[Show abstract][Hide abstract] ABSTRACT: Schistosomiasis is a debilitating neglected tropical disease that infects over 200 million people worldwide. To combat this disease, in 2012, the World Health Organization announced a goal of reducing and eliminating transmission of schistosomes. Current control focuses primarily on mass drug administration (MDA). Therefore, we monitored transmission of Schistosoma mansoni via fecal egg counts and genetic markers in a typical school based MDA setting to ascertain the actual impacts of MDA on the targeted schistosome population.
[Show abstract][Hide abstract] ABSTRACT: Gastropod immunology is informed importantly by the study of the frequent encounters snails endure with digeneans (digenetic trematodes). One of the hallmarks of gastropod-digenean associations is their specificity: any particular digenean parasite species is transmitted by a limited subset of snail taxa. We discuss the nature of this specificity, including its immunological basis. We then review studies of the model gastropod Biomphalaria glabrata indicating that the baseline responses of snails to digeneans can be elevated in a specific manner. Studies incorporating molecular and functional approaches are then highlighted, and are further suggestive of the capacity for specific gastropod immune responses. These studies have led to the compatibility polymorphism hypothesis: the interactions between diversified fibrinogen-related proteins (FREPs) and diverse carbohydrate-decorated polymorphic parasite antigens determine recognition and trigger specific immunity. Complex glycan structures are also likely to play a role in the host specificity typifying snail-digenean interactions. We conclude by noting the dynamic and consequential interactions between snails and digeneans can be considered as drivers of diversification of digenean parasites and in the development and maintenance of specific immunity in gastropods.
Developmental and comparative immunology. 07/2014;
[Show abstract][Hide abstract] ABSTRACT: As part of a global survey of schistosomes, a total of 16,109 freshwater snails representing 14 species were collected from lakes, ponds, rivers, rice fields and swamps mostly in the Terai region of southern Nepal. Only two snails were found to harbor avian schistosome cercariae even though Nepal is well known for its rich avian diversity. One schistosome infection was from an individual of Radix luteola and on the basis of phylogenetic analyses using 28S rDNA and cox1 sequences, grouped as a distinctive and previously unknown lineage within Trichobilharzia. This genus is the most speciose within the family Schistosomatidae. It includes 40 described species worldwide, and its members mostly infect anseriform birds (ducks) and two families of freshwater snails (Lymnaeidae and Physidae). The second schistosome cercaria was recovered from an individual of Indoplanorbis exustus that was also actively emerging a Petasiger-like echinostome cercaria. Although I. exustus is commonly infected with mammalian schistosomes of the Schistosoma indicum species group on the Indian subcontinent, this is the first specifically documented avian schistosome reported in this snail. Both the cercariae reported here are among the largest of all schistosome cercariae recovered to date. The I. exustus-derived schistosome clustered most closely with Macrobilharzia macrobilharzia, although it seems to represent a distinct lineage. Specimens of Macrobilharzia have thus far not been recovered from snails, being known only as adult worms from anhingas and cormorants. This study is the first to characterize by sequence data avian schistosomes recovered from Asian freshwater habitats. This approach can help unravel the complex of cryptic species causing cercarial dermatitis here and elsewhere in the world.
Parasitology International 12/2013; · 2.30 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: This review provides an update of ongoing efforts to expand our understanding of the diversity inherent within the Schistosomatidae, the parasites responsible for causing schistosomiasis and cercarial dermatitis. By revealing more of the species present, particularly among understudied avian schistosomes, we gain increased understanding of patterns of schistosome diversification, and their abilities to colonize new hosts and habitats. Schistosomes reveal a surprising ability to switch into new snail and vertebrate host species, into new intrahost habitats, and may adopt novel body forms in the process. Often these changes are not associated with deep splits or long branches in their phylogeny, suggesting some are of relatively recent origin. Several hypotheses prompted by the new observations are discussed, helping to focus thinking on processes influencing not only schistosome diversification but also their pathogenicity and abundance.
