Characterisation of the faecal virome of captive and wild Tasmanian devils using virus-like particles metagenomics and meta-transcriptomics

AbstractBackgroundThe Tasmanian devil is an endangered carnivorous marsupial threatened by devil facial tumour disease (DFTD). While research on DFTD has been extensive, little is known about the viruses present in devils, and whether any of these are of potential conservation relevance for this endangered species.MethodsUsing both metagenomics based on virus-like particle (VLP) enrichment and sequence-independent amplification (VLP metagenomics), and meta-transcriptomics based on bulk RNA sequencing, we characterised and compared the faecal viromes of captive and wild Tasmanian devils.ResultsA total of 54 devil faecal samples collected from captive (n = 2) and wild (n = 4) populations were processed for virome characterisation using both approaches. We detected many novel, highly divergent viruses, including vertebrate viruses, bacteriophage and other dietary associated plant and insect viruses. In total, 18 new vertebrate viruses, including novel sapelovirus, astroviruses, bocaviruses, papillomaviruses and gammaherpesvirus were identified, as well as known mammalian pathogens including rabbit haemorrhagic disease virus 2 (RHDV2). Captive devils showed significantly lower levels of viral diversity than wild devils. Comparison of the two methodological approaches revealed substantial differences in the number and types of viruses detected, with meta-transcriptomics mainly identifying RNA viruses, and VLP metagenomics largely identifying DNA viruses.ConclusionThis study has greatly expanded our knowledge of eukaryotic viruses in the Tasmanian devil and provides important baseline information that will contribute to the conservation and captive management of this endangered species. In addition, our results showed that a combination of VLP metagenomics and meta-transcriptomics may be a more comprehensive approach to virome characterisation than either method alone.

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Fecal Viral Diversity of Captive and Wild Tasmanian Devils Characterized Using Virion-Enriched Metagenomics and Metatranscriptomics

Journal of Virology ◽

10.1128/jvi.00205-19 ◽

2019 ◽

Vol 93 (11) ◽

Cited By ~ 17

Author(s):

Rowena Chong ◽

Mang Shi ◽

Catherine E. Grueber ◽

Edward C. Holmes ◽

Carolyn J. Hogg ◽

...

Keyword(s):

Endangered Species ◽

Population Decline ◽

Significant Risk ◽

Rabbit Hemorrhagic Disease Virus ◽

Viral Diversity ◽

Hemorrhagic Disease ◽

Tasmanian Devil ◽

Dna Viruses ◽

Viral Communities ◽

Devil Facial Tumor Disease

ABSTRACT The Tasmanian devil is an endangered carnivorous marsupial threatened by devil facial tumor disease (DFTD). While research on DFTD has been extensive, little is known about viruses in devils and whether any are of potential conservation relevance for this endangered species. Using both metagenomics based on virion enrichment and sequence-independent amplification (virion-enriched metagenomics) and metatranscriptomics based on bulk RNA sequencing, we characterized and compared the fecal viromes of captive and wild devils. A total of 54 fecal samples collected from two captive and four wild populations were processed for virome characterization using both approaches. In total, 24 novel marsupial-related viruses, comprising a sapelovirus, astroviruses, rotaviruses, picobirnaviruses, parvoviruses, papillomaviruses, polyomaviruses, and a gammaherpesvirus, were identified, as well as known mammalian pathogens such as rabbit hemorrhagic disease virus 2. Captive devils showed significantly lower viral diversity than wild devils. Comparison of the two virus discovery approaches revealed substantial differences in the number and types of viruses detected, with metatranscriptomics better suited for RNA viruses and virion-enriched metagenomics largely identifying more DNA viruses. Thus, the viral communities revealed by virion-enriched metagenomics and metatranscriptomics were not interchangeable and neither approach was able to detect all viruses present. An integrated approach using both virion-enriched metagenomics and metatranscriptomics constitutes a powerful tool for obtaining a complete overview of both the taxonomic and functional profiles of viral communities within a sample. IMPORTANCE The Tasmanian devil is an iconic Australian marsupial that has suffered an 80% population decline due to a contagious cancer, devil facial tumor disease, along with other threats. Until now, viral discovery in this species has been confined to one gammaherpesvirus (dasyurid herpesvirus 2 [DaHV-2]), for which captivity was identified as a significant risk factor. Our discovery of 24 novel marsupial-associated RNA and DNA viruses, and that viral diversity is lower in captive than in wild devils, has greatly expanded our knowledge of gut-associated viruses in devils and provides important baseline information that will contribute to the conservation and captive management of this endangered species. Our results also revealed that a combination of virion-enriched metagenomics and metatranscriptomics may be a more comprehensive approach for virome characterization than either method alone. Our results thus provide a springboard for continuous improvements in the way we study complex viral communities.

