RESUMEN
Digenean trematodes are a large, complex group of parasitic flatworms that infect an incredible diversity of organisms, including humans. Larval development of most digeneans takes place within a snail (Gastropoda). Compatibility between snails and digeneans is often very specific, such that suitable snail hosts define the geographical ranges of diseases caused by these worms. The immune cells (hemocytes) of a snail are sentinels that act as a crucial barrier to infection by larval digeneans. Hemocytes coordinate a robust and specific immunological response, participating directly in parasite killing by encapsulating and clearing the infection. Hemocyte proliferation and differentiation are influenced by unknown digenean-specific exogenous factors. However, we know nothing about the endogenous control of hemocyte development in any gastropod model. Here, we identify and functionally characterize a progranulin [Biomphalaria glabrata granulin (BgGRN)] from the snail B. glabrata, a natural host for the human blood fluke Schistosoma mansoni Granulins are growth factors that drive proliferation of immune cells in organisms, spanning the animal kingdom. We demonstrate that BgGRN induces proliferation of B. glabrata hemocytes, and specifically drives the production of an adherent hemocyte subset that participates centrally in the anti-digenean defense response. Additionally, we demonstrate that susceptible B. glabrata snails can be made resistant to infection with S. mansoni by first inducing hemocyte proliferation with BgGRN. This marks the functional characterization of an endogenous growth factor of a gastropod mollusc, and provides direct evidence of gain of resistance in a snail-digenean infection model using a defined factor to induce snail resistance to infection.
Asunto(s)
Hemocitos/fisiología , Hemocitos/parasitología , Péptidos y Proteínas de Señalización Intercelular/administración & dosificación , Schistosoma mansoni/fisiología , Esquistosomiasis mansoni/parasitología , Caracoles/parasitología , Animales , Hemocitos/efectos de los fármacos , Interacciones Huésped-Parásitos/efectos de los fármacos , Schistosoma mansoni/efectos de los fármacos , Esquistosomiasis mansoni/prevención & control , Caracoles/citologíaRESUMEN
BACKGROUND: Cercarial dermatitis, colloquially "swimmer's itch", is a rash contracted in natural bodies of water, when people are exposed to skin-penetrating, larval flatworm parasites of the family Schistosomatidae, that emerge from aquatic snails. Swimmer's itch is a globally-distributed, allergic condition, of which we know very little regarding local dynamics of transmission. This study aims to gather relevant information on swimmer's itch in Canada, from multiple perspectives, including the human experience, parasite and host presence and distributions, and insight from historical perspectives. METHODS: Herein we utilize a mixed-methods approach towards examining the environmental health issue of swimmer's itch in Canadian lakes from a nation-wide viewpoint, with an example from Alberta. We examine the human perspective of having contracted swimmer's itch through a self-reporting surveillance system implemented over a 5-year period. We also conducted a 3-year species survey of parasites and intermediate snail hosts within lakes in central Alberta and compiled this data with snail and vertebrate (definitive) host survey data from across Alberta to examine potential for future spread. We compare the results from our surveys to a historical review of the literature to examine the extent of swimmer's itch across Canada and identify where future efforts should be focused. RESULTS: Over 3800 cases of swimmer's itch were captured across Canada by the self-reporting surveillance system. Swimmer's itch cases were reported from every province except Prince Edward Island. Species surveys in Alberta revealed 7 new parasite and host records, with potential for swimmer's itch to occur throughout most of the province based on host distributions. A review and comparison to the literature has highlighted several knowledge gaps surrounding schistosome species, host species and their distributions and contributions towards swimmer's itch. CONCLUSIONS: Swimmer's itch is a greater environmental health hazard across Canada than previous literature would have alluded. This study provides proof-of-concept for the utility of a self-reporting surveillance system for swimmer's itch in Canada. Recommendations are made towards implementing a systems-thinking approach that incorporates citizen-scientists for future research, management, and policy surrounding swimmer's itch.
Asunto(s)
Prurito/epidemiología , Schistosomatidae , Infecciones por Trematodos/epidemiología , Animales , Canadá/epidemiología , Humanos , Lagos , Schistosomatidae/genética , Schistosomatidae/aislamiento & purificación , Caracoles/parasitología , Encuestas y Cuestionarios , NataciónRESUMEN
Zygocercous (aggregating) cercarial larvae were recently discovered emerging from a physid snail during a molecular survey of cercariae from molluscs in lakes in central Alberta, Canada. This manuscript delves into the characterization of these cercariae through morphological and molecular techniques and provides the first genetic information for a zygocercous larval trematode. Analyses of cytochrome c oxidase I of mitochondrial DNA and two partial regions of nuclear ribosomal DNA sequences revealed the zygocercous cercariae to belong to the genus Australapatemon Sudarikov, 1959. Further analyses of sequences of Australapatemon burti (Miller, 1923), from cercariae and adults collected from across North America, indicate a complex of nine genetically-distinct lineages within this species, a surprising level of diversity. The zygocercous cercariae, along with adult worms collected from ducks in Manitoba, Canada, and from Mexico, represent one of these lineages, and are herein described as Australapatemon mclaughlini n. sp. Seven lineages cannot yet be identified, but one is tentatively identified as Australapatemon burti.
