Is Genetically Diverse in Animals and Appears to Have Crossed the Host Barrier to Humans on (At Least) Two Occasions
Chlamydia pneumoniae is a common human and animal pathogen associated with a wide range of diseases. Since the first isolation of C. pneumoniae TWAR in 1965, all human isolates have been essentially clonal, providing little evolutionary insight. To address this gap, we investigated the genetic diversity of 30 isolates from diverse geographical locations, from both human and animal origin (amphibian, reptilian, equine and marsupial). Based on the level of variation that we observed at 23 discreet gene loci, it was clearly evident that the animal isolates were more diverse than the isolates of human origin. Furthermore, we show that C. pneumoniae isolates could be grouped into five major genotypes, A-E, with A, B, D and E genotypes linked by geographical location, whereas genotype C was found across multiple continents. Our evidence strongly supports two separate animal-to-human cross species transfer events in the evolutionary history of this pathogen. The C. pneumoniae human genotype identified in the USA, Canada, Taiwan, Iran, Japan, Korea and Australia (non-Indigenous) most likely originated from a single amphibian or reptilian lineage, which appears to have been previously geographically widespread. We identified a separate human lineage present in two Australian Indigenous isolates (independent geographical locations). This lineage is distinct and is present in Australian amphibians as well as a range of Australian marsupials.
Vyšlo v časopise:
Is Genetically Diverse in Animals and Appears to Have Crossed the Host Barrier to Humans on (At Least) Two Occasions. PLoS Pathog 6(5): e32767. doi:10.1371/journal.ppat.1000903
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000903
Souhrn
Chlamydia pneumoniae is a common human and animal pathogen associated with a wide range of diseases. Since the first isolation of C. pneumoniae TWAR in 1965, all human isolates have been essentially clonal, providing little evolutionary insight. To address this gap, we investigated the genetic diversity of 30 isolates from diverse geographical locations, from both human and animal origin (amphibian, reptilian, equine and marsupial). Based on the level of variation that we observed at 23 discreet gene loci, it was clearly evident that the animal isolates were more diverse than the isolates of human origin. Furthermore, we show that C. pneumoniae isolates could be grouped into five major genotypes, A-E, with A, B, D and E genotypes linked by geographical location, whereas genotype C was found across multiple continents. Our evidence strongly supports two separate animal-to-human cross species transfer events in the evolutionary history of this pathogen. The C. pneumoniae human genotype identified in the USA, Canada, Taiwan, Iran, Japan, Korea and Australia (non-Indigenous) most likely originated from a single amphibian or reptilian lineage, which appears to have been previously geographically widespread. We identified a separate human lineage present in two Australian Indigenous isolates (independent geographical locations). This lineage is distinct and is present in Australian amphibians as well as a range of Australian marsupials.
Zdroje
1. GraystonJT
1965 Immunisation against trachoma. Pan Am Health Organ Sci Publ 147 549
2. StoreyCC
LusherM
YatesP
RichmondSJ
1993 Evidence for Chlamydia pneumoniae of non-human origin. J Gen Microbiol 139 2621 2626
3. BodettiTJ
JacobsonE
WanC
HafnerL
PospischilA
2002 Molecular evidence to support the expansion of the host range of Chlamydophila pneumoniae to include reptiles as well as humans, horses, koalas and amphibians. Syst App Microbiol 25 146 152
4. BergerL
VolpK
MathewsS
SpeareR
TimmsP
1999 Chlamydia pneumoniae in a free-ranging giant barred frog (Mixophyes iteratus) from Australia. J Clin Microbiol 37 2378 2380
5. HotzelH
GrossmannE
MutschmannF
SachseK
2001 Genetic characterization of a Chlamydophila pneumoniae isolate from an African frog and comparison to currently accepted biovars. Syst Appl Microbiol 24 63 66
6. WardropS
FowlderA
O'CallaghanP
GiffardP
TimmsP
1999 Characterization of the koala biovar of Chlamydia pneumoniae at four gene loci–ompAVD4, ompB, 16S rRNA, groESL spacer region. Syst Appl Microbiol 22 22 27
7. KutlinA
RoblinPM
KumarS