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Blood Parasites in Endangered Wildlife-Trypanosomes Discovered during a Survey of Haemoprotozoa from the Tasmanian Devil

Pathogens ◽

10.3390/pathogens9110873 ◽

2020 ◽

Vol 9 (11) ◽

pp. 873

Author(s):

Siobhon L. Egan ◽

Manuel Ruiz-Aravena ◽

Jill M. Austen ◽

Xavier Barton ◽

Sebastien Comte ◽

...

Keyword(s):

Emerging Infectious Diseases ◽

Protozoan Parasite ◽

Blood Parasites ◽

Rapid Decline ◽

Tasmanian Devil ◽

Devil Facial Tumour Disease ◽

Transmissible Cancer ◽

Carnivorous Marsupial ◽

The Impact ◽

Single Blood Sample

The impact of emerging infectious diseases is increasingly recognised as a major threat to wildlife. Wild populations of the endangered Tasmanian devil, Sarcophilus harrisii, are experiencing devastating losses from a novel transmissible cancer, devil facial tumour disease (DFTD); however, despite the rapid decline of this species, there is currently no information on the presence of haemoprotozoan parasites. In the present study, 95 Tasmanian devil blood samples were collected from four populations in Tasmania, Australia, which underwent molecular screening to detect four major groups of haemoprotozoa: (i) trypanosomes, (ii) piroplasms, (iii) Hepatozoon, and (iv) haemosporidia. Sequence results revealed Trypanosoma infections in 32/95 individuals. Trypanosoma copemani was identified in 10 Tasmanian devils from three sites and a second Trypanosoma sp. was identified in 22 individuals that were grouped within the poorly described T. cyclops clade. A single blood sample was positive for Babesia sp., which most closely matched Babesia lohae. No other blood protozoan parasite DNA was detected. This study provides the first insight into haemoprotozoa from the Tasmanian devil and the first identification of Trypanosoma and Babesia in this carnivorous marsupial.

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Devil women

Pacific Conservation Biology ◽

10.1071/pc18021 ◽

2018 ◽

Vol 24 (3) ◽

pp. 271

Author(s):

Samantha Fox ◽

Carolyn J. Hogg ◽

Catherine E. Grueber ◽

Katherine Belov

Keyword(s):

At Risk ◽

Government Agencies ◽

Full Potential ◽

Tasmanian Devil ◽

Common Goal ◽

Personal Stories ◽

Devil Facial Tumour Disease ◽

Risk Of Extinction ◽

Carnivorous Marsupial ◽

The Devil

The Tasmanian devil, an iconic carnivorous marsupial, is at risk of extinction due to a contagious cancer called devil facial tumour disease. Saving any species from extinction requires strong partnerships between government agencies, zoo bodies and academia. The Devil Tools & Tech project brought these groups together under a single banner to achieve a common goal. The project has strong leadership from women. Here we tell our personal stories as to how we came to be involved in saving the devil and emphasise the importance of strong networks for women to reach their full potential.

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Immunity in rabbits experimentally infected with rabbit haemorrhagic disease (RHD) virus

Immunology Letters ◽

10.1016/s0165-2478(97)87357-9 ◽

1997 ◽

Vol 56 (1-3) ◽

pp. 130

Author(s):

W DeptuÅ‚a

Keyword(s):

Rabbit Haemorrhagic Disease ◽

Haemorrhagic Disease

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Microbial metagenomic approach uncovers the first rabbit haemorrhagic disease virus genome in Sub-Saharan Africa

Scientific Reports ◽

10.1038/s41598-021-91961-2 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Anise N. Happi ◽

Olusola A. Ogunsanya ◽

Judith U. Oguzie ◽

Paul E. Oluniyi ◽

Alhaji S. Olono ◽

...

