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Detection of Classic and Cryptic Strongyloides Genotypes bioRxiv preprint doi: https://doi.org/10.1101/549535; this version posted February 13, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 1 Detection of classic and cryptic Strongyloides genotypes by deep amplicon 2 sequencing: A preliminary survey of dog and human specimens collected 3 from remote Australian communities 4 5 Meruyert Beknazarova1*, Joel L. N. Barratt2,3*, Richard S. Bradbury2, Meredith Lane2,4, Harriet 6 Whiley1, Kirstin Ross1 7 8 * corresponding authors 9 1 Environmental Health, Flinders University, South Australia 10 2 Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention 11 3 Oak Ridge Associated Universities, Oak Ridge, Tennessee 12 4 Synergy America Inc. 13 14 15 1 bioRxiv preprint doi: https://doi.org/10.1101/549535; this version posted February 13, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 16 Abstract 17 Strongyloidiasis is a neglected disease caused by the human infective nematodes 18 Strongyloides stercoralis, Strongyloides fuelleborni subsp. fuelleborni and Strongyloides 19 fuelleborni subsp. kellyi. The zoonotic potential of S. stercoralis and the potential role of dogs 20 in the maintenance of strongyloidiasis transmission has been a topic of interest and discussion 21 for many years. In Australia, strongyloidiasis is prevalent in remote socioeconomically 22 disadvantaged communities in the north of the continent. Being an isolated continent that has 23 been separated from other regions for a long geological period, knowledge on the diversity of 24 Australian Strongyloides genotypes is an important addition to our understanding of the genetic 25 diversity within the genus. Using PCR enrichment combined with Illumina sequencing 26 technology, we sequenced the Strongyloides SSU 18S rDNA hyper-variable I and hyper- 27 variable IV regions using Strongyloides-specific primers, and a fragment of the mtDNA cox1 28 gene using primers that are broadly specific for Strongyloides sp. and hookworms. These loci 29 were amplified from DNA extracted from human and dog faeces, and one human sputum 30 sample. Using this approach, we confirm for the first time that potentially zoonotic S. 31 stercoralis genotypes are present in Australia, suggesting that dogs represent a potential 32 reservoir of human strongyloidiasis in remote Australian communities. 33 Author summary 34 Strongyloides stercoralis is a soil-transmitted nematode that causes the disease 35 strongyloidiasis. Due to the autoinfective nature of this parasite, it can re-infect a host causing 36 chronic infection. If not diagnosed and treated it can be highly detrimental to human health and 37 has a high mortality rate. Strongyloidiasis is common in remote communities in the north of 38 Australia and has been an issue for decades. Despite various successful intervention programs 39 to treat human strongyloidiasis, the disease remains endemic in those communities. Here for the 2 bioRxiv preprint doi: https://doi.org/10.1101/549535; this version posted February 13, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 40 first time we looked at the Australian dogs’ potential to infect humans and found that they carry 41 two genetically distinct strains of Strongyloides spp., one of which also infects humans. This 42 supports the hypothesis that dogs are a potential source for human strongyloidiasis. We also 43 found that dogs in Australia might be carrying unique haplotypes. Whether these new 44 haplotypes are also human infective is to be confirmed by further research. 45 46 47 48 49 Keywords: Strongyloides, genotypes, dogs, Australia, zoonoses, hookworms, Ancylostoma 3 bioRxiv preprint doi: https://doi.org/10.1101/549535; this version posted February 13, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 50 Introduction 51 Strongyloidiasis is a neglected disease caused by the human infective nematodes 52 Strongyloides stercoralis, Strongyloides fuelleborni subsp. fuelleborni and Strongyloides 53 fuelleborni subsp. kellyi (Grove, 1996). Worldwide, it is estimated to infect up to 370 million 54 people and is predominately found in socioeconomically disadvantaged communities (Olsen et 55 al., 2009, Bisoffi et al., 2013, Beknazarova et al., 2016). While S. stercoralis is a globally 56 distributed nematode, S. f. fuelleborni has thus far only reported in Africa and Southeast Asia 57 and S. f. kellyi from Papua New Guinea (PNG) (Thanchomnang et al., 2017, Pampiglione and 58 Ricciardi, 1971, Ashford et al., 1992). 