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      Are molecular tools clarifying or confusing our understanding of the public health threat from zoonotic enteric protozoa in wildlife?

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          Abstract

          Emerging infectious diseases are frequently zoonotic, often originating in wildlife, but enteric protozoa are considered relatively minor contributors. Opinions regarding whether pathogenic enteric protozoa may be transmitted between wildlife and humans have been shaped by our investigation tools, and have led to oscillations regarding whether particular species are zoonotic or have host-adapted life cycles.

          When the only approach for identifying enteric protozoa was morphology, it was assumed that many enteric protozoa colonized multiple hosts and were probably zoonotic. When molecular tools revealed genetic differences in morphologically identical species colonizing humans and other animals, host specificity seemed more likely. Parasites from animals found to be genetically identical - at the few genes investigated - to morphologically indistinguishable parasites from human hosts, were described as having zoonotic potential. More discriminatory molecular tools have now sub-divided some protozoa again. Meanwhile, some infection events indicate that, circumstances permitting, some “host-specific” protozoa, can actually infect various hosts. These repeated changes in our understanding are linked intrinsically to the investigative tools available.

          Here we review how molecular tools have assisted, or sometimes confused, our understanding of the public health threat from nine enteric protozoa and example wildlife hosts ( Balantoides coli - wild boar; Blastocystis sp. - wild rodents; Cryptosporidium spp. - wild fish; Encephalitozoon spp. - wild birds; Entamoeba spp. - non-human primates; Enterocytozoon bieneusi - wild cervids; Giardia duodenalis - red foxes; Sarcocystis nesbitti - snakes; Toxoplasma gondii - bobcats).

          Molecular tools have provided evidence that some enteric protozoa in wildlife may infect humans, but due to limited discriminatory power, often only the zoonotic potential of the parasite is indicated. Molecular analyses, which should be as discriminatory as possible, are one, but not the only, component of the toolbox for investigating potential public health impacts from pathogenic enteric protozoa in wildlife.

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          Highlights

          • Wildlife is a potential reservoir of disease agents that may infect humans.

          • The public health threat from enteric protozoa in wildlife is poorly understood.

          • Molecular tools may help in understanding this threat, but may also confuse.

          • We use nine enteric protozoa-wildlife host examples to review the current position.

          • Data accumulate, but more discriminatory tools and other approaches are important.

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          Most cited references159

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          Zoonotic potential and molecular epidemiology of Giardia species and giardiasis.

          Molecular diagnostic tools have been used recently in assessing the taxonomy, zoonotic potential, and transmission of Giardia species and giardiasis in humans and animals. The results of these studies have firmly established giardiasis as a zoonotic disease, although host adaptation at the genotype and subtype levels has reduced the likelihood of zoonotic transmission. These studies have also identified variations in the distribution of Giardia duodenalis genotypes among geographic areas and between domestic and wild ruminants and differences in clinical manifestations and outbreak potentials of assemblages A and B. Nevertheless, our efforts in characterizing the molecular epidemiology of giardiasis and the roles of various animals in the transmission of human giardiasis are compromised by the lack of case-control and longitudinal cohort studies and the sampling and testing of humans and animals living in the same community, the frequent occurrence of infections with mixed genotypes and subtypes, and the apparent heterozygosity at some genetic loci for some G. duodenalis genotypes. With the increased usage of multilocus genotyping tools, the development of next-generation subtyping tools, the integration of molecular analysis in epidemiological studies, and an improved understanding of the population genetics of G. duodenalis in humans and animals, we should soon have a better appreciation of the molecular epidemiology of giardiasis, the disease burden of zoonotic transmission, the taxonomy status and virulences of various G. duodenalis genotypes, and the ecology of environmental contamination.
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            Use of ITS2 Region as the Universal DNA Barcode for Plants and Animals

            Background The internal transcribed spacer 2 (ITS2) region of nuclear ribosomal DNA is regarded as one of the candidate DNA barcodes because it possesses a number of valuable characteristics, such as the availability of conserved regions for designing universal primers, the ease of its amplification, and sufficient variability to distinguish even closely related species. However, a general analysis of its ability to discriminate species in a comprehensive sample set is lacking. Methodology/Principal Findings In the current study, 50,790 plant and 12,221 animal ITS2 sequences downloaded from GenBank were evaluated according to sequence length, GC content, intra- and inter-specific divergence, and efficiency of identification. The results show that the inter-specific divergence of congeneric species in plants and animals was greater than its corresponding intra-specific variations. The success rates for using the ITS2 region to identify dicotyledons, monocotyledons, gymnosperms, ferns, mosses, and animals were 76.1%, 74.2%, 67.1%, 88.1%, 77.4%, and 91.7% at the species level, respectively. The ITS2 region unveiled a different ability to identify closely related species within different families and genera. The secondary structure of the ITS2 region could provide useful information for species identification and could be considered as a molecular morphological characteristic. Conclusions/Significance As one of the most popular phylogenetic markers for eukaryota, we propose that the ITS2 locus should be used as a universal DNA barcode for identifying plant species and as a complementary locus for CO1 to identify animal species. We have also developed a web application to facilitate ITS2-based cross-kingdom species identification (http://its2-plantidit.dnsalias.org).
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              Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease.

              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.
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                Author and article information

                Contributors
                Journal
                Int J Parasitol Parasites Wildl
                Int J Parasitol Parasites Wildl
                International Journal for Parasitology: Parasites and Wildlife
                Elsevier
                2213-2244
                13 February 2019
                August 2019
                13 February 2019
                : 9
                : 323-341
                Affiliations
                [a ]Parasitology Laboratory, Department of Food Safety and Infection Biology, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, PO Box 369 Sentrum, 0102, Oslo, Norway
                [b ]Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London, WC1E 7HT, United Kingdom
                [c ]Department of Companion Animal Clinical Sciences, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, PO Box 369 Sentrum, 0102, Oslo, Norway
                [d ]United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory, Building 1001, Beltsville, MD, 20705-2350, USA
                [e ]Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05, České Budějovice, Czech Republic
                [f ]Faculty of Agriculture, University of South Bohemia in České Budějovice, Studentská 1668, 370 05, Czech Republic
                [g ]College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou, 450046, China
                [h ]Department of Microbiology and Parasitology, Faculty of Pharmacy, Complutense University, Plaza Ramón y Cajal s/n, 28040, Madrid, Spain
                [i ]Centre for Sustainable Aquatic Ecosystems, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, WA, 6150, Australia
                [j ]Institute of Epidemiology, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, 17493, Greifswald, Insel Riems, Germany
                [k ]Department of Microbiology, University of Tennessee, Knoxville, TN, 37996-1937, USA
                [l ]Laboratory of Molecular & Evolutionary Parasitology, RAPID Group, School of Biosciences, University of Kent, Canterbury, UK
                Author notes
                []Corresponding author. lucy.robertson@ 123456nmbu.no
                [1]

                Currently at: Scientific Research Experiment Center & Laboratory Animal Center, Henan University of Chinese Medicine, Zhengzhou, 450046, China.

                Article
                S2213-2244(18)30184-6
                10.1016/j.ijppaw.2019.01.010
                6626983
                31338293
                9a4d661b-4650-4e74-8b9d-02136481da8d
                © 2019 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 21 December 2018
                : 30 January 2019
                : 31 January 2019
                Categories
                Special section: Emerging Zoonoses and Wildlife

                emerging infection,host specificity,protozoa,transmission,wildlife,zoonosis

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