Asunto(s)
Trematodos/clasificación , Animales , Cercarias/clasificación , ADN Mitocondrial , ADN Ribosómico/genética , Patos/parasitología , Tipificación Molecular , América del Norte , Filogenia , Caracoles/parasitología , Trematodos/genéticaRESUMEN
Digenean trematode distributions, compatibility profiles with their snail hosts, and complete life cycles remain mysteries in many parts of the world. Surveys of digenean biology and ecology provide further insight and perspective into just how incredibly diverse and important helminth parasites are in shaping local ecosystems. Past surveys have provided substantial characterizations of adult digeneans within their definitive hosts, and many now have contributed toward furthering our understanding of larval digeneans within their intermediate host communities. However, much information about the diversity of digeneans and their relationships with their snail intermediate hosts are lacking in many locations across the globe. This is certainly true in Canada, where few records related to digenean-snail relationships exist. Currently, there is a need for more information about the presence and distribution of digeneans across Canada, and how this compares to other parts of North America and beyond. To address this diversity gap in Western Canada, six lakes within central Alberta were surveyed for the presence of snails and larval digenean species and their associations. This investigation into the diversity of digeneans utilized a combined approach of morphological and molecular tools to identify 39 digenean species among five snail host species, from biweekly collections, taken over the course of 2 years (2013-2014). Here, digenean-snail combinations, presence, and distribution across sampling sites and lakes are reported. Overall, this survey contributes new information toward digenean-snail compatibility, life cycles, and distribution in Northern lake ecosystems within North America.
Asunto(s)
Interacciones Huésped-Parásitos , Estadios del Ciclo de Vida , Caracoles/parasitología , Trematodos/crecimiento & desarrollo , Infecciones por Trematodos/parasitología , Alberta , Animales , Ecología , Ecosistema , Geografía , Especificidad del Huésped , Humanos , Lagos , Larva , América del Norte , Alineación de Secuencia , Análisis de Secuencia de ADN , Caracoles/clasificación , Encuestas y Cuestionarios , Trematodos/clasificación , Trematodos/citología , Trematodos/genéticaRESUMEN
Fibrinogen-related proteins or FREPs constitute a large family of molecules, defined by the presence of a fibrinogen-related domain (FReD). These molecules are found in all animals and are diverse in both form and function. Here, we review the current understanding of gastropod FREPs, which are characterized by the presence of a fibrinogen domain connected to one or two immunoglobulin superfamily domains by way of a short interceding region. We present a historical perspective on the discovery of FREPs in gastropods followed by a summary of advances made in the nearly two decades of research focused on the characterization of FREPs in Biomphalaria glabrata (BgFREPs). Topics covered include BgFREP genomic architecture, predicted structure and known functions, structural comparisons between BgFREPs, and evidence of somatic diversification. Also examined are the expression patterns of BgFREPs during snail development and immunological challenges. Recent functional characterization of the role BgFREPs play in the defence response against digenean trematodes is also presented, as well as new data investigating the nucleotide-level genomic conservation of FREPs among Pulmonate gastropods. Finally, we identify areas in need of further research. These include confirming and identifying the specific binding targets of BgFREPs and elucidating how they later engage snail haemocytes to elicit an immunological response, precise mechanisms and importance of BgFREP diversification, characterizing the tissue expression patterns of BgFREPs, as well as addressing whether gastropod FREPs retain immunological importance in alternative snail-trematode associations or more broadly in snail-pathogen interactions.
