IAP2-22-407

Building the molecular tools to monitor the success of biological control for schistosomiasis

Schistosomiasis is a water-borne parasitic disease, caused by trematode blood flukes of the genus Schistosoma. As an important and impactful neglected tropical disease of global importance, schistosomiasis has been subject to large-scale attempts to reduce the disease burden, with the key tool being school-based or community-wide preventative chemotherapy (mass drug administration; MDA) with the anthelminthic praziquantel. Over 1.5 billion doses of praziquantel have been donated by the manufacturer, Merck, for deworming in sub-Saharan Africa over the last 15 years. MDA has been enormously successful in reducing schistosomiasis morbidity, and this success has led to an increasing focus of using MDA to interrupt transmission in many regions, and an ultimate goal of the elimination of the disease. There is widespread agreement that successful elimination will require additional interventions to supplement MDA (Rollinson et al, 2013).

In the pre-praziquantel era, snail control was the major contributor to successful campaigns to control schistosomiasis in many regions (Sokolow et al, 2018). While snail control continues to be a major focus of research in schistosomiasis control (e.g. Allan et al. 2020) and could be very cost-effective (Lo et al. 2018) , it is no longer used at a large scale in control programmes. Snail control approaches include molluscicides, engineering and biological habitat modification and biological control. There has been concern over the broader environmental impacts of all of these approaches, potentially limiting their large-scale applicability, but biological control with native species seems likely to be the most acceptable, particularly if predators with fisheries value could be used (Ozretich et al. 2022). A number of snail predators have been proposed as likely candidates for biological control of snail numbers, including prawns, a number of bird species and fish. While the impact of snail biological control will ultimately be assessed by impact on schistosomiasis transmission, there is also a need to monitor the impact of snail control directly on the target schistosome-transmitting snails. Traditionally this involves manual searching for snails in areas of appropriate habitat, which is slow (and thus expensive) and difficult to replicate (Sokolow et al, 2018). Furthermore, a number of biological control programmes have been plagued by off-target impact on the biological community, so careful and holistic monitoring of such programmes is critical.

The Brierley lab is soon (planned for late 2022) to introduce 100,000 captive-bred tagged individuals of the native African sharptooth catfish (Clarias gariepinus) to Lake Victoria near Mwanza, Tanzania to augment the local population. In this project, we will leverage Brierley’s work to test novel molecular approaches to monitoring both the impact of the catfish release on both species of Schistosoma-transmitting snails (Biomphalaria sudanica and B. choanomphala) and other snails, but also more widely on the fauna of Lake Victoria in the Mwanza area. The Brierley team is already monitoring schistosome transmission and collecting baseline material that will become available for this project, and extensive baseline data on trematode diversity is available from the area thanks to previous work by the NHM group. The precise course of the project will depend on the interests of the student, but the student will have the opportunity to develop molecular tools to monitor snail communities and fish diets via molecular barcoding (e.g. Routtu et al. 2014) of snail and trematode diversity in environmental DNA (e.g. Douchet et al. 2022) and to monitor the populations of target snail species using amplicon panels with next-generation sequencing, as well as developing interdisciplinary fieldwork skills in malacology, fisheries biology and parasitology and expertise in bioinformatics and data analysis.

Methodology

Molecular biology approaches including PCR and next-generation sequencing, population genomics. Malacological and environmental fieldwork in Mwanza, Tanzania. Snail rearing facilities are available so colonies of the relevant species could be established.

Project Timeline

Year 1

Initial literature review of existing molecular tools. Development of molecular methods: this will include both thorough testing of the most promising primers identified in the literature on snails and trematodes relevant to Lake Victoria. Material is available for B. glabrata in Glasgow and for other species and genera of snails at the NHM, London. Testing could use material from previous projects in Lake Victoria and material from the UK where avian schistosomes are present seasonally, and cause outbreaks of cercarial dermatitis among open-water swimmers. Existing material for fish diet experiments is available from St. Andrews.

Year 2

Fieldwork in Tanzania to collect fish and snail material post-release, and collect water and sediment samples for eDNA analysis. Collections will take place in Clarias introduction and from control areas. There would also be the opportunity to be involved in collection and work with Schistosoma material, according to the interests of the student. Development of a novel SNP amplicon panel for B. sudanica and B. choanomphala. Genome assemblies for both species should be available (developed by Steinauer lab, Western University of Health Sciences, USA), but if not we could generate suitable resources as part of this project. Laboratory work to test barcoding tools on collected material. Prepare first publication describing success of barcoding approach in African setting.

Year 3

Second fieldwork trip to Tanzania for additional sampling point. Molecular processing of material collected following protocols established during year 2. During this year, the student will be encouraged to attend an International conference to present results, such as the American Society for Tropical Medicine and Hygiene meeting (Oct/Nov each year), which is preceded by the COR-NTD meeting specifically on operational research around NTD control. Comparison of eDNA barcoding estimates of fish and snail abundance with survey data and estimates of fish abundance from acoustic surveys carried out by the St Andrews team.

Year 3.5

Complete final molecular work and data analysis, and writing main publication outcomes describing the impact of Clarias release on snail population genetics, and barcoding results on impacts on the lake community. Thesis writing.

Training
& Skills

The student will receive a highly interdisciplinary training in molecular biology, freshwater biology fieldwork skills, data analysis and bioinformatics skills. Most of these skills will be acquired by training and expertise within the supervising research groups. Post-graduate students in the college of medical, veterinary and life sciences in Glasgow also receive mandatory training in transferable and research skills. The student will also gain experience in presenting research through lab meetings and attendance at national meetings such as the Malacological Society of London and the British Society for Parasitology.

References & further reading

Allan et al. 2020. Snail-Related Contributions from the Schistosomiasis Consortium for Operational Research and Evaluation Program Including Xenomonitoring, Focal Mollusciciding, Biological Control, and Modeling. Am J Trop Med Hyg. 103(S1):66-79.
Douchet et al. (2022). Make visible the invisible: Optimized development of an environmental DNA metabarcoding tool for the characterization of trematode parasitic communities. Environmental DNA, 4:627– 641.
Lo et al. 2018. Impact and cost-effectiveness of snail control to achieve disease control targets for schistosomiasis. Proc Natl Acad Sci U S A. 115: E584–E591.
Ozretich et al. 2022. The Potential for Aquaculture to Reduce Poverty and Control Schistosomiasis in Côte d’Ivoire (Ivory Coast) during an Era of Climate Change: A Systematic Review. Reviews in Fisheries Science & Aquaculture, 30:4, 467-497
Rollinson et al., 2013. Time to set the agenda for schistosomiasis elimination, Acta tropica 128:423-440.
Routtu et al. 2014. Selective and universal primers for trematode barcoding in freshwater snails. Parasitol Res. 113:2535-40.
Sokolow et al., 2018. To Reduce the Global Burden of Human Schistosomiasis, Use ‘Old Fashioned’ Snail Control. Trends in Parasitology 34:23-40.

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