Understanding links between microbial communities and emerging fungal pathogens in complex ecosystem

Lead Research Organisation: Imperial College London
Department Name: School of Public Health

Abstract

Modern-day amphibians are known to be suffering rates of extinction that far exceed any other class of vertebrates, including those experienced by mammals and birds, and nearly one third of amphibian species are threatened. The question of why amphibians are going extinct at these accelerated rates has puzzled scientists for three decades. A clue to the mystery came about when scientists working in Central America and Australia noted that the rapid declines in amphibian biodiversity were spreading in a wave-like manner. These patterns of decline were caused by an emerging infectious disease and in 1997 researchers discovered that a fungal pathogen, called a 'chytrid', was the cause, naming it Batrachochytrium dendrobatidis (Bd). Since then, our research has identified South East Asia as the cradle of this amphibian pandemic, and has mapped the spread of Bd worldwide At the same time, alongside finding regions of the world where Bd is highly pathogenic, we have also discovered places where it is not causing any obvious disease which begs the question Why?

Increasingly, we find that the invasion, establishment and amplification of Bd in uninfected amphibians is strongly influence by the microbial communities that are found inhabiting the skins of amphibians. As Alexander Fleming famously discovered, microbes predate and attack one another with a diverse array of strategies and our research seeks to understand how this microbial warfare influences whether an amphibian community survives, or succumbs, to its infection. This question will be addressed by using high-throughput DNA sequencing technologies to characterise the microbes on amphibians around the world using molecular barcoding techniques. Our main idea is that the amphibians that survive infection infection are 'clothed' by a protective community of bacteria and fungi. We will show whether this it true, then will attempt to identify the toxic molecules that are protecting the amphibians from their chytrid onslaught.

Finally, we will seek to isolate and grow microbes that are protective against Bd - sometimes called 'probiotics'. Here, we will extend our focus to include fungi because (and as Fleming showed) they can be very potent protectors against invasive organisms. We already have isolated candidate fungal 'promycotics', and we will use experiments to determine whether they do in fact protect amphibians against lethal infection by Bd; such promycotics may then offer a much-needed biocontrol against emerging pathogens such as Bd. This, ultimately, is the major applied goal of our project.

Planned Impact

Who will benefit from our research?

Our work will be of direct use to those working to stem the spread of invasive species and infection. Major project stakeholders are the GB non-native species secretariat, DEFRA, the Animal and Plant Health Agency and Natural England whom all work to contain the spread of infection into GB. Alongside Government, there is a UK-wide network of NGO's whom work on amphibian conservation and the threat that chytrids present - two of our Project Partners are FrogLife whom have supported our work on Great Crested Newts over the years. Outside of the UK, there is a global network of conservation biologists, international NGOs ('Save the Frogs!'; 'Amphibian Ark'; the IUCN), national NGOs ('KARCH'; 'Museo Nacional Ciencias Naturales') whom we are actively engaged in with in facilitating attempts to understand and mitigate the panzootic of chytrids and other fungal infections (bat White Nose Syndrome, sudden oak death, crayfish plague, Ash dieback). Our methods and data are of direct relevance to understanding patterns of transmission and host loss. As such our research will directly impact the policy and activities that these end-users and stakeholders deliver: A direct example is our 2014 work with the Morris Animal Foundation and Mohamed Bin Zayed Species Conservation Fund to assess whether an outbreak of Bd is occurring on Madagascar - this resulted in a 'top 100 paper' out of 11,000 in Scientific Reports 2015.

More widely, our research addresses the broader issue of biosecurity and pathogen evolution. A major output of globalisation is a more homogenised biota and it is becoming increasingly recognised that novel plagues constitute a major threat to biodiversity and ecosystem function. Our work is of interest to policy advisors and trade bodies (the OIE, the EU, OECD) and scientists working to understand the ecosystem-level impact of invasive species. Our main point of interaction with the UK government is via the 'Amphibians Health Committee' that comprises academics, NGO's and government officials (APHA/ VLA/ DEFRA/ NNSS): this committee works to ensure that the UK response to the introduction of new pathogenic chytrids is evidence-based and not reactive.

