FEMS Pathogens and Disease, 73, 2015, 1–3 doi: 10.1093/femspd/ftu008 Advance Access Publication Date: 4 December 2014 Commentary
COMMENTARY
Two more species of Chlamydia–does it make a difference? Konrad Sachse1,∗ and Karine Laroucau2 1
Friedrich-Loeffler-Institut (Federal Research Institute for Animal Health), Institute of Molecular Pathogenesis, Naumburger Str. 96a, 07743 Jena, Germany and 2 University Paris-Est, Anses, Animal Health Laboratory, ´ eral ´ Bacterial Zoonoses Unit 23, avenue du gen de Gaulle, 94706 Maisons-Alfort, France ∗ Corresponding author: Friedrich-Loeffler-Institut (Federal Research Institute for Animal Health), Institute of Molecular Pathogenesis, Naumburger Str. 96a, 07743 Jena, Germany. Tel: +0049-3641-8042334; E-mail: [email protected] One sentence Summary: This commentary explains the implications of the recent introduction of two new Chlamydia spp. Editor: Viviane Bremer
ABSTRACT The recent description of Chlamydia (C.) avium and C. gallinacea as new species of the reunited genus Chlamydia can be expected to have implications on the perception of avian chlamydiosis. We discuss possible effects on epidemiology, diagnosis and our understanding of aetiopathogenesis resulting from this discovery. Key words: Chlamydia; C. avium; C. gallinacea
The recent description of Chlamydia (C.) avium and C. gallinacea as new species of the reunited genus Chlamydia (Sachse et al., 2014) can be expected to have immediate implications on the perception of avian chlamydiosis as an economically important disease and the assessment of its zoonotic potential. Firstly, the aetiopathogenesis of avian chlamydiosis (also known as psittacosis, ornithosis or parrot fever) can be revised. C. psittaci is no longer the only possible causative agent, but, depending on the avian host, two more chlamydial players should be taken into account. C. gallinacea can be encountered in domestic poultry, guinea fowl, turkeys, ducks and probably other birds, while C. avium has so far been found in pigeons and psittacines. The pathogenicity of the new species has yet to be investigated. The few data available suggest that C. avium was capable of causing respiratory disease in parrots and pigeons (Sachse et al., 2014). Concerning C. gallinacea, no pathological case has been documented yet as either the positive chickens showed no clinical signs or other bacterial pathogens were also present. It could be speculated that C. gallinacea was just a commensal in poultry as its regular
natural host, but the situation in other avian hosts may be different. It would be interesting to revisit previous outbreaks of avian chlamydiosis and check for the presence and possible contribution of the new species, especially in those cases where the diagnostic testing stopped at the Chlamydiaceae level. This also applies to human cases of psittacosis. In an earlier study, three workers of a French slaughterhouse who had previously handled C. gallinacea-infected chickens showed signs of atypical pneumonia (Laroucau et al., 2009). Thus, a zoonotic potential has to be considered as well, even though previous exposure of these individuals to C. psittaci cannot be ruled out. Secondly, the observations leading to the discovery of the new species suggest a substantial prevalence of dual infections including other members of the Chlamydiaceae family. This seems to be a common phenomenon in the chlamydial area (Pantchev et al., 2010; Dean et al., 2013). C. avium or C. gallinacea were repeatedly detected alongside C. psittaci in the same flock and even in the same bird (KrautwaldJunghanns et al., 2013; Laroucau et al., 2014), which raises interesting questions on their interplay in the course of
Received: 5 September 2014; Accepted: 20 October 2014 C FEMS 2014. All rights reserved. For permissions, please e-mail: [email protected]
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FEMS Pathogens and Disease, 2015, Vol. 73, No. 1
Figure 1. Phylogenetic reconstruction based on complete 16S rRNA genes from type strains of all established Chlamydiceae spp. including the new species of C. avium and C. gallinacea. Construction of the tree was based on the Jukes–Cantor genetic distance model using the neighbour-joining algorithm with Waddlia chondrophila as outgroup. Bootstrap values indicate the stability of the branches based on 100 replicates. The bar represents 2% sequence divergence.
