Mitochondrial genome sequencing reveals potential origins of the scabies mite  Sarcoptes scabiei  infesting two iconic Australian marsupials

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Abstract

Background

Debilitating skin infestations caused by the mite, Sarcoptes scabiei, have a profound impact on human and animal health globally. In Australia, this impact is evident across different segments of Australian society, with a growing recognition that it can contribute to rapid declines of native Australian marsupials. Cross-host transmission has been suggested to play a significant role in the epidemiology and origin of mite infestations in different species but a chronic lack of genetic resources has made further inferences difficult. To investigate the origins and molecular epidemiology of S. scabiei in Australian wildlife, we sequenced the mitochondrial genomes of S. scabiei from diseased wombats ( Vombatus ursinus) and koalas ( Phascolarctos cinereus) spanning New South Wales, Victoria and Tasmania, and compared them with the recently sequenced mitochondrial genome sequences of S. scabiei from humans.

Results

We found unique S. scabiei haplotypes among individual wombat and koala hosts with high sequence similarity (99.1% - 100%). Phylogenetic analysis of near full-length mitochondrial genomes revealed three clades of S. scabiei (one human and two marsupial), with no apparent geographic or host species pattern, suggestive of multiple introductions. The availability of additional mitochondrial gene sequences also enabled a re-evaluation of a range of putative molecular markers of S. scabiei, revealing that cox1 is the most informative gene for molecular epidemiological investigations. Utilising this gene target, we provide additional evidence to support cross-host transmission between different animal hosts.

Conclusions

Our results suggest a history of parasite invasion through colonisation of Australia from hosts across the globe and the potential for cross-host transmission being a common feature of the epidemiology of this neglected pathogen. If this is the case, comparable patterns may exist elsewhere in the ‘New World’. This work provides a basis for expanded molecular studies into mange epidemiology in humans and animals in Australia and other geographic regions.

Electronic supplementary material

The online version of this article (10.1186/s12862-017-1086-9) contains supplementary material, which is available to authorized users.

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Most cited references 34

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Emerging infectious diseases of wildlife: a critical perspective.

Daniel Tompkins, Scott Carver, Menna Jones … (2015)

We review the literature to distinguish reports of vertebrate wildlife disease emergence with sufficient evidence, enabling a robust assessment of emergence drivers. For potentially emerging agents that cannot be confirmed, sufficient data on prior absence (or a prior difference in disease dynamics) are frequently lacking. Improved surveillance, particularly for neglected host taxa, geographical regions and infectious agents, would enable more effective management should emergence occur. Exposure to domestic sources of infection and human-assisted exposure to wild sources were identified as the two main drivers of emergence across host taxa; the domestic source was primary for fish while the wild source was primary for other taxa. There was generally insufficient evidence for major roles of other hypothesized drivers of emergence.

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Skin infections and infestations in Aboriginal communities in northern Australia.

Jonathan Carapetis, Lauren Currie (2000)

The most important skin infections in Aboriginal communities in central and northern Australia are scabies and streptococcal pyoderma. Scabies is endemic in many remote Aboriginal communities, with prevalences in children up to 50%. The cycles of scabies transmission underlie much of the pyoderma. Up to 70% of children have skin sores, with group A streptococcus (GAS) the major pathogen. Group A streptococcus is responsible for the continuing outbreaks of post-streptococcal glomerulonephritis and acute rheumatic fever (ARF). The cycles of scabies transmission in dogs and humans do not appear to significantly overlap. Guidelines have been developed for community control of scabies and skin sores and successful community initiated coordinated programmes have occurred. The anthropophilic dermatophyte Trichophyton rubrum is ubiquitous in many communities, again reflecting living conditions. Other skin infections related to the tropical environment include melioidosis, nocardiosis, Chromobacterium violaceum and chromoblastomycosis. Sustainable and long-term improvements in scabies, skin sores and GAS-related disease and tinea require fundamental changes that address social and economic inequities and, in particular, living conditions and overcrowding.

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Genetic epidemiology of Sarcoptes scabiei (Acari: Sarcoptidae) in northern Australia.

