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      Genotypes and Mouse Virulence of Toxoplasma gondii Isolates from Animals and Humans in China

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          Abstract

          Background

          Recent population structure studies of T. gondii revealed that a few major clonal lineages predominated in different geographical regions. T. gondii in South America is genetically and biologically divergent, whereas this parasite is remarkably clonal in North America and Europe with a few major lineages including Types I, II and III. Information on genotypes and mouse virulence of T. gondii isolates from China is scarce and insufficient to investigate its population structure, evolution, and transmission.

          Methodology/Principal Findings

          Genotyping of 23 T. gondii isolates from different hosts using 10 markers for PCR-restriction fragment length polymorphism analyses (SAG1, SAG2, SAG3, BTUB, GRA6, c22-8, c29-2, L358, PK1 and Apico) revealed five genotypes; among them three genotypes were atypical and two were archetypal. Fifteen strains belong to the Chinese 1 lineage, which has been previously reported as a widespread lineage from swine, cats, and humans in China. Two human isolates fall into the type I and II lineages and the remaining isolates belong to two new atypical genotypes (ToxoDB#204 and #205) which has never been reported in China. Our results show that these genotypes of T. gondii isolates are intermediately or highly virulent in mice except for the strain TgCtwh6, which maintained parasitemia in mice for 35 days post infection although it possesses the uniform genotype of Chinese 1. Additionally, phylogenetic network analyses of all isolates of genotype Chinese 1 are identical, and there is no variation based on the sequence data generated for four introns (EF1, HP2, UPRT1 and UPRT7) and two dense granule proteins (GRA6 and GRA7).

          Conclusion/Significance

          A limited genetic diversity was found and genotype Chinese 1 (ToxoDB#9) is dominantly circulating in mainland China. The results will provide a useful profile for deep insight to the population structure, epidemiology and biological characteristics of T. gondii in China.

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          Most cited references35

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          Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease.

          D K Howe, L D Sibley (1995)
          The population genetic structure of Toxoplasma gondii was determined by multilocus restriction fragment length polymorphism analysis at 6 loci in 106 independent isolates from humans and animals. Phylogenetic and statistical analyses indicated a highly unusual population structure consisting of 3 widespread clonal lineages. Extensively mixed genotypes were only apparent in 4 strains, which indicated that, while not separate species, sexual recombination between the 3 lineages is exceedingly rare in natural populations. T. gondii is a major cause of subclinical human infection and an important opportunistic pathogen that causes severe disease in immunocompromised patients. While strains from all 3 lineages were isolated from humans, the majority of human toxoplasmosis cases were associated with strains of a type II genotype. The correlation of specific clonal lineages with human toxoplasmosis has important implications for development of vaccines, drug treatments, and diagnostic protocols.
          Article 0 comments Cited 196 times – based on 0 reviews     Review now
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            Identification of a 200- to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR.

            W Homan, M Vercammen, J De Braekeleer … (2000)
            We have identified a novel 529bp fragment that is repeated 200- to 300-fold in the genome of Toxoplasma gondii. This 529bp fragment was utilised for the development of a very sensitive and specific PCR for diagnostic purposes, and a quantitative competitive-PCR for the evaluation of cyst numbers in the brains of chronically infected mice. The 529bp fragment was found in all 60 strains of T. gondii tested, and it discriminates DNA of T. gondii from that of other parasites. Toxoplasma gondii DNA was detected in amniotic fluid of patients, as well as in various tissues from infected mice. Polymerase chain reaction with the 529bp fragment was more sensitive than with the 35-copy B1 gene. For the quantitative competitive-PCR, a 410-bp competitor molecule was co-amplified with similar efficiency as the 529bp fragment. Quantitative competitive-PCR produced a linear relationship between the relative amounts of PCR product and the number of tachyzoites in the range of 10(2)-10(4) tachyzoites and 100-3000 tissue cysts. A highly significant correlation between visual counting of brain cysts and quantitative competitive-PCR was obtained in mice chronically infected with Toxoplasma. Thus, quantitative competitive-PCR with the 529bp fragment can be used as an alternative for the tedious visual counting of brain cysts in experimental animals. With the quantitative competitive-PCR, furthermore, we could confirm the copy number of the 529bp fragment in tachyzoites and estimate the number of bradyzoites per cyst.
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              Population structure and mouse-virulence of Toxoplasma gondii in Brazil.

