Microbiological and clinical features of Corynebacterium urealyticum: urinary tract stones and genomics as the Rosetta Stone
2008; Elsevier BV; Volume: 14; Issue: 7 Linguagem: Inglês
10.1111/j.1469-0691.2008.02023.x
ISSN1469-0691
AutoresFrancisco García Soriano, Andreas Tauch,
Tópico(s)Mycobacterium research and diagnosis
ResumoABSTRACTCorynebacterium urealyticum, formerly known as coryneform CDC group D2, was first recognized to be involved in human infections 30 years ago. It is a slow-growing, lipophilic, asaccharolytic and usually multidrug-resistant organism with potent urease activity. Its cell wall peptidoglycan, menaquinone, mycolic and cellular fatty acid composition is consistent with that of the genus Corynebacterium. DNA–DNA hybridization studies and 16S rDNA sequencing analysis have been used to determine the degree of relatedness of C. urealyticum to other corynebacterial species. The genome of the type strain consists of a circular chromosome with a size of 2 369 219 bp and a mean G + C content of 64.2%, and analysis of its genome explains the bacterium's lifestyle. C. urealyticum is a common skin colonizer of hospitalized elderly individuals who are receiving broad-spectrum antibiotics. It is an opportunistic pathogen causing mainly acute cystitis, pyelonephritis, encrusted cystitis, and encrusted pyelitis. More infrequently, it causes other infections, but mainly in patients with urological diseases. Infections are more common in males than in females, and treatment requires administration of antibiotics active against the organism in vitro, mainly glycopeptides, as well as surgical intervention, the latter mostly in cases of chronic infection. Mortality directly associated with infection by this organism is not frequent, but encrusted pyelitis in kidney-recipient patients may cause graft loss. The outcome of infection by this organism is reasonably good if the microbiological diagnosis is made and patients are treated appropriately. ABSTRACT Corynebacterium urealyticum, formerly known as coryneform CDC group D2, was first recognized to be involved in human infections 30 years ago. It is a slow-growing, lipophilic, asaccharolytic and usually multidrug-resistant organism with potent urease activity. Its cell wall peptidoglycan, menaquinone, mycolic and cellular fatty acid composition is consistent with that of the genus Corynebacterium. DNA–DNA hybridization studies and 16S rDNA sequencing analysis have been used to determine the degree of relatedness of C. urealyticum to other corynebacterial species. The genome of the type strain consists of a circular chromosome with a size of 2 369 219 bp and a mean G + C content of 64.2%, and analysis of its genome explains the bacterium's lifestyle. C. urealyticum is a common skin colonizer of hospitalized elderly individuals who are receiving broad-spectrum antibiotics. It is an opportunistic pathogen causing mainly acute cystitis, pyelonephritis, encrusted cystitis, and encrusted pyelitis. More infrequently, it causes other infections, but mainly in patients with urological diseases. Infections are more common in males than in females, and treatment requires administration of antibiotics active against the organism in vitro, mainly glycopeptides, as well as surgical intervention, the latter mostly in cases of chronic infection. Mortality directly associated with infection by this organism is not frequent, but encrusted pyelitis in kidney-recipient patients may cause graft loss. The outcome of infection by this organism is reasonably good if the microbiological diagnosis is made and patients are treated appropriately. Isolation of urease-positive coryneforms from urine samples in cases of encrusted cystitis was reported in 1945 [1Cifuentes Delatte L Urgoiti LC Urioste R Estudio general de 315 casos de infecciones urinarias.Rev Clin Esp. 1945; 18: 258-261Google Scholar] and later [2Aubert J Dore B Touchard G Loetitia G La cystite incrustée à urine alcaline.J Urol. 1982; 88: 359-363PubMed Google Scholar], but such corynebacteria were not well characterized. A non-spore-forming, aerobic and Gram-positive bacillus with strong urease activity was described by King in 1972 as coryneform CDC group D2 [3King EO The identification of unusual gram-negative bacteria. (Preliminary revision by RE Weaver, HW Tatum, and DG Hollis). Centers for Disease Control, Atlanta, GA1972Google Scholar]. In 1979, Jacobs and Perlino described a case of pneumonia in a debilitated patient from whom such an organism was iso lated [4Jacobs Jr, NF Perlino CA 'Diphtheroid' pneumonia.South Med J. 1979; 72: 475-476Crossref PubMed Scopus (23) Google Scholar]. This organism was implicated for the first time in urinary tract infections (UTIs) in a report published in 1985 [5Soriano F Ponte C Santamaría M et al.Corynebacterium group D2 as a cause of alkaline-encrusted cystitis: report of four cases and characterization of the organism.J Clin Microbiol. 