S.F. Walton, A. Dougall, S Pizzutto … (2004)

Utilising three hypervariable microsatellite markers we have previously shown that scabies mites on people are genetically distinct from those on dogs in sympatric populations in northern Australia. This had important ramifications on the formulation of public health control policies. In contrast phylogenetic analyses using mitochondrial markers on scabies mites infecting multiple animal hosts elsewhere in the world could not differentiate any genetic variation between mite haplotype and host species. Here we further analyse the intra-specific relationship of Sarcoptes scabiei var. hominis with S. scabiei var. canis by using both mitochondrial DNA and an expanded nuclear microsatellite marker system. Phylogenetic studies using sequences from the mitochondrial genes coding for 16S rRNA and Cytochrome Oxidase subunit I demonstrated significant relationships between S. scabiei MtDNA haplotypes, host species and geographical location. Multi-locus genotyping using 15 microsatellite markers substantiated previous data that gene flow between scabies mite populations on human and dog hosts is extremely rare in northern Australia. These data clearly support our previous contention that control programs for human scabies in endemic areas with sympatric S. scabiei var. hominis and var. canis populations must focus on human-to-human transmission. The genetic division of dog and human derived scabies mites also has important implications in vaccine and diagnostic test development as well as the emergence and monitoring of drug resistance in S. scabiei in northern Australia.

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Author and article information

Contributors

Tamieka A. Fraser: Tamieka.Fraser@researh.usc.edu.au

Renfu Shao: rshao@usc.edu.au

Nicholas M. Fountain-Jones: nfountainjones@gmail.com

Michael Charleston: michael.charleston@utas.edu.au

Alynn Martin: alynn.martin@utas.edu.au

Pam Whiteley: pamw@unimelb.edu.au

Roz Holme: wombat.hospital@gmail.com

Scott Carver: scott.carver@utas.edu.au

Adam Polkinghorne:

ORCID: http://orcid.org/0000-0002-6803-9222

apolking@usc.edu.au

Journal

Journal ID (nlm-ta): BMC Evol Biol

Journal ID (iso-abbrev): BMC Evol. Biol

Title: BMC Evolutionary Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2148

Publication date (Electronic): 28 November 2017

Publication date PMC-release: 28 November 2017

Publication date Collection: 2017

Volume: 17

Electronic Location Identifier: 233

Affiliations

[1 ]ISNI 0000 0004 1936 826X, GRID grid.1009.8, School of Biological Sciences, University of Tasmania, ; Sandy Bay, Hobart, TAS Australia

[2 ]ISNI 0000 0001 1555 3415, GRID grid.1034.6, Centre for Animal Health Innovation, School of Science and Engineering, University of the Sunshine Coast, ; Sippy Downs, QLD Australia

[3 ]ISNI 0000000419368657, GRID grid.17635.36, University of Minnesota, ; Minneapolis, MN USA

[4 ]ISNI 0000 0004 1936 834X, GRID grid.1013.3, School of Information Technologies, University of Sydney, ; Camperdown, NSW Australia

[5 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, ; Werribee, VIC Australia

[6 ]Cedar Creek Wombat Rescue Inc. & Hospital, Cedar Creek, NSW Australia

Author information

Adam Polkinghorne http://orcid.org/0000-0002-6803-9222

Article

Publisher ID: 1086

DOI: 10.1186/s12862-017-1086-9

PMC ID: 5706379

PubMed ID: 29183283

SO-VID: 5e8f4924-88ff-4d27-860a-3690f7325d72

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 23 June 2017

Date accepted : 21 November 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100008190, Holsworth Wildlife Research Endowment;

Custom metadata

ScienceOpen disciplines: Evolutionary Biology

Keywords: sarcoptes scabiei,wombat,koala,mitochondrial genome sequencing,cox1,phylogeny,conservation

Data availability:

ScienceOpen disciplines: Evolutionary Biology

Keywords: sarcoptes scabiei, wombat, koala, mitochondrial genome sequencing, cox1, phylogeny, conservation

Mitochondrial genome sequencing reveals potential origins of the scabies mite Sarcoptes scabiei infesting two iconic Australian marsupials

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Coleoptera

Most cited references 34

Emerging infectious diseases of wildlife: a critical perspective.

Skin infections and infestations in Aboriginal communities in northern Australia.

Genetic epidemiology of Sarcoptes scabiei (Acari: Sarcoptidae) in northern Australia.

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