              H.F.J. Pena, S.M. Gennari, J.P. Dubey … (2008)
              Recent studies found that isolates of Toxoplasma gondii from Brazil were biologically and genetically different from those in North America and Europe. However, to date only a small number of isolates have been analysed from different animal hosts in Brazil. In the present study DNA samples of 46 T. gondii isolates from cats in 11 counties in São Paulo state, Brazil were genetically characterised using 10 PCR restriction fragment length polymorphism markers including SAG1, SAG2, SAG3, BTUB, GRA6, c22-8, c29-2, L358, PK1 and Apico. An additional marker, CS3, that locates on chromosome VIIa and has previously been shown to be linked to acute virulence of T. gondii was also used to determine its association to virulence in mice. Genotyping of these 46 isolates revealed a high genetic diversity with 20 genotypes but no clonal Type I, II or III lineage was found. Two of the 46 isolates showed mixed infections. Combining genotyping data in this study with recent reported results from chickens, dogs and cats in Brazil (total 125 isolates) identified 48 genotypes and 26 of these genotypes had single isolates. Four of the 48 genotypes with multiple isolates identified from different hosts and locations are considered the common clonal lineages in Brazil. These lineages are designated as Types BrI, BrII, BrIII and BrIV. These results indicate that the T. gondii population in Brazil is highly diverse with a few successful clonal lineages expanded into wide geographical areas. In contrast to North America and Europe, where the Type II clonal lineage is overwhelmingly predominant, no Type II strain was identified from the 125 Brazil isolates. Analysis of mortality rates in infected mice indicates that Type BrI is highly virulent, Type BrIII is non-virulent, whilst Type BrII and BrIV lineages are intermediately virulent. In addition, allele types at the CS3 locus are strongly linked to mouse-virulence of the parasite. Thus, T. gondii has an epidemic population structure in Brazil and the major lineages have different biological traits.
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                Author and article information

                Contributors
                Sylvie Bisser: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2013
                Publication date (Electronic): 7 January 2013
                Volume: 8
                Issue: 1
                Electronic Location Identifier: e53483
                Affiliations
                [1 ]Department of Parasitology, Provincial Laboratory of Microbiology & Parasitology and the Key Laboratory of Zoonoses Anhui, Anhui Medical University, Hefei, Anhui, China
                [2 ]Clinical Laboratory, the First Affiliated Hospital of Anhui Medical University, Hefei, Anhui, China
                [3 ]Clinical Laboratory, the First Affiliated Hospital of Anhui University of Traditional Chinese Medicine, Hefei, Anhui, China
                [4 ]Provincial Institute of Parasitic Diseases Control Anhui, Hefei, Anhui, China
                [5 ]State Key Laboratory of Biocontrol, School of Life Sciences, the Key laboratory of Tropical Diseases Control, the Ministry of Education, and the Department of Parasitology, Sun Yat-Sen University, Guangzhou, Guangdong, China
                [6 ]Department of Parasitology, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China
                [7 ]Department of Pathogen Biology, Nanjing Medical University, Nanjing, Jiangsu, China
                [8 ]Department of Parasitology, and the Key Laboratory of Tropical Disease Control, Ministry of Education, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, Guangdong, China
                INSERM U1094, University of Limoges School of Medicine, France
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: LW HC WL YW FL ZL XW JS. Performed the experiments: LW HC DL JG XH. Analyzed the data: LW HC XS XX KH QL. Wrote the paper: LW JS.

                Article
                Publisher ID: PONE-D-12-20504
                DOI: 10.1371/journal.pone.0053483
                PMC ID: 3538538
                PubMed ID: 23308233
                SO-VID: 80b0ad9b-ade6-4314-b822-803b6ed11733
                Copyright statement: Copyright @ 2013
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 5 July 2012
                Date accepted : 30 November 2012
                Page count
                Pages: 11
                Funding
                This work was supported by the National Basic Research Program of China (973 Program, No. 2010CB530001) ( http://www.973.gov.cn/Default_3.aspx). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Biology
                Subject: Genetics
                Subject: Heredity
                Subject: Genotypes
                Subject: Microbiology
                Subject: Protozoology
                Subject: Parastic Protozoans
                Subject: Toxoplasma Gondii
                Subject: Parasitology
                Subject: Zoology
                Subject: Parasitology
                Subject: Medicine
                Subject: Infectious Diseases
                Subject: Parasitic Diseases
                Subject: Veterinary Science
                Subject: Veterinary Diseases
                Subject: Veterinary Parasitology

                ScienceOpen disciplines: Uncategorized
                Data availability:
                ScienceOpen disciplines: Uncategorized

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