1985; 21: 788-792Crossref PubMed Google Scholar] concerning four patients with alkaline encrusted cystitis. In the same year, eight cases of UTI caused by this organism were also reported [6Ortí T Martín A Palafox E Bonilla I Infecciones urinarias por Corynebacterium spp.: presentatión de 8 casos.Med Clin (Barc). 1985; 85: 266-268PubMed Google Scholar], and 2 years later, a report concerning 43 patients with asymptomatic bacteriuria, cystitis, acute pyelonephritis with bacteraemia, encrusted cystitis and wound infection was published [7Aguado JM Ponte C Soriano F Bacteriuria with a multiply resistant species of Corynebacterium (Corynebacterium group D2): an unnoticed cause of urinary tract infection.J Infect Dis. 1987; 156: 144-150Crossref PubMed Scopus (54) Google Scholar]. These results were expanded and confirmed 3 years later in the largest series reported so far [8Soriano F Aguado JM Ponte C Fernàndez-Roblas R Rodríguez-Tudela JL Urinary tract infection caused by Corynebacterium group D2. Report of 82 cases and review.Rev Infect Dis. 1990; 12: 1019-1034Crossref PubMed Scopus (83) Google Scholar]. After different taxonomic studies, it was concluded that coryneform CDC group D2 was a true Corynebacterium species, different from all others known, and it was named Corynebacterium urealyticum, stressing its strong ability to split urea [9Pitcher D Soto A Soriano F Valero-Guillén P Classification of coryneform bacteria associated with human urinary tract infections (group D2) as Corynebacterium urealyticum sp. nov.Int J Syst Bacteriol. 1992; 42: 178-181Crossref PubMed Scopus (54) Google Scholar]. Recently, the complete genome sequence of C. urealyticum has been determined [10Tauch A Trost E Tilker A et al.The lifestyle of Corynebacterium urealyticum derived from its complete genome sequence established by pyrosequencing.J Biotechnol. 2008; (in press).Crossref Scopus (72) Google Scholar]. Interpretation of genome sequences requires a 'Rosetta Stone' to decode biological information in the finest detail, just as the deciphering of the ancient Egyptian hieroglyphics required the original Rosetta Stone. The combination of genomics and bioinformatics constitutes a discipline that has now been applied to understanding the genome of a stone-forming bacterial pathogen. The taxonomic classification of C. urealyticum (CDC coryneform group D2) was originally based on biochemical characteristics [9Pitcher D Soto A Soriano F Valero-Guillén P Classification of coryneform bacteria associated with human urinary tract infections (group D2) as Corynebacterium urealyticum sp. nov.Int J Syst Bacteriol. 1992; 42: 178-181Crossref PubMed Scopus (54) Google Scholar,11Herrera-Alcaraz EA Valero-Guillén PL Martín-Luengo F Soriano F Taxonomic implications of the chemical analysis of the D2 group of corynebacteria.FEMS Microbiol Lett. 1990; 60: 341-344Crossref PubMed Google Scholar,12Riegel P Grimont PAD de Briel D et al.Corynebacterium group D2 ('Corynebacterium urealyticum') constitutes a new genomic species.Res Microbiol. 1992; 143: 307-313Crossref PubMed Scopus (10) Google Scholar]. The cell wall peptidoglycan of C. urealyticum contains meso-diaminopimelic acid, and arabinose and galactose are the major cell wall sugars. The major menaquinone is MK-9(H2). Tuberculostearic acid and short-chain mycolic acids (C26–C36) are present [11Herrera-Alcaraz EA Valero-Guillén PL Martín-Luengo F Soriano F Taxonomic implications of the chemical analysis of the D2 group of corynebacteria.FEMS Microbiol Lett. 1990; 60: 341-344Crossref PubMed Google Scholar,13Couderc F de Briel D Demont N Gilard V Promé JC Mass spectrometry as a tool for identifying group D2 corynebacteria by their fatty acid profiles.J Gen Microbiol. 1991; 137: 1903-1909Crossref PubMed Scopus (15) Google Scholar]. Members of the species C. urealyticum are characterized by their potent ability to hydrolyze urea [5Soriano F Ponte C Santamaría M et al.Corynebacterium group D2 as a cause of alkaline-encrusted cystitis: report of four cases and characterization of the organism.J Clin Microbiol. 