2. How will they benefit?

Project outputs framed for the visiting public at Imperial College and ZSL: Visitors to ZSL's London Zoo (annually 1 million) can see our research outputs via the newly refurbished AmphibianConservation Centre. Two dedicated video screens report results of the amphibian disease research program and daily live presentations made by keepers, researchers and trained presenters provide a proactive platform for informing the public regarding amphibian diseases, amphibian conservation, and our efforts to understand and mitigate the problem. Additionally, several thousand Greater London school children take part in ZSL's EdExcel program, a large component of which comprises presentations by members of the amphibian disease research team. Regular public symposia have amphibian disease issues as the topic, hosted by notables such as Sir David Attenborough. At Imperial College the team regularly presents at our summer Science Festival and Fringe event - these event's attract many thousands of public participants.

Publications

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Description Our genomic databases of batrachochytrid presence, incidence and genotype have assisted in a global, quantitative assessment of the amphibian chytridiomycosis panzootic that demonstrated its role in the decline of at least 501 amphibian species over the past half-century, including 90 presumed extinctions. This research has been recently published:

O'Hanlon, S. J., A. Rieux, R. A. Farrer, G. M. Rosa, B. Waldman, A. Bataille, T. A. Kosch, K. A. Murray, B. Brankovics, M. Fumagalli, M. D. Martin, N. Wales, M. Alvarado-Rybak, K. A. Bates, L. Berger, S. Boll, L. Brookes, F. Clare, E. A. Courtois, A. A. Cunningham, T. M. Doherty-Bone, P. Ghosh, D. J. Gower, W. E. Hintz, J. Hoglund, T. S. Jenkinson, C. F. Lin, A. Laurila, A. Loyau, A. Martel, S. Meurling, C. Miaud, P. Minting, F. Pasmans, D. S. Schmeller, B. R. Schmidt, J. M. G. Shelton, L. F. Skerratt, F. Smith, C. Soto-Azat, M. Spagnoletti, G. Tessa, L. F. Toledo, A. Valenzuela-Sanchez, R. Verster, J. Voros, R. J. Webb, C. Wierzbicki, E. Wombwell, K. R. Zamudio, D. M. Aanensen, T. Y. James, M. T. P. Gilbert, C. Weldon, J. Bosch, F. Balloux, T. W. J. Garner, and M. C. Fisher. 2018. 'Recent Asian origin of chytrid fungi causing global amphibian declines', Science, 360: 621-+.
Exploitation Route This research is leading to tighter international and national biosecurity in the wildlife trade
Sectors Environment,Transport

 
Description 1) We have trained a global network of scientists to undertake research on chytrid pathogens through standardising protocols for isolation, monitoring and surveillance. This work has been used to map the disease worldwide and has contributed to a global, quantitative assessment of the amphibian chytridiomycosis pandemic, identifying chytrids as the causative agent in the declines of 500 amphibian species over the past half-century, including 90 presumed extinctions. The evidence generated has been used to identify species most at risk of infection, to locate yet-uninfected regions of the planet, and to forecast future associations between global warming and the severity of infection in montane regions. 2) We have developed a non-lethal method for isolating amphibian-parasitising chytrids and have used this approach to build a culture collection of the organism from 5 continents, 23 countries and 62 amphibian species. We used genomic analysis of this biological repository to identify the origins of B. dendrobatidis to East Asia, and to date this pathogens emergence to the early 20th Century. This dataset has been key evidence identifying Asia as a hotspot for batrachochytrids, resulting in increased biosecurity for amphibians that are exported from this region. 3) Our work has been central in solving the enigmatic mass mortalities and declines of fire salamanders in the Netherlands, resulting in the discovery of a new species of pathogenic chytrid, B. salamandrivorans, which we identified as also having an Asian origin5. This discovery has led to bans in the trade of salamander species in a growing number of countries / regions alongside the listing of B. salamandrivorans by the OIE (World Organisation for Animal Health). To date, these listings and bans have prevented the establishment of this batrachochytrid in the Americas. 4) Our disease mitigation research is on-going, but has included investigating safe treatments to cure the disease in captive animals; whether field treatments can be used to reduce the impact of the disease on wild populations of amphibians; whether the impact of the pathogen can be reduced through pre-exposure of animals to a hypovirulent lineage of the fungus; and whether bacterial communities are protective against disease. Ongoing work on Mallorca has led to the local elimination of infections in the IUCN Red List Critically Endangered Alytes muletensis, and ongoing efforts are predicted to lead to complete clearance from the island.
First Year Of Impact 2018
Sector Environment
Impact Types Policy & public services

 
Description Wildlife disease 
Organisation Zoological Society of London
Department Institute of Zoology
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Research grants won and commenced Publications in leading journals (Science) Genomic epidemiology and experimental analysis
Collaborator Contribution Shared research staff and resources
Impact Research publications, grants, conferences and training