Keyword(s):

Virus Genome ◽

Sub Saharan Africa ◽

High Morbidity ◽

Vp60 Gene ◽

Band Size ◽

Rabbit Haemorrhagic Disease ◽

Sub Saharan ◽

Domestic Rabbits ◽

Haemorrhagic Disease ◽

Pcr Targeting

AbstractRabbit Haemorrhagic Disease (RHD) causes high morbidity and mortality in rabbits and hares. Here, we report the first genomic characterization of lagovirus GI.2 virus in domestic rabbits from sub-Saharan Africa. We used an unbiased microbial metagenomic Next Generation Sequencing (mNGS) approach to diagnose the pathogen causing the suspected outbreak of RHD in Ibadan, Nigeria. The liver, spleen, and lung samples of five rabbits from an outbreak in 2 farms were analyzed. The mNGS revealed one full and two partial RHDV2 genomes on both farms. Phylogenetic analysis showed close clustering with RHDV2 lineages from Europe (98.6% similarity with RHDV2 in the Netherlands, and 99.1 to 100% identity with RHDV2 in Germany), suggesting potential importation. Subsequently, all the samples were confirmed by RHDV virus-specific RT-PCR targeting the VP60 gene with the expected band size of 398 bp for the five rabbits sampled. Our findings highlight the need for increased genomic surveillance of RHDV2 to track its origin, understand its diversity and to inform public health policy in Nigeria, and Sub-Saharan Africa.

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Low major histocompatibility complex diversity in the Tasmanian devil predates European settlement and may explain susceptibility to disease epidemics

Biology Letters ◽

10.1098/rsbl.2012.0900 ◽

2013 ◽

Vol 9 (1) ◽

pp. 20120900 ◽

Cited By ~ 36

Author(s):

Katrina Morris ◽

Jeremy J. Austin ◽

Katherine Belov

Keyword(s):

Major Histocompatibility Complex ◽

Tasmanian Devil ◽

Major Histocompatibility ◽

European Settlement ◽

Low Genetic Diversity ◽

Histocompatibility Complex ◽

Devil Facial Tumour Disease ◽

History Of ◽

Mhc Diversity ◽

Disease Epidemics

The Tasmanian devil ( Sarcophilus harrisii ) is at risk of extinction owing to the emergence of a contagious cancer known as devil facial tumour disease (DFTD). The emergence and spread of DFTD has been linked to low genetic diversity in the major histocompatibility complex (MHC). We examined MHC diversity in historical and ancient devils to determine whether loss of diversity is recent or predates European settlement in Australia. Our results reveal no additional diversity in historical Tasmanian samples. Mainland devils had common modern variants plus six new variants that are highly similar to existing alleles. We conclude that low MHC diversity has been a feature of devil populations since at least the Mid-Holocene and could explain their tumultuous history of population crashes.

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Timing and severity of immunizing diseases in rabbits is controlled by seasonal matching of host and pathogen dynamics

Journal of The Royal Society Interface ◽

10.1098/rsif.2014.1184 ◽

2015 ◽

Vol 12 (103) ◽

pp. 20141184 ◽

Cited By ~ 20

Author(s):

Konstans Wells ◽

Barry W. Brook ◽

Robert C. Lacy ◽

Greg J. Mutze ◽

David E. Peacock ◽

...

Keyword(s):

Local Population ◽

Disease Outbreaks ◽

Maternal Antibodies ◽

Timing Of Reproduction ◽

Demographic Rates ◽

Pathogen Dynamics ◽

Rabbit Haemorrhagic Disease ◽

Seasonal Epidemics ◽

Haemorrhagic Disease

Infectious diseases can exert a strong influence on the dynamics of host populations, but it remains unclear why such disease-mediated control only occurs under particular environmental conditions. We used 16 years of detailed field data on invasive European rabbits ( Oryctolagus cuniculus ) in Australia, linked to individual-based stochastic models and Bayesian approximations, to test whether (i) mortality associated with rabbit haemorrhagic disease (RHD) is driven primarily by seasonal matches/mismatches between demographic rates and epidemiological dynamics and (ii) delayed infection (arising from insusceptibility and maternal antibodies in juveniles) are important factors in determining disease severity and local population persistence of rabbits. We found that both the timing of reproduction and exposure to viruses drove recurrent seasonal epidemics of RHD. Protection conferred by insusceptibility and maternal antibodies controlled seasonal disease outbreaks by delaying infection; this could have also allowed escape from disease. The persistence of local populations was a stochastic outcome of recovery rates from both RHD and myxomatosis. If susceptibility to RHD is delayed, myxomatosis will have a pronounced effect on population extirpation when the two viruses coexist. This has important implications for wildlife management, because it is likely that such seasonal interplay and disease dynamics has a strong effect on long-term population viability for many species.