infection and, finally, their individual contribution to pathology and sequelae. Future research should address dual and multiple bacterial infections in order to identify possible synergies or competitive and inhibitory effects between individual agents. Thirdly, the epidemiology of avian chlamydiosis is becoming more complex in the light of the introduction of two more chlamydial species. It is no longer correct to ascribe chlamydial infections in birds automatically to C. psittaci. In fact, the classical causative agent of psittacosis may be completely absent in flocks testing positive for Chlamydiaceae as shown in a previous survey (Laroucau et al., 2009). The prevalence of C. gallinacea can even be higher than that of C. psittaci, as recently shown in a study of poultry and turkey flocks from four European countries and China (Zocevic et al., 2012). Data from a survey in breeder pigeons in Germany revealed that C. avium was present in 4 of 27 (14.8%) flocks (Krautwald-Junghanns et al., 2013), while in France, 10 of 125 (8%) Chlamydiaceae-positive samples from urban pigeons proved positive for the agent (Gasparini et al., 2011). Its general prevalence in psittacine birds cannot be
assessed yet since the findings reported so far represent individual cases. Fourthly, the diagnostic approach to avian chlamydial infections (and chlamydial infections in general) should be updated. Detection assays for C. gallinacea (Zocevic et al., 2012) and C. avium (Zocevic et al., 2013) using real-time PCR have already been published, and a DNA microarray covering all Chlamydiaceae spp. (Borel et al., 2008) has meanwhile been extended to include the new species (Schnee and Sachse 2014). In any case, species-specific assays should be used to unambiguously identify the agent(s) involved. Assays based on parallel detection technology, such as DNA microarray, are ideally suited to retrieve unexpected chlamydial species and reveal cases of multiple infections. All in all, the Chlamydia landscape has been further enriched through the addition of two species (see Fig. 1). A new and interesting area is opening up to researchers. The elucidation of pathogenicity mechanisms, identification of virulence characteristics, comparative genomics, intra-species genetic and phenotypic variability, as well as systematic studies on
Sachse and Laroucau
epidemiology, zoonotic transmission and host–pathogen interactions should be placed on the short-term agenda. Conflict of interest statement. None declared.
REFERENCES Borel N, Kempf E, Hotzel H, et al. Direct identification of chlamydiae from clinical samples using a DNA microarray assay: a validation study. Mol Cell Probe 2008;22: 55–64. Dean D, Rothschild J, Ruettger A, et al. Zoonotic Chlamydiaceae species associated with trachoma, Nepal. Emerg Infect Dis 2013;19:1948–55. Gasparini J, Erin N, Bertin C, et al. Impact of urban environment and host phenotype on the epidemiology of Chlamydiaceae in feral pigeons (Columba livia). Environ Microbiol 2011;13: 3186–93. Krautwald-Junghanns ME, Stolze J, Schmidt V, et al. [Efficacy of doxycyclin for chlamydiosis in pigeon flocks] in German. ¨ Tierarztl Praxis 2013;41:392–8. Laroucau K, Aaziz R, Meurice L Outbreak of psittacosis in a group of women exposed to Chlamydia psittaci- infected chickens. Eurosurveillance, in press [EMID:ce1270d610605ffb].
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Laroucau K, Vorimore F, Aaziz R, et al. Isolation of a new chlamydial agent from infected domestic poultry coincided with cases of atypical pneumonia among slaughterhouse workers in France. Infect Genet Evol 2009;9:1240–7. Pantchev A, Sting R, Bauerfeind R, et al. Detection of all Chlamydophila and Chlamydia spp. of veterinary interest using species-specific real-time PCR assays. Comp Immunol Microb 2010;33:473–84. Sachse K, Laroucau K, Riege K, et al. Evidence for the existence of two new members of the family Chlamydiaceae and proposal of Chlamydia avium sp. nov. and Chlamydia gallinacea sp. nov. Syst Appl Microbiol 2014;37:79–88. Schnee C, Sachse K (2014) DNA microarray-based detection of multiple pathogens: Mycoplasma spp. and Chlamydia spp. In: ´ Cunha MV, Inacio J (eds). Methods in Molecular Biology, Vol. XXX: Molecular Diagnosis in Veterinary Laboratory Practice— Reviews and Protocols, Chapter 14 (in press). Zocevic A, Vorimore F, Marhold C, et al. Molecular characterization of atypical Chlamydia and evidence of their dissemination in different European and Asian chicken flocks by specific real-time PCR. Environ Microbiol 2012;14:2212–22. Zocevic A, Vorimore F, Vicari N, et al. A real-time PCR assay for the detection of atypical strains of Chlamydiaceae from pigeons. PLoS One 2013;8:e58741.
