Genome-Wide Analyses of Individual Strongyloides stercoralis (Nematoda: Rhabditoidea) Provide Insights into Population Structure and Reproductive Life Cycles

Kikuchi, Taisei; Hino, Akinori; Tanaka, Teruhisa; Aung, Myo Pa Pa Thet Hnin Htwe; Afrin, Tanzila; Nagayasu, Eiji; Tanaka, Ryusei; Higashiarakawa, Miwa; Win, Kyu Kyu; Hirata, Tetsuya; Htike, Wah Win; Fujita, Jiro; Maruyama, Haruhiko

doi:10.1371/journal.pntd.0005253

Cited by 32 publications

(52 citation statements)

References 33 publications

(48 reference statements)

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“…An approach similar to a previous S . stercoralis population study [ 46 ] was used to analyze the whole genome data. In brief, raw reads were trimmed with skewer [ 50 ] (version 0.1.123; -q 30 -Q30 -l 60).…”

Section: Methodsmentioning

confidence: 99%

“…Recent comparative analyses of the mitochondrial locus cytochrome c oxidase subunit 1 ( cox 1) [ 6 , 36 , 38 , 45 ] and the whole genome sequence of 33 individual S . stercoralis from Japan and Myanmar [ 46 ] indicated that there is substantial genetic diversity among S . stercoralis isolated from human hosts and [ 38 ] suggested that there might exist human- and dog-specialized subpopulations.…”

Section: Introductionmentioning

confidence: 99%

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Different but overlapping populations of Strongyloides stercoralis in dogs and humans—Dogs as a possible source for zoonotic strongyloidiasis

et al. 2017

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Strongyloidiasis is a much-neglected soil born helminthiasis caused by the nematode Strongyloides stercoralis. Human derived S. stercoralis can be maintained in dogs in the laboratory and this parasite has been reported to also occur in dogs in the wild. Some authors have considered strongyloidiasis a zoonotic disease while others have argued that the two hosts carry host specialized populations of S. stercoralis and that dogs play a minor role, if any, as a reservoir for zoonotic S. stercoralis infections of humans. We isolated S. stercoralis from humans and their dogs in rural villages in northern Cambodia, a region with a high incidence of strongyloidiasis, and compared the worms derived from these two host species using nuclear and mitochondrial DNA sequence polymorphisms. We found that in dogs there exist two populations of S. stercoralis, which are clearly separated from each other genetically based on the nuclear 18S rDNA, the mitochondrial cox1 locus and whole genome sequence. One population, to which the majority of the worms belong, appears to be restricted to dogs. The other population is indistinguishable from the population of S. stercoralis isolated from humans. Consistent with earlier studies, we found multiple sequence variants of the hypervariable region I of the 18 S rDNA in S. stercoralis from humans. However, comparison of mitochondrial sequences and whole genome analysis suggest that these different 18S variants do not represent multiple genetically isolated subpopulations among the worms isolated from humans. We also investigated the mode of reproduction of the free-living generations of laboratory and wild isolates of S. stercoralis. Contrary to earlier literature on S. stercoralis but similar to other species of Strongyloides, we found clear evidence of sexual reproduction. Overall, our results show that dogs carry two populations, possibly different species of Strongyloides. One population appears to be dog specific but the other one is shared with humans. This argues for the strong potential of dogs as reservoirs for zoonotic transmission of S. stercoralis to humans and suggests that in order to reduce the exposure of humans to infective S. stercoralis larvae, dogs should be treated for the infection along with their owners.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Different but overlapping populations of Strongyloides stercoralis in dogs and humans—Dogs as a possible source for zoonotic strongyloidiasis

et al. 2017

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“…Furthermore, Strongyloides genotyping surveys Barratt et al (2019b) and Jaleta et al (2017). This scheme was expanded here to include haplotype XV of 18S HVR-I (GenBank Accession: MT436714), identified in genomes sequenced from Japanese humans by Kikuchi et al (2016). For the purposes of this study, note that the haplotypes originally defined after the description of Barratt and colleagues were split into smaller segments as shown here.…”

