e1319 [View Article]
     [Google Scholar]
  22. 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]
  23. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
     [Google Scholar]
  24. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S et al. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 2015; 5:8365 [View Article] [PubMed]
     [Google Scholar]
  25. Davis JJ, Wattam AR, Aziz RK, Brettin T, Butler R et al. The PATRIC Bioinformatics resource center: expanding data and analysis capabilities. Nucleic Acids Res 2020; 48:D606–D612 [View Article] [PubMed]
     [Google Scholar]
  26. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article] [PubMed]
     [Google Scholar]
  27. Bertelli C, Laird MR, Williams KP. Simon Fraser University Research Computing Group Lau BY et al. Islandviewer 4: Expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res 2017; 45:W30–W35 [View Article] [PubMed]
     [Google Scholar]
  28. Ortiz-Pérez A, Martín-de-Hijas NZ, Esteban J, Fernández-Natal MI, García-Cía JI et al. High frequency of macrolide resistance mechanisms in clinical isolates of Corynebacterium species. Microb Drug Resist 2010; 16:273–277 [View Article] [PubMed]
     [Google Scholar]
  29. Salem N, Salem L, Saber S, Ismail G, Bluth MH. Corynebacterium urealyticum: a comprehensive review of an understated organism. Infect Drug Resist 2015; 8:129–145 [View Article] [PubMed]
     [Google Scholar]
  30. Navas J, Fernández-Martínez M, Salas C, Cano ME, Martínez-Martínez L. Susceptibility to Aminoglycosides and distribution of aph and aac(3)-XI genes among Corynebacterium striatum clinical isolates. PLoS One 2016; 11:e0167856 [View Article] [PubMed]
     [Google Scholar]
  31. Schroven K, Aertsen A, Lavigne R. Bacteriophages as drivers of bacterial virulence and their potential for biotechnological exploitation. FEMS Microbiol Rev 2021; 45: [View Article]
     [Google Scholar]
  32. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–21 [View Article] [PubMed]
     [Google Scholar]
  33. Liu B, Zheng D, Jin Q, Chen L, Yang J. VFDB 2019: A comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res 2019; 47:D687–D692 [View Article] [PubMed]
     [Google Scholar]
  34. Begley TP, Kinsland C, Strauss E. The biosynthesis of coenzyme a in bacteria. In Vitamins & Hormones Elsevier; pp 157–171
     [Google Scholar]
  35. Ballas P, Rückert C, Wagener K, Drillich M, Kämpfer P et al. Corynebacterium urogenitale sp. nov. isolated from the genital tract of a cow. Int J Syst Evol Microbiol 2020; 70:3625–3632 [View Article] [PubMed]
     [Google Scholar]
  36. Ballas P, Rückert C, Wagener K, Drillich M, Kämpfer P et al. Corynebacterium endometrii sp. nov., isolated from the uterus of a cow with endometritis. Int J Syst Evol Microbiol 2020; 70:146–152 [View Article] [PubMed]
     [Google Scholar]
  37. Laguardia-Nascimento M, Branco KMGR, Gasparini MR, Giannattasio-Ferraz S, Leite LR et al. Vaginal microbiome characterization of nellore cattle using metagenomic analysis. PLoS One 2015; 10:e0143294 [View Article] [PubMed]
     [Google Scholar]
  38. Wang M-L, Liu M-C, Xu J, An L-G, Wang J-F et al. Uterine microbiota of dairy cows with clinical and subclinical endometritis. Front Microbiol 2018; 9:2691 [View Article]
     [Google Scholar]
  39. Giannattasio-Ferraz S, Laguardia-Nascimento M, Gasparini MR, Leite LR, Araujo FMG et al. A common vaginal microbiota composition among breeds of Bos taurus indicus (Gyr and Nellore. Braz J Microbiol 2019; 50:1115–1124 [View Article] [PubMed]
     [Google Scholar]
  40. Ballas P, Reinländer U, Schlegl R, Ehling-Schulz M, Drillich M et al. Characterization of intrauterine cultivable aerobic microbiota at the time of insemination in dairy cows with and without mild endometritis. Theriogenology 2021; 159:28–34 [View Article] [PubMed]
     [Google Scholar]
  41. El-Jakee J, Ahmed W, El-Seedy F, Abd El-Moez S. Bacterial profile of the genital tract in femalebuffalo during the different reproductive stages. Glob Vet 2008; 2:7–14
     [Google Scholar]
  42. Sugumaran R, Sistla S, Chavhan P, Deb AK. Corynebacterium amycolatum: An unusual cause of corneal ulcer. BMJ Case Rep 2020; 13: [View Article] [PubMed]
     [Google Scholar]
  43. Borde K, Rao V, Shah M, Pavani N, Anand M. Not always a commensal: A case of mastitis by Corynebacterium amycolatum. IDCases 2020; 20:e00728 [View Article] [PubMed]
     [Google Scholar]
  44. Lefèvre CR, Pelletier R, Le Monnier A, Corvec S, Bille E. Clinical relevance and antimicrobial susceptibility profile of the unknown human pathogen corynebacterium aurimucosum. J Med Microbiol 2021; 70:
     [Google Scholar]
  45. Lo S, Thiam I, Fall B, Ba-Diallo A, Diallo OF et al. Urinary tract infection with Corynebacterium aurimucosum after urethroplasty stricture of the urethra: a case report. J Med Case Rep 2015; 9:156 [View Article] [PubMed]
     [Google Scholar]
  46. Chen X, Zhao X, Chen L, Zeng W, Xu H. Vaginitis caused by corynebacterium amycolatum in a prepubescent girl. J Pediatr Adolesc Gynecol 2015; 28:e165–167 [View Article] [PubMed]
     [Google Scholar]
  47. Spaulding CN, Hultgren SJ. Adhesive PILI in UTI pathogenesis and drug development. Pathogens 2016; 5: [View Article] [PubMed]
     [Google Scholar]
  48. Giannattasio-Ferraz S, Maskeri L, Oliveira AP, Barbosa-Stancioli EF, Putonti C. Draft genome sequence of Citrobacter freundii UFMG-H9, isolated from urine from a healthy bovine heifer (Gyr breed. Microbiol Resour Announc 2020; 9: [View Article] [PubMed]
     [Google Scholar]
  49. Giannattasio-Ferraz S, Maskeri L, Oliveira AP, Barbosa-Stancioli EF, Putonti C. Three draft genome sequences of Staphylococcus species isolated from the urine of healthy bovine heifers (Gyr breed. Microbiol Resour Announc 2020; 9: [View Article] [PubMed]
     [Google Scholar]
  50. Hurst RE, Zebrowski R. Identification of proteoglycans present at high density on bovine and human bladder luminal surface. J Urol 1994; 152:1641–1645 [View Article] [PubMed]
     [Google Scholar]
  51. Neugent ML, Hulyalkar NV, Nguyen VH, Zimmern PE, De Nisco NJ. Advances in understanding the human urinary microbiome and its potential role in urinary tract infection. MBio 2020; 11: [View Article]
     [Google Scholar]
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Corynebacterium phoceense, resident member of the urogenital microbiota?
Microbiology 167, 001068 (2021); https://doi.org/10.1099/mic.0.001068
/content/journal/micro/10.1099/mic.0.001068
/content/journal/micro/10.1099/mic.0.001068
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