COMMENTARY
Two more species of Chlamydia–does it make a difference? Konrad Sachse1,∗ and Karine Laroucau2 1
Friedrich-Loeffler-Institut (Federal Research Institute for Animal Health), Institute of Molecular Pathogenesis, Naumburger Str. 96a, 07743 Jena, Germany and 2 University Paris-Est, Anses, Animal Health Laboratory, ´ eral ´ Bacterial Zoonoses Unit 23, avenue du gen de Gaulle, 94706 Maisons-Alfort, France ∗ Corresponding author: Friedrich-Loeffler-Institut (Federal Research Institute for Animal Health), Institute of Molecular Pathogenesis, Naumburger Str. 96a, 07743 Jena, Germany. Tel: +0049-3641-8042334; E-mail: [email protected] One sentence Summary: This commentary explains the implications of the recent introduction of two new Chlamydia spp. Editor: Viviane Bremer
ABSTRACT The recent description of Chlamydia (C.) avium and C. gallinacea as new species of the reunited genus Chlamydia can be expected to have implications on the perception of avian chlamydiosis. We discuss possible effects on epidemiology, diagnosis and our understanding of aetiopathogenesis resulting from this discovery. Key words: Chlamydia; C. avium; C. gallinacea
The recent description of Chlamydia (C.) avium and C. gallinacea as new species of the reunited genus Chlamydia (Sachse et al., 2014) can be expected to have immediate implications on the perception of avian chlamydiosis as an economically important disease and the assessment of its zoonotic potential. Firstly, the aetiopathogenesis of avian chlamydiosis (also known as psittacosis, ornithosis or parrot fever) can be revised. C. psittaci is no longer the only possible causative agent, but, depending on the avian host, two more chlamydial players should be taken into account. C. gallinacea can be encountered in domestic poultry, guinea fowl, turkeys, ducks and probably other birds, while C. avium has so far been found in pigeons and psittacines. The pathogenicity of the new species has yet to be investigated. The few data available suggest that C. avium was capable of causing respiratory disease in parrots and pigeons (Sachse et al., 2014). Concerning C. gallinacea, no pathological case has been documented yet as either the positive chickens showed no clinical signs or other bacterial pathogens were also present. It could be speculated that C. gallinacea was just a commensal in poultry as its regular
natural host, but the situation in other avian hosts may be different. It would be interesting to revisit previous outbreaks of avian chlamydiosis and check for the presence and possible contribution of the new species, especially in those cases where the diagnostic testing stopped at the Chlamydiaceae level. This also applies to human cases of psittacosis. In an earlier study, three workers of a French slaughterhouse who had previously handled C. gallinacea-infected chickens showed signs of atypical pneumonia (Laroucau et al., 2009). Thus, a zoonotic potential has to be considered as well, even though previous exposure of these individuals to C. psittaci cannot be ruled out. Secondly, the observations leading to the discovery of the new species suggest a substantial prevalence of dual infections including other members of the Chlamydiaceae family. This seems to be a common phenomenon in the chlamydial area (Pantchev et al., 2010; Dean et al., 2013). C. avium or C. gallinacea were repeatedly detected alongside C. psittaci in the same flock and even in the same bird (KrautwaldJunghanns et al., 2013; Laroucau et al., 2014), which raises interesting questions on their interplay in the course of
Received: 5 September 2014; Accepted: 20 October 2014 C FEMS 2014. All rights reserved. For permissions, please e-mail: [email protected]
1
2
FEMS Pathogens and Disease, 2015, Vol. 73, No. 1
Figure 1. Phylogenetic reconstruction based on complete 16S rRNA genes from type strains of all established Chlamydiceae spp. including the new species of C. avium and C. gallinacea. Construction of the tree was based on the Jukes–Cantor genetic distance model using the neighbour-joining algorithm with Waddlia chondrophila as outgroup. Bootstrap values indicate the stability of the branches based on 100 replicates. The bar represents 2% sequence divergence.