KohlhoffS
BodettiT
2007 Molecular characterization of Chlamydophila pneumoniae isolates from Western barred bandicoots. J Med Microbiol 56 407 417
8. GraystonJT
2000 Background and current knowledge of Chlamydia pneumoniae and atherosclerosis. J Infect Dis 181 Suppl 3 S402 S410
9. KuoCC
JacksonLA
CampbellLA
GraysonJT
1995 Chlamydia pneumoniae TWAR. Clin Microbiol Rev 8 451 461
10. SaikkuP
LeinonenM
MattilaK
EkmanMR
NieminenMS
1988 Serological evidence of an association of a novel Chlamydia, TWAR, with chronic coronary heart disease and acute myocardial infarction. Lancet 2 983 986
11. WesslenL
PahlsonC
FrimanG
FohlmanJ
LindquistO
1992 Myocarditis caused by Chlamydia pneumoniae (TWAR) and sudden unexpected death in a Swedish elite orienteer. Lancet 340 427 428
12. SriramS
MitchellW
StrattonC
1998 Multiple sclerosis associated with Chlamydia pneumoniae infection of the CNS. Neurology 50 571 572
13. BalinBJ
GerardHC
ArkingEJ
AppeltDM
BraniganPJ
1998 Identification and localization of Chlamydia pneumoniae in the Alzheimer's brain. Med Microbiol Immunol 187 23 42
14. ReadTD
BrunhamRC
ShenC
GillSR
HeidelbergJF
2000 Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res 6 1397 1406
15. KalmanS
MitchellW
MaratheR
LammelC
FanJ
1999 Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nature Genetics 21 385 389
16. ShiraiM
KirakawaH
KimotoM
TabuchiM
KishiF
2000 Comparison of whole genome sequences of Chlamydia pneumoniae J138 from Japan and CWL029 from USA. Nucleic Acids Res 12 2311 2314
17. GengMM
SchuhmacherA
MuehldorferI
BenschKW
SchaeferKP
2003 The genome sequence of Chlamydia pneumoniae TW183 and comparison with other Chlamydia strains based on whole genome sequence analysis. Genbank Accession No AE009440
18. RatteiT
OttS
GutackerM
RuppJ
MaassM
2007 Genetic diversity of the obligate intracellular bacterium Chlamydophila pneumoniae by genome-wide analysis of single nucleotide polymorphisms: evidence for highly clonal population structure. BMC Genomics 8 355
19. PeelingRW
BrunhamRC
1996 Chlamydiae as pathogens: new species and new issues. Emerg Infect Dis 2 307 319
20. WillsJM
WatsonG
LusherM
MairTS
WoodD
1990 Characterisation of Chlamydia psittaci isolated from a horse. Vet Microbiol 24 11 19
21. GlassickT
GiffardP
TimmsP
1996 Outer membrane protein 2 gene sequence indicates that Chlamydia pecorum and Chlamydia pneumoniae cause infection in koalas. Syst Appl Microbiol 19 457 464
22. MyersGSA
MathewsSA
EppingerM
MitchellC
O'BrienKK
2009 Evidence that human Chlamydia pneumoniae was zoonotically acquired. J Bacteriol 191 7225 7233
23. AbromaitisS
HeftyPS
StephensRS
2009 Chlamydia pneumoniae encodes a functional aromatic amino acid hydroxylase. FEMS Immunol Med Microbiol 55 196 205
24. ZhangYX
FoxJG
HoY
ZhangL
StillsHFJr
1993 Comparison of the major outer-membrane protein (MOMP) gene of mouse pneuomonitis (MoPn) and hamster SFPD strains of Chlamydia trachomatis with other Chlamydia strains. Mol Biol Evol 10 1327 1342
25. StothardDR
BoguslawskiG
JonesRB
1998 Phylogenetic analysis of the Chlamydia trachomatis major outer membrane protein and examination of potential pathogenic determinants. Infect Immun 66 3618 3625
26. BrunelleBW
SensabaughGF
2006 The ompA gene in Chlamydia trachomatis differs in phylogeny and rate of evolution from other regions of the genome. Infect Immun 74 578 585
27. EverettKD
BushRM
AndersenAA
1999 Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. Int J Syst Bacteriol 49 415 440
28. ReedKD
RuthGR
MeyerJA
ShuklaSK
2000 Chlamydia pneumoniae infection in a breeding colony of African clawed frogs (Xenopus tropicalis). Emerg Infect Dis 6 196 199
29. PetterssonB
AnderssonA
LeitnerT
OlsvikO
UhlenM
1997 Evolutionary relationships among members of the genus Chlamydia based on 16S ribosomal DNA analysis. J Bacteriol 179 4195 4205
30. WilsonPA
PhippsJ
SamuelD
SaundersNA
1996 Development of a simplified polymerase chain reaction-enzyme immunoassay for the detection of Chlamydia pneumoniae. J Appl Bacteriol 80 431 438
31. KwonSJ
LeeKJ
ChoenDS
KimKS
LeeSJ
2004 The sequence of 16S rRNA of Korean isolate Chlamydia pneumoniae LKK-1. Unpublished 2004, Submitted (February-2004) to the EMBL/GenBank/DDBJ databases
32. HatchTP
AllanI
PearceJH
1984 Structural and polypeptide differences between envelopes of infective and reproductive life cycle forms of Chlamydia spp. J Bacteriol 157 13 20