1985; 21: 788-792Crossref PubMed Google Scholar,14van Bosterhaut B Claeys G Gigi J Wauters G Isolation of Corynebacterium group D2 from clinical specimens.Eur J Clin Microbiol. 1987; 6: 418-419Crossref PubMed Scopus (28) Google Scholar] and by their failure to produce acid from carbohydrates [9Pitcher D Soto A Soriano F Valero-Guillén P Classification of coryneform bacteria associated with human urinary tract infections (group D2) as Corynebacterium urealyticum sp. nov.Int J Syst Bacteriol. 1992; 42: 178-181Crossref PubMed Scopus (54) Google Scholar,14van Bosterhaut B Claeys G Gigi J Wauters G Isolation of Corynebacterium group D2 from clinical specimens.Eur J Clin Microbiol. 1987; 6: 418-419Crossref PubMed Scopus (28) Google Scholar]. Moreover, DNA–DNA hybridization studies [9Pitcher D Soto A Soriano F Valero-Guillén P Classification of coryneform bacteria associated with human urinary tract infections (group D2) as Corynebacterium urealyticum sp. nov.Int J Syst Bacteriol. 1992; 42: 178-181Crossref PubMed Scopus (54) Google Scholar,12Riegel P Grimont PAD de Briel D et al.Corynebacterium group D2 ('Corynebacterium urealyticum') constitutes a new genomic species.Res Microbiol. 1992; 143: 307-313Crossref PubMed Scopus (10) Google Scholar] and 16S rRNA sequence analysis [15Pascual C Lawson PA Farrow JAE Navarro Gimenez M Collins MD Phylogenetic analysis of the genus Corynebacterium based on 16S rRNA gene sequences.Int J Syst Bacteriol. 1995; 45: 724-728Crossref PubMed Scopus (146) Google Scholar,16Ruimy R Riegel P Boiron P Monteil H Christen R Phylogeny of the genus Corynebacterium deduced from analyses of small-subunit ribosomal DNA sequences.Int J Syst Bacteriol. 1995; 45: 740-746Crossref PubMed Scopus (89) Google Scholar] were used to determine the degree of relatedness of C. urealyticum to other corynebacterial species. On the basis of small-subunit rRNA sequence data, a close phylogenetic relationship between C. urealyticum and C. jeikeium was observed [15Pascual C Lawson PA Farrow JAE Navarro Gimenez M Collins MD Phylogenetic analysis of the genus Corynebacterium based on 16S rRNA gene sequences.Int J Syst Bacteriol. 1995; 45: 724-728Crossref PubMed Scopus (146) Google Scholar,16Ruimy R Riegel P Boiron P Monteil H Christen R Phylogeny of the genus Corynebacterium deduced from analyses of small-subunit ribosomal DNA sequences.Int J Syst Bacteriol. 1995; 45: 740-746Crossref PubMed Scopus (89) Google Scholar]. More recently, this analysis was complemented by using partial sequences of the RNA polymerase beta-subunit gene (rpoB) in phylogenetic studies of corynebacteria [17Khamis A Raoult D La Scola B rpoB gene sequencing for identification of Corynebacterium species.J Clin Microbiol. 2004; 42: 3925-3931Crossref PubMed Scopus (214) Google Scholar,18Khamis A Raoult D La Scola B Comparison between rpoB and 16S rRNA gene sequencing for molecular identification of 168 clinical isolates of Corynebacterium.J Clin Microbiol. 2005; 43: 1934-1936Crossref PubMed Scopus (125) Google Scholar]. Both C. urealyticum and C. jeikeium are strict aerobes that exhibit lipid-requiring and multidrug-resistance phenotypes [19Funke G Bernard KA Coryneform Gram-positive rods.in: Murray PR Manual of clinical microbiology. 9th edn. ASM Press, Washington, DC2007: 485-514Google Scholar] and belong to a separate branch in the genus Corynebacterium [16Ruimy R Riegel P Boiron P Monteil H Christen R Phylogeny of the genus Corynebacterium deduced from analyses of small-subunit ribosomal DNA sequences.Int J Syst Bacteriol. 1995; 45: 740-746Crossref PubMed Scopus (89) Google Scholar,17Khamis A Raoult D La Scola B rpoB gene sequencing for identification of Corynebacterium species.J Clin Microbiol. 2004; 42: 3925-3931Crossref PubMed Scopus (214) Google Scholar]. However, C. jeikeium can be differentiated from C. urealyticum because it is non-urealytic and produces acid from glucose [19Funke G Bernard KA Coryneform Gram-positive rods.in: Murray PR Manual of clinical microbiology. 9th edn. ASM Press, Washington, DC2007: 485-514Google Scholar,20Jackman PJH Pitcher DG Pelczynska S Borman P Classification of corynebacteria associated with endocarditis (group JK) as Corynebacterium jeikeium sp. nov.Syst Appl Microbiol. 