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doi: 10.7554/eLife.50095.

Antagonism between parasites within snail hosts impacts the transmission of human schistosomiasis

Affiliations

Antagonism between parasites within snail hosts impacts the transmission of human schistosomiasis

Martina R Laidemitt et al. Elife. .

Abstract

Human disease agents exist within complex environments that have underappreciated effects on transmission, especially for parasites with multi-host life cycles. We examined the impact of multiple host and parasite species on transmission of the human parasite Schistosoma mansoni in Kenya. We show S. mansoni is impacted by cattle and wild vertebrates because of their role in supporting trematode parasites, the larvae of which have antagonistic interactions with S. mansoni in their shared Biomphalaria vector snails. We discovered the abundant cattle trematode, Calicophoron sukari, fails to develop in Biomphalaria pfeifferi unless S. mansoni larvae are present in the same snail. Further development of S. mansoni is subsequently prevented by C. sukari's presence. Modeling indicated that removal of C. sukari would increase S. mansoni-infected snails by two-fold. Predictable exploitation of aquatic habitats by humans and their cattle enable C. sukari to exploit S. mansoni, thereby limiting transmission of this human pathogen.

Keywords: Schistosoma mansoni; antagonism; ecology; epidemiology; global health; neglected tropical diseases; pastoralism; schistosomiasis; trematode biodiversity.

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Conflict of interest statement

ML, LA, HW, MM, GM, EL No competing interests declared

Figures

Figure 1.
Figure 1.. Trematode biodiversity in the S. mansoni hyperendemic area of western Kenya.
(A) The different types of trematode cercariae recovered either uniquely from B. pfeifferi from streams or from B. sudanica from the lakeshore, or that were recovered from both snail species (in red), confirmed with mitochondrial barcodes. (B) Kasabong (ephemeral stream) and Asao (perennial stream), the overall prevalence of larval trematode infections in B. pfeifferi is shown along with pie charts showing the composition of the trematode infections. Note the large proportions of infections comprised of C. sukari or S. mansoni. (C) A sample of six trematode with inferred life cycles (in some cases directly documented) to point out the variety of invertebrate and vertebrate hosts (and plants) involved in such cycles. (D) Peak prevalence of S. mansoni (indicated on vertical axis as the percent shedding cercariae) from three different Biomphalaria taxa to experimental infection with S. mansoni miracidia (five miracida/snail) derived from local school children. (E) The prevalence of C. sukari, S. mansoni, and other trematodes from bimonthly surveys of Kasabong and Asao. Note C. sukari is the most abundant trematode in both locations. The turtle, carp and frog images in panel C were reproduced from Pixabay (https://pixabay.com/photos/turtle-animal-wildlife-wild-nature-1517920/, https://pixabay.com/vectors/animal-carp-fish-freshwater-lake-2029698/, and https://pixabay.com/photos/tree-frog-anuran-frog-amphibians-299886/ respectively), under the terms of the Pixabay license (https://pixabay.com/service/license/).
Figure 2.
Figure 2.. Trematode hierarchy in B. pfeifferi at Asao Stream.
The dominance hierarchy was worked out through both experimental superinfections of snails with existing infections (green numbers), and by maintaining infected snails from the field to see if they switched from shedding one type of cercaria to another (orange numbers). Percentages shown are the prevalence of infected B. pfeifferi (shedding/total number of B. pfeifferi collected) for each group.
Figure 3.
Figure 3.. Human and cattle parasite interactions at Asao Stream.
(A) Field-derived B. pfeifferi shown not to be shedding any cercariae at the time of collection were either left as unexposed controls or were exposed to S. mansoni (five miracidia/snail). Note that, unexpectedly, exposed snails were just as likely to subsequently shed C. sukari as S. mansoni cercariae compared to the control groups (p=<0.001). A few unexposed snails also shed cercariae, indicating that some of the snails had prepatent snails at the time of infection. (B) The prevalence of lab-reared B. pfeifferi exposed to various combinations of miracidia (see horizontal axis) of C. sukari and/or S. mansoni that subsequently shed cercariae of either species. Exposures to either species were with five miracidia/snail, 50 or 60 snails were used for each of 5 treatments for three separate experiments (total of 850 snails used). Separate ANOVAs were done for S. mansoni and C. sukari (each involving comparison of four groups), followed by pairwise comparisons. (C) Histological section of B. pfeifferi exposed to C. sukari for 8 days. Note the undeveloped sporocyst and the layer of hemocytes around it. (D) Histological section of B. pfeifferi exposed to S. mansoni for 8 days. The sporocyst has grown considerably and has developing daughter sporocysts within.
Figure 4.
Figure 4.. Field observations supported experimental results.
(A) Graph showing the number of single infections of B. pfeifferi with either S. mansoni or C. sukari and the number of observed double infections, which was significantly fewer than the number of double infections expected by chance (p=<0.001). (B) Correlation between the abundance of S. mansoni and C. sukari infections (XY pairs = 25, Pearson r = 0.622, p=0.0009) in B. pfeifferi from our stream survey data (prevalence of each parasite from 25 collection time points).
Figure 5.
Figure 5.. Mathematical model combining field and experimental observations.
(A) At three different levels of S. mansoni prevalence in snails, the predicted reduction in prevalence of shedding snails from our transmission model due to the presence of C. sukari is estimated. In each case, the proportion of snails shedding S. mansoni is reduced by at least one half in the presence of C. sukari. (B) Relationship from model showing how S. mansoni cercariae production is maximized in this system only when the input of S. mansoni miracidia is very high relative to the input of C. sukari miracidia.
Figure 5—figure supplement 1.
Figure 5—figure supplement 1.. Conceptual diagram of the mathematical model.
Each snail class includes both juvenile and adult age groups.
Figure 5—figure supplement 2.
Figure 5—figure supplement 2.. The proportion of snails shedding S. mansoni and C. sukari under a range of miracidial inputs and exposure rates.
The impact of miracidial input levels on the proportion of snails shedding each parasite and the miracidial input levels which result in levels seen in our field data vary with B. pfeifferi exposure rates.
Figure 5—figure supplement 3.
Figure 5—figure supplement 3.. The infection prevalence of S. mansoni and C. sukari in B. pfeifferi and their cercarial production are sensitive to both the exposure rate per week per snail density in the habitat and the weekly input of S. mansoni miracidia (3a), but less sensitive to the weekly input of C. sukari miracidia (3b).

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