infection and, finally, their individual contribution to pathology and sequelae. Future research should address dual and multiple bacterial infections in order to identify possible synergies or competitive and inhibitory effects between individual agents. Thirdly, the epidemiology of avian chlamydiosis is becoming more complex in the light of the introduction of two more chlamydial species. It is no longer correct to ascribe chlamydial infections in birds automatically to C. psittaci. In fact, the classical causative agent of psittacosis may be completely absent in flocks testing positive for Chlamydiaceae as shown in a previous survey (Laroucau et al., 2009). The prevalence of C. gallinacea can even be higher than that of C. psittaci, as recently shown in a study of poultry and turkey flocks from four European countries and China (Zocevic et al., 2012). Data from a survey in breeder pigeons in Germany revealed that C. avium was present in 4 of 27 (14.8%) flocks (Krautwald-Junghanns et al., 2013), while in France, 10 of 125 (8%) Chlamydiaceae-positive samples from urban pigeons proved positive for the agent (Gasparini et al., 2011). Its general prevalence in psittacine birds cannot be
assessed yet since the findings reported so far represent individual cases. Fourthly, the diagnostic approach to avian chlamydial infections (and chlamydial infections in general) should be updated. Detection assays for C. gallinacea (Zocevic et al., 2012) and C. avium (Zocevic et al., 2013) using real-time PCR have already been published, and a DNA microarray covering all Chlamydiaceae spp. (Borel et al., 2008) has meanwhile been extended to include the new species (Schnee and Sachse 2014). In any case, species-specific assays should be used to unambiguously identify the agent(s) involved. Assays based on parallel detection technology, such as DNA microarray, are ideally suited to retrieve unexpected chlamydial species and reveal cases of multiple infections. All in all, the Chlamydia landscape has been further enriched through the addition of two species (see Fig. 1). A new and interesting area is opening up to researchers. The elucidation of pathogenicity mechanisms, identification of virulence characteristics, comparative genomics, intra-species genetic and phenotypic variability, as well as systematic studies on
Sachse and Laroucau
epidemiology, zoonotic transmission and host–pathogen interactions should be placed on the short-term agenda. Conflict of interest statement. None declared.
REFERENCES Borel N, Kempf E, Hotzel H, et al. Direct identification of chlamydiae from clinical samples using a DNA microarray assay: a validation study. Mol Cell Probe 2008;22: 55–64. Dean D, Rothschild J, Ruettger A, et al. Zoonotic Chlamydiaceae species associated with trachoma, Nepal. Emerg Infect Dis 2013;19:1948–55. Gasparini J, Erin N, Bertin C, et al. Impact of urban environment and host phenotype on the epidemiology of Chlamydiaceae in feral pigeons (Columba livia). Environ Microbiol 2011;13: 3186–93. Krautwald-Junghanns ME, Stolze J, Schmidt V, et al. [Efficacy of doxycyclin for chlamydiosis in pigeon flocks] in German. ¨ Tierarztl Praxis 2013;41:392–8. Laroucau K, Aaziz R, Meurice L Outbreak of psittacosis in a group of women exposed to Chlamydia psittaci- infected chickens. Eurosurveillance, in press [EMID:ce1270d610605ffb].
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Laroucau K, Vorimore F, Aaziz R, et al. Isolation of a new chlamydial agent from infected domestic poultry coincided with cases of atypical pneumonia among slaughterhouse workers in France. Infect Genet Evol 2009;9:1240–7. Pantchev A, Sting R, Bauerfeind R, et al. Detection of all Chlamydophila and Chlamydia spp. of veterinary interest using species-specific real-time PCR assays. Comp Immunol Microb 2010;33:473–84. Sachse K, Laroucau K, Riege K, et al. Evidence for the existence of two new members of the family Chlamydiaceae and proposal of Chlamydia avium sp. nov. and Chlamydia gallinacea sp. nov. Syst Appl Microbiol 2014;37:79–88. Schnee C, Sachse K (2014) DNA microarray-based detection of multiple pathogens: Mycoplasma spp. and Chlamydia spp. In: ´ Cunha MV, Inacio J (eds). Methods in Molecular Biology, Vol. XXX: Molecular Diagnosis in Veterinary Laboratory Practice— Reviews and Protocols, Chapter 14 (in press). Zocevic A, Vorimore F, Marhold C, et al. Molecular characterization of atypical Chlamydia and evidence of their dissemination in different European and Asian chicken flocks by specific real-time PCR. Environ Microbiol 2012;14:2212–22. Zocevic A, Vorimore F, Vicari N, et al. A real-time PCR assay for the detection of atypical strains of Chlamydiaceae from pigeons. PLoS One 2013;8:e58741.