1987; 9: 83-90Crossref Scopus (68) Google Scholar]. A recent study demonstrated that cellular fatty acid analysis is a powerful method for the reliable identification and differentiation of corynebacterial species [21van den Velde S Lagrou K Desmet K Wauters G Verhaegen J Species identification of corynebacteria by cellular fatty acid analysis.Diagn Microbiol Infect Dis. 2006; 54: 99-104Crossref PubMed Scopus (23) Google Scholar]. The cellular fatty acid composition of C. urealyticum is consistent with that of the genus Corynebacterium, with the majority of cellular fatty acids being of the straight-chain, mono-unsaturated types [11Herrera-Alcaraz EA Valero-Guillén PL Martín-Luengo F Soriano F Taxonomic implications of the chemical analysis of the D2 group of corynebacteria.FEMS Microbiol Lett. 1990; 60: 341-344Crossref PubMed Google Scholar,21van den Velde S Lagrou K Desmet K Wauters G Verhaegen J Species identification of corynebacteria by cellular fatty acid analysis.Diagn Microbiol Infect Dis. 2006; 54: 99-104Crossref PubMed Scopus (23) Google Scholar]. In addition, small amounts of tuberculostearic acid were consistently detected in several studies [11Herrera-Alcaraz EA Valero-Guillén PL Martín-Luengo F Soriano F Taxonomic implications of the chemical analysis of the D2 group of corynebacteria.FEMS Microbiol Lett. 1990; 60: 341-344Crossref PubMed Google Scholar,13Couderc F de Briel D Demont N Gilard V Promé JC Mass spectrometry as a tool for identifying group D2 corynebacteria by their fatty acid profiles.J Gen Microbiol. 1991; 137: 1903-1909Crossref PubMed Scopus (15) Google Scholar,21van den Velde S Lagrou K Desmet K Wauters G Verhaegen J Species identification of corynebacteria by cellular fatty acid analysis.Diagn Microbiol Infect Dis. 2006; 54: 99-104Crossref PubMed Scopus (23) Google Scholar]. A comparative study on the phospholipid composition of C. urealyticum, C. jeikeium and C. amycolatum strains revealed significant differences related to the acyl chains of the glycerol moiety of these compounds, and most notably, the presence of high levels of a 10-methyleneoctadecanoyl moiety in the detected inositol-containing phospholipids of C. urealyticum [22Yagüe G Segovia M Valero-Guillén PL Phospholipid composition of several clinically relevant Corynebacterium species as determined by mass spectrometry: an unusual fatty acyl moiety is present in inositol-containing phospholipids of Corynebacterium urealyticum.Microbiology. 2003; 149: 1675-1685Crossref PubMed Scopus (25) Google Scholar]. DNA–DNA hybridization studies for intraspecies comparison revealed tight hybridization groups of C. urealyticum strains that were distinct from validly established species [9Pitcher D Soto A Soriano F Valero-Guillén P Classification of coryneform bacteria associated with human urinary tract infections (group D2) as Corynebacterium urealyticum sp. nov.Int J Syst Bacteriol. 1992; 42: 178-181Crossref PubMed Scopus (54) Google Scholar,12Riegel P Grimont PAD de Briel D et al.Corynebacterium group D2 ('Corynebacterium urealyticum') constitutes a new genomic species.Res Microbiol. 1992; 143: 307-313Crossref PubMed Scopus (10) Google Scholar]. The high levels of interstrain DNA homology were consistent with the criterion of a homogenous species. Ribotyping (rRNA gene restriction length polymorphism) of C. urealyticum strains from urine samples and skin infections was used for epidemiological tracking [23Soto A Pitcher DG Soriano F A numerical analysis of ribosomal RNA gene patterns for typing clinical isolates of Corynebacterium group D2.Epidemiol Infect. 1991; 107: 263-272Crossref PubMed Scopus (10) Google Scholar]. The C. urealyticum isolates were remarkably homogenous and could be assigned to eight clusters only, despite the deliberate use of strains from a variety of sources. Comparison by ribotyping of C. urealyticum strains from human-related and animal-related sources revealed predominant ribotypes for each group of isolates [24Nieto E Vindel A Valero-Guillén PL Saéz-Nieto JA Soriano F Biochemical, antimicrobial susceptibility and genotyping studies on Corynebacterium urealyticum isolates from diverse sources.J Med Microbiol. 2000; 49: 759-763Crossref PubMed Scopus (15) Google Scholar]. Some ribotypes were found only in strains from human-related sources, whereas others were obtained only from isolates from animal-related sources. Two isolates with different antimicrobial susceptibilities exhibited an identical ribotype, indicating that the genotypic profile is more stable than the antibiogram [24Nieto E Vindel A Valero-Guillén PL Saéz-Nieto JA Soriano F Biochemical, antimicrobial susceptibility and genotyping studies on Corynebacterium urealyticum isolates from diverse sources.J Med Microbiol. 