Section: Rationale For Study Designmentioning

confidence: 99%

Machine learning-based analyses support the existence of species complexes for Strongyloides fuelleborni and Strongyloides stercoralis

Barratt

Sapp

2020

Parasitology

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Human strongyloidiasis is a serious disease mostly attributable to Strongyloides stercoralis and to a lesser extent Strongyloides fuelleborni, a parasite mainly of non-human primates. The role of animals as reservoirs of human-infecting Strongyloides is ill-defined, and whether dogs are a source of human infection is debated. Published multi-locus sequence typing (MLST) studies attempt to elucidate relationships between Strongyloides genotypes, hosts, and distributions, but typically examine relatively few worms, making it difficult to identify population-level trends. Combining MLST data from multiple studies is often impractical because they examine different combinations of loci, eliminating phylogeny as a means of examining these data collectively unless hundreds of specimens are excluded. A recently-described machine learning approach that facilitates clustering of MLST data may offer a solution, even for datasets that include specimens sequenced at different combinations of loci. By clustering various MLST datasets as one using this procedure, we sought to uncover associations among genotype, geography, and hosts that remained elusive when examining datasets individually. Multiple datasets comprising hundreds of S. stercoralis and S. fuelleborni individuals were combined and clustered. Our results suggest that the commonly proposed ‘two lineage’ population structure of S. stercoralis (where lineage A infects humans and dogs, lineage B only dogs) is an over-simplification. Instead, S. stercoralis seemingly represents a species complex, including two distinct populations over-represented in dogs, and other populations vastly more common in humans. A distinction between African and Asian S. fuelleborni is also supported here, emphasizing the need for further resolving these taxonomic relationships through modern investigations.

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“…Genetic analysis has shown that there are genotypic variations in S. stercoralis populations and global diversity. There are two lineages of S. stercoralis , termed type A and type B 3 . Type A causes infections in humans and dogs, while type B infects only dogs 4 .…”

Section: Introductionmentioning

confidence: 99%

Prevalence of Strongyloides stercoralis infection and hyperinfection syndrome among renal allograft recipients in Central Europe

Winnicki

Eder

Mazal

et al. 2018

Sci Rep

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Strongyloides stercoralis is not hyperendemic in European countries but has been increasing in prevalence due to migration and travel. The infection is characterized by a mostly asymptomatic course or nonspecific symptoms in healthy subjects. However, immunosuppression or chemotherapy have been described as leading triggers for Strongyloides stercoralis hyperinfection syndrome and may have a fatal course. A post hoc analysis was performed among renal transplant patients during a 5-year period. Plasma samples of two hundred kidney allograft recipients were retrospectively analyzed for Strongyloides stercoralis seropositivity by established ELISA testing. Positive Strongyloides stercoralis serology was found in 3% of allograft recipients. One patient developed a life-threatening hyperinfection syndrome. His Strongyloides IgG signal had been elevated for years before the outbreak of the disease. Stronglyoides infections in transplant recipients are an important issue that physicians also in Central Europe should be aware of, given the risk of hyperinfection syndrome and the challenges in clinical diagnosis. Our study suggests that recipient and donor screening should be recommended in kidney transplantation programs in Central Europe as Strongyloides infection rates increase and its prevalence may be underestimated. Further research is needed to understand why some Strongyloides stercoralis seropositive individuals develop hyperinfection syndrome and others do not.

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Genome-Wide Analyses of Individual Strongyloides stercoralis (Nematoda: Rhabditoidea) Provide Insights into Population Structure and Reproductive Life Cycles

Cited by 32 publications

References 33 publications

Different but overlapping populations of Strongyloides stercoralis in dogs and humans—Dogs as a possible source for zoonotic strongyloidiasis

Different but overlapping populations of Strongyloides stercoralis in dogs and humans—Dogs as a possible source for zoonotic strongyloidiasis

Machine learning-based analyses support the existence of species complexes for Strongyloides fuelleborni and Strongyloides stercoralis

Prevalence of Strongyloides stercoralis infection and hyperinfection syndrome among renal allograft recipients in Central Europe

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