33. ThomasNS
LusherM
StoreyCC
ClarkeIN
1997 Plasmid diversity in Chlamydia. Microbiol 143 1847 1854
34. GrayA
1988 Society and culture: demographic and social history.
JuppJ
The Australian people: An encyclopedia of the nation, its people and their origins Oakleigh Cambridge University press 88
35. MoorPE
CollignonPC
GilbertGL
1999 Pulsed-field gel electrophoresis used to investigate genetic diversity of Haemophilus influenzae type b isolates in Australia shows differences between Aboriginal and non-Aboriginal isolates. J Clin Microbiol 37 1524 1531
36. CochraneM
WalkerP
Gibbs
TimmsP
2005 Multiple genotypes of Chlamydia pneumoniae identified in human carotid plaque. Microbiol 151 2285 2290
37. RozenS
SkaletskyHJ
2000 Primer3 on the WWW for general users and for biologist programmers.
KrawetzS
MisenerS
Bioinformatics Methods and Protocols: Methods in Molecular Biology Totowa, NJ Humana Press 365 386
38. DrummondAJ
AshtonB
CheungM
HeledJ
KearseM
2007 Geneious version 4.7. Available: http://www.geneious.com/. Accessed 13 August 2009
39. DwyerRS
TreharneJD
JonesBR
HerringJ
1972 Chlamydial infection. Results of micro-immunofluorescence tests for the detection of type-specific antibody in certain chlamydial infections. Br J Vener Dis 48 452 459
40. ColesKA
TimmsP
SmithDW
2001 Koala biovar of Chlamydia pneumoniae infects human and koala monocytes and induces increased uptake of lipids in vitro. Infect Immun 69 7894 7897
41. Dreses-WerringloerU
BhuiyanM
ZhaoY
GerardHC
Whittum-HudsonJ
2008 Initial characterization of Chlamydophila (Chlamydia) pneumoniae cultured from the late-onset Alzheimer brain. Int J Med Microbiol 299 187 201
42. RamirezJA
1996 Isolation of Chlamydia pneumoniae from the coronary artery of a patient with coronary atherosclerosis. Ann Intern Med 125 979 982
43. LeeSJ
NamEC
WonJ
ParkWS
KimWJ
2003 Characterization of the first Korean isolate of a Chlamydia pneumoniae strain. J Infect Dis Japan 56 62 64
44. HuttonS
DoddH
1993 C. pneumoniae successfully isolated. Current topics 42 43
45. AscheVL
HuttonSI
DouglasFP
1993 Serological evidence of the three chlamydial species in an Aboriginal community in the Northern Territory. Med J Aust 158 606 604
46. WarrenK
SwanR
BodettiT
FriendT
HillS
2005 Ocular Chlamydiales infections of Western barred bandicoots (Perameles bougainville) in Western Australia. J Zoo Wildl Med 36 100 102
47. BlumerC
ZimmermannDR
WeilenmannR
VaughanL
PospischilA
2007 Chlamydiae in free-ranging and captive frogs in Switzerland. Vet Pathol 44 144 150
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 5
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Quorum Sensing Inhibition Selects for Virulence and Cooperation in
- The Role of Intestinal Microbiota in the Development and Severity of Chemotherapy-Induced Mucositis
- Susceptibility to Anthrax Lethal Toxin-Induced Rat Death Is Controlled by a Single Chromosome 10 Locus That Includes
- Demonstration of Cross-Protective Vaccine Immunity against an Emerging Pathogenic Ebolavirus Species