2000; 49: 759-763Crossref PubMed Scopus (15) Google Scholar]. Very recently, the complete genome sequence of the type strain C. urealyticum DSM7109 (NCTC 12011; ATCC 43042) [9Pitcher D Soto A Soriano F Valero-Guillén P Classification of coryneform bacteria associated with human urinary tract infections (group D2) as Corynebacterium urealyticum sp. nov.Int J Syst Bacteriol. 1992; 42: 178-181Crossref PubMed Scopus (54) Google Scholar] has been determined by a combination of ultrafast pyrosequencing and Sanger technology [10Tauch A Trost E Tilker A et al.The lifestyle of Corynebacterium urealyticum derived from its complete genome sequence established by pyrosequencing.J Biotechnol. 2008; (in press).Crossref Scopus (72) Google Scholar,25Tauch A Trost E Bekel T Goesmann A Ludewig U Pühler A Ultrafast de novo sequencing of Corynebacterium urealyticum using the Genome Sequencer 20 System.Biochemica. 2006; 4: 4-6Google Scholar]. The genome of C. urealyticum DSM7109 consists of a circular chromosome with a size of 2 369 219 bp and a mean G + C content of 64.2%, which is close to the value of 62% that was determined previously by the thermal DNA denaturation method [9Pitcher D Soto A Soriano F Valero-Guillén P Classification of coryneform bacteria associated with human urinary tract infections (group D2) as Corynebacterium urealyticum sp. nov.Int J Syst Bacteriol. 1992; 42: 178-181Crossref PubMed Scopus (54) Google Scholar]. Genome annotation revealed 2024 protein-coding sequences, of which 78% were considered to be orthologues of genes in the C. jeikeium K411 genome. The close phylogenetic relationship between C. urealyticum and C. jeikeium is also reflected by the highly conserved order of orthologous genes and the presence of only two breakpoints in the architecture of the chromosome [10Tauch A Trost E Tilker A et al.The lifestyle of Corynebacterium urealyticum derived from its complete genome sequence established by pyrosequencing.J Biotechnol. 2008; (in press).Crossref Scopus (72) Google Scholar]. Metabolic analysis of the genome sequence provided clear evidence that the lipid-requiring ('lipophilic') phenotype of C. urealyticum is attributable to the absence of a microbial type I fatty acid synthase gene and thus represents a fatty acid auxotrophy [10Tauch A Trost E Tilker A et al.The lifestyle of Corynebacterium urealyticum derived from its complete genome sequence established by pyrosequencing.J Biotechnol. 2008; (in press).Crossref Scopus (72) Google Scholar]. In addition, C. urealyticum is apparently unable to utilize sugars as carbon and energy sources because of the absence of characteristic sugar uptake systems and the absence of genes for anaplerotic functions. Accordingly, exogenous fatty acids are required not only to supplement the fatty acid auxotrophy, but also to serve as sources of carbon and energy for C. urealyticum. The utilization of exogenous fatty acids occurs via the β-oxidation pathway and a large repertoire of auxiliary genes involved in uptake and degradation of structurally diverse fatty acid compounds [10Tauch A Trost E Tilker A et al.The lifestyle of Corynebacterium urealyticum derived from its complete genome sequence established by pyrosequencing.J Biotechnol. 2008; (in press).Crossref Scopus (72) Google Scholar]. This comprehensive gene repertoire reflects the adaptation of C. urealyticum to those habitats on the human skin that provide an appropriate amount of exogenous fatty acids for growth. The urease genes of C. urealyticum DSM7109 are organized in a cluster with the order ure-ABCEFGD, and seem to play the dominant role in the pathogenicity of this species [10Tauch A Trost E Tilker A et al.The lifestyle of Corynebacterium urealyticum derived from its complete genome sequence established by pyrosequencing.J Biotechnol. 2008; (in press).Crossref Scopus (72) Google Scholar]. 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Adherence of C. glutamicum to host tissues may be mediated by a proteinaceous pilus that is covalently anchored to the cell wall and encoded by the structural genes spaDEF and the cognate sortase genes srtBC in C. urealyticum DSM7109 [10Tauch A Trost E Tilker A et al.The lifestyle of Corynebacterium urealyticum derived from its complete genome sequence established by pyrosequencing.J Biotechnol. 2008; (in press).Crossref Scopus (72) Google Scholar]. 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