59 In Australia, strongyloidiasis is prevalent in remote communities located across the 60 Northern Territory, Queensland, Western Australia, northern South Australia and northern New 61 South Wales (Page et al., 2016). Current estimates indicate that infection rates in some 62 communities are up to 41% or 60% based on microscopy or serology respectively (Heydon and 63 Green, 1931, Sampson et al., 25-26 June 2003, Miller et al., 2018, Holt et al., 2017). Despite 64 initially successful intervention programs targeting treatment to eliminate human 65 strongyloidiasis in remote Australian communities, the disease remains endemic (Kearns et al., 66 2017, Page et al., 2006). Reappearance of the infection could possibly be as a result of zoonotic 67 transmission from dog reservoirs given that dogs and humans share a close and intimate cultural 68 bond in rural and remote Indigenous communities of Australia (Constable et al., 2010). 69 The zoonotic potential of S. stercoralis infected dogs and their potential role in the 70 maintenance of strongyloidiasis transmission has been a topic of interest and discussion for 71 many years (Beknazarova et al., 2017b, Goncalves et al., 2007, Takano et al., 2009). Molecular 72 data from human and dog derived S. stercoralis are useful in understanding the nature of cross 73 infection. There are two regions of the S. stercoralis nuclear and mitochondrial genome that are 4 bioRxiv preprint doi: https://doi.org/10.1101/549535; this version posted February 13, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 74 considered to be conserved within the Strongyloides genus and can be used as markers for 75 molecular typing of S. stercoralis. Hyper-variable regions (HVR) I and IV of the small Subunit 76 (SSU) 18s ribosomal DNA and the cytochrome c-oxidase subunit 1 (cox1) gene of the 77 mitochondrial DNA (mtDNA) have been widely used to study relationships between S. 78 stercoralis from different hosts and different geographic locations (Hasegawa et al., 2009, 79 Hasegawa et al., 2010, Jaleta et al., 2017, Nagayasu et al., 2017, Basso et al., 2018). Based on 80 genetic analysis of these genetic loci, it has been recently found that there are two genetically 81 different S. stercoralis strains, one is dog and human infective, and the other is dog specific. 82 These data were collected from dogs and humans in Cambodia and Japan (Jaleta et al., 2017, 83 Nagayasu et al., 2017). 84 Being an isolated continent that has been separated from other regions for a long 85 geological period, Australia could represent an interesting addition to our understanding of the 86 genetic diversity within S. stercoralis and the Strongyloides genus more generally. Indigenous 87 Australians have inhabited the continent for at least 40,000 years and dogs (in the form of 88 dingoes) were likely introduced up to 12,000 years ago (Clutton-Brock, 1995). Given this long 89 period of relative isolation, it might be expected that Australia could harbor unique endemic 90 genotypes or unique sub-species of S. stercoralis that have evolved within dog and human 91 populations over this period. 92 Using PCR enrichment combined with Illumina sequencing technology, we sequenced 93 the Strongyloides SSU 18S rDNA hyper-variable I and hyper-variable IV regions using 94 Strongyloides-specific primers, and a fragment of the mtDNA cox1 gene using primers that are 95 broadly specific for Strongyloides sp. and hookworms. This approach was applied to DNA 96 extracted from human and dog faeces, and one human sputum sample. The main focus of this 97 study was to genotype Australian human and dog S. stercoralis strains to see whether dogs 5 bioRxiv preprint doi: https://doi.org/10.1101/549535; this version posted February 13, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 98 carry human S. stercoralis strains and/or vice versa. To our knowledge this is the first time 99 human and dog S. stercoralis have been studied in Australia on a molecular level. 100 Methods 101 Study area and faeces collection 102 Dog faecal samples were collected from communities in the Northern Territory, 103 Australia. Dog faeces were collected from the environment (i.e., the ground) in the selected 104 communities and stored in the DESS (dimethyl sulfoxide, disodium EDTA, and saturated 105 NaCL) solution to preserve the DNA (Beknazarova et al., 2017a).
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