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Habitat factors related to wild rabbit population trends after the initial impact of rabbit haemorrhagic disease

Wildlife Research ◽

10.1071/wr05107 ◽

2006 ◽

Vol 33 (6) ◽

pp. 467 ◽

Cited By ~ 27

Author(s):

Carlos Calvete ◽

Enrique Pelayo ◽

Javier Sampietro

Keyword(s):

Habitat Quality ◽

Population Trends ◽

Wild Rabbit ◽

Pest Species ◽

Predator Species ◽

Rabbit Population ◽

Habitat Factors ◽

Rabbit Haemorrhagic Disease ◽

Haemorrhagic Disease

The European wild rabbit (Oryctolagus cuniculus) is an introduced pest species in Australia and New Zealand. Rabbits have a devastating negative impact on agricultural production and biodiversity in these countries, and Rabbit Haemorrhagic Disease (RHD) is currently included in control strategies for rabbit populations. On the other hand, the European wild rabbit is a key native prey species in the Iberian Peninsula. Since the arrival of RHD, however, rabbit populations have undergone dramatic decreases and several predator species at risk of extinction are currently dependent on the rabbit population density. Therefore, from the point of view of biodiversity conservation, evaluating habitat correlates and trends of rabbit populations after the first RHD epizootic is of great interest to improve the long-term control or promotion of wild rabbit populations. We estimated the relationship between habitat factors and long-term population trends as well as the relationships between habitat factors and rabbit abundance 2 and 14 years after the arrival of RHD in several Iberian rabbit populations. We observed that only 26% of surveyed populations seemed to experience an increase in rabbit abundance over the last 12 years and that this increase was higher in the low-rabbit-abundance areas of l992, leading to high rabbit abundance in 2004. Our results suggested that short- and long-term impacts of RHD were related to habitat quality. The initial impact of RHD was higher in more suitable habitats, but increasing long-term population trends were positively related to good habitat quality.

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The emergence of rabbit haemorrhagic disease virus: will a non-pathogenic strain protect the UK?

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2001.0897 ◽

2001 ◽

Vol 356 (1411) ◽

pp. 1087-1095 ◽

Cited By ~ 22

Author(s):

P.J. White ◽

R.A. Norman ◽

R.C. Trout ◽

E.A. Gould ◽

P.J. Hudson

Keyword(s):

Disease Virus ◽

Pathogenic Strain ◽

Rabbit Haemorrhagic Disease Virus ◽

Rabbit Haemorrhagic Disease ◽

Seroprevalence Data ◽

Age Structured ◽

Reproductive Rates ◽

The Uk ◽

Haemorrhagic Disease ◽

Age Structured Model

Rabbit haemorrhagic disease virus emerged in China in 1984, and has killed hundreds of millions of wild rabbits in Australia and Europe. In the UK there appears to be an endemic non–pathogenic strain, with high levels of seroprevalence being recorded, in the absence of associated mortality. Using a seasonal, age–structured model we examine the hypothesis that differences in rabbit population demography differentially affect the basic reproductive rates ( R 0 ) of the pathogenic and non–pathogenic strains, leading to each dominating in some populations and not others. The strain with the higher R 0 excluded the other, with the dynamics depending upon the ratio of the two R 0 values. When the non–pathogenic strain dominated, the pathogenic strain caused only transient mortality, although this could be significant when the two R 0 values were similar. When the pathogenic strain dominated, repeated epidemics led to host eradication. Seroprevalence data suggest that the non–pathogenic strain may be protecting some, but not all UK populations, with half being ‘at risk’ from invasion by the pathogenic strain and a fifth prone to significant transient mortality. We identify key questions for empirical research to test this prediction.

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