Asunto(s)
Biomphalaria/genética , Biomphalaria/inmunología , Inmunidad Innata , Inmunoglobulinas/genética , Animales , Biomphalaria/metabolismo , Inmunoglobulinas/metabolismoRESUMEN
Freshwater gastropods of the genera Lymnaea Lamarck, 1799, Physa Draparnaud, 1801, Gyraulus Charpentier, 1837, Radix Montfort, 1810, and Stagnicola Jeffreys, 1830 are considered suitable intermediate hosts for avian schistosomes. A large trematode biodiversity survey performed across 3 yr on 6 lakes in Alberta confirmed 3 already-reported snail hosts for 7 North American avian schistosomes; however, the cytochrome c oxidase subunit 1 (COI) nucleotide sequence from 1 cercarial sample (from a single specimen of Planorbella trivolvis) was distinct from all other COI schistosome sequences. As part of a simultaneous, comparable study of P. trivolvis by us in Michigan, we collected another cercarial type from 6 lakes that was 99% similar (COI) to the aforementioned cercarial type. Phylogenetic analyses of the COI and 28S rDNA genes recovered the former cercaria in a clade of avian schistosomes. In Michigan, the feces of a Canada goose (Branta canadensis Linnaeus, 1758) had a miracidium with an identical COI nucleotide sequence. Preliminary swimmer's itch and cercarial emergence studies were performed to determine if the cercariae could cause swimmer's itch and to study the emergence pattern as compared with species of Trichobilharzia Skrjabin and Zakharow, 1920.
Asunto(s)
Gastrópodos/parasitología , Schistosoma/aislamiento & purificación , Alberta , Animales , Secuencia de Bases , Teorema de Bayes , Aves , Cercarias/anatomía & histología , Cercarias/clasificación , Cercarias/aislamiento & purificación , Dermatitis/parasitología , Complejo IV de Transporte de Electrones/genética , Heces/parasitología , Humanos , Lagos , Michigan , Filogenia , ARN Ribosómico 28S/genética , Schistosoma/anatomía & histología , Schistosoma/clasificación , Schistosoma/fisiología , Alineación de SecuenciaRESUMEN
Parasites have been neglected from most biodiversity surveys even though they are an essential component of ecosystems and intimately associated with the free-living communities within them. Parasites with complex life cycles, such as digenean trematode flatworms, utilize at least two host species within an ecosystem for their development and transmission, taking advantage of species networks to complete their life cycles. Despite this knowledge, our understanding of the processes that contribute to parasite community assembly, and which limit their geographic distributions, are rudimentary, including the importance of host diversity. Utilizing recent advancements in the identification of cryptic trematode species through molecular barcoding, we examined patterns of community assembly involving 79 species in six Alberta lakes over three years. Specifically, we focused on spatiotemporal variation in trematode diversity within their snail first intermediate hosts (component communities), how this might relate to host diversity through the specificity of host-parasite relationships, and the role of certain environmental factors in structuring these communities. We found substantial natural fluctuations of trematode communities through space and time within these lakes. Trematode communities were diverse, showing an overall positive relationship with snail diversity, but were often dominated by a few common species. We found that ecoregion and lake trophic status were key predictors for the presence of these trematode species. Such information is key for understanding how biodiversity alterations may affect parasite community composition, as well as our ability to formulate predictive models, by considering how this could influence both species richness and evenness.
RESUMEN
Despite over 100 years of digenean trematode parasite species descriptions, from a wide diversity of vertebrate and invertebrate host species, our ability to recognize the diversity of trematode species within a single lake remains an incredible challenge. The most challenging aspect is the identification of species from larval stages derived from intermediate hosts, due to the disjointed data of adult worm morphological descriptions, from which species are named, and links to corresponding molecular identifiers in depauperate databases. Cryptic species also play a significant role in the challenge of linking trematode larvae to adults, species identifications, and estimating diversity. Herein, we utilize a large, longitudinal dataset of snail first-intermediate host infection data from lakes in Alberta, Canada, to infer trematode larval diversity using molecular phylogenetics and snail host associations. From our assessments, we uncover a diversity of 79 larval trematode species among just five snail host species. Only 14 species were identified to a previously described species, while the other 65 species are either cryptic or otherwise unrepresented by mitochondrial genes in GenBank. This study currently represents the largest and most diverse singular molecular survey of trematode larval fauna composed of over one thousand mitochondrial sequences. Surprisingly, rarefaction analyses indicate we have yet to capture the complete diversity of trematodes from our sampling area.
RESUMEN
Swimmer's itch (cercarial dermatitis) is a nuisance encountered by bathers and recreational water users worldwide. The condition is caused by the penetration of larval digenean trematodes (cercariae) of the family Schistosomatidae, into the skin, following their release into freshwater from pulmonate snails that serve as the intermediate hosts for these parasites. This study utilizes qPCR-based cercariometry to monitor and quantify cercariae from water samples collected at 5 lakes in northern Michigan. The resolution provided by qPCR facilitated assessment of the environmental and biological drivers of swimmer's itch-causing cercariae concentrations, allowing us to demonstrate that cercarial abundance is greatest at the top of the water column, in locations with prevailing on- and alongshore winds.