Trends in Parasitology 07/2013; · 5.51 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: For ethical and logistical reasons, population-genetic studies of parasites often rely on the non-invasive sampling of offspring shed from their definitive hosts. However, if the sampled offspring are naturally derived from a small number of parents, then the strong family structure can result in biased population-level estimates of genetic parameters, particularly if reproductive output is skewed. Here, we document and correct for the strong family structure present within schistosome offspring (miracidia) that were collected non-invasively from humans in western Kenya. By genotyping 2,424 miracidia from 12 patients at 12 microsatellite loci and using a sibship clustering program, we found that the samples contained large numbers of siblings. Furthermore, reproductive success of the breeding schistosomes was skewed, creating differential representation of each family in the offspring pool. After removing the family structure with an iterative jacknifing procedure, we demonstrated that the presence of relatives led to inflated estimates of genetic differentiation and linkage disequilibrium, and downwardly-biased estimates of inbreeding coefficients (FIS). For example, correcting for family structure yielded estimates of FST among patients that were 27 times lower than estimates from the uncorrected samples. These biased estimates would cause one to draw false conclusions regarding these parameters in the adult population. We also found from our analyses that estimates of the number of full sibling families and other genetic parameters of samples of miracidia were highly intercorrelated but are not correlated with estimates of worm burden obtained via egg counting (Kato-Katz). Whether genetic methods or the traditional Kato-Katz estimator provide a better estimate of actual number of adult worms remains to be seen. This study illustrates that family structure must be explicitly accounted for when using offspring samples to estimate the genetic parameters of adult parasite populations.
[Show abstract][Hide abstract] ABSTRACT: Because the digenetic trematode fauna of Nepal is poorly known, we began to search for schistosomes in and around Chitwan National Park (CNP) of southern Nepal. Both domestic and wild Indian elephants (Elephus maximus) are present, and we found one of two dung samples from wild elephants and 1 of 22 (4.5%) dung samples from domestic elephants to be positive for schistosome eggs. The morphology of the eggs and both cox1 and 28S sequences derived from the eggs/miracidia were consistent with Bivitellobilharzia nairi, reported here for the first time from Nepal. Also, 7 of 14 faecal samples from the Asian or greater one-horned rhinoceros (Rhinoceros unicornis) contained viable eggs indistinguishable from those of B. nairi. This identification was confirmed by comparison with both cox1 and 28S sequences from B. nairi eggs/miracidia derived from Nepalese and Sri Lankan elephants. This represents the first sequence-verified identification of a schistosome from any species of rhinoceros, and the first verified occurrence of a representative of Bivitellobilharzia (a genus of 'elephant schistosomes') in mammals other than elephants. Our work suggests that elephants and rhinos share B. nairi in CNP, even though these two members of the 'charismatic megafauna' belong to unrelated mammalian families. Their shared life style of extensive contact with freshwater habitats likely plays a role, although the snail intermediate host and mode of definitive host infection for B. nairi have yet to be documented. This report also supports Bivitellobilharzia as a monophyletic group and its status as a distinct genus within Schistosomatidae.
Journal of Helminthology 10/2012; · 1.16 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The majority of parasite species exhibit host specificity. In general, our understanding of this phenomenon is poor. We address this question using the digenean Schistosoma mansoni as our model parasite. The larval development of S. mansoni occurs in snails of the genus Biomphalaria. For example, the Neotropical snail B. glabrata supports S. mansoni development whereas the North and Central American species B. obstructa does not. A series of experiments is underway to explore B. obstructa’s lack of compatibility with S. mansoni. Snails were exposed to S. mansoni miracidia and sectioned to determine if there is an epidermal barrier that prevents penetration. Histological sections revealed that miracidia penetrated B. obstructa although no exposed snails shed S. mansoni cercariae. Second, we exposed B. obstructa to Echinostoma paraensei - a parasite known to interfere with hemocytes of B. glabrata – to see if pre-exposure to this parasite would enable development of S. mansoni in B. obstructa. Although we were successful in establishing E. paraensei infections in B. obstructa, this did not facilitate S. mansoni infection. Thus, unlike some B. glabrata strains, B. obstructa snails cannot be made more vulnerable by exposure to E. paraensei. Additional experiments are underway to determine if B. obstructa’s lack of compatibility to S. mansoni is specific to certain life stages of parasite development, or if resistance can be broken down by application of environmental stresses or by knock-down of specific immune genes.
2012 Society for Advancement of Hispanics/Chicanos and Native Americans in Science National Conference; 10/2012
[Show abstract][Hide abstract] ABSTRACT: Schistosomiasis, a neglected tropical disease, owes its continued success to freshwater snails that support production of prolific numbers of human-infective cercariae. Encounters between schistosomes and snails do not always result in the snail becoming infected, in part because snails can mount immune responses that prevent schistosome development. Fibrinogen-related protein 3 (FREP3) has been previously associated with snail defense against digenetic trematode infection. It is a member of a large family of immune molecules with a unique structure consisting of one or two immunoglobulin superfamily domains connected to a fibrinogen domain; to date fibrinogen containing proteins with this arrangement are found only in gastropod molluscs. Furthermore, specific gastropod FREPs have been shown to undergo somatic diversification. Here we demonstrate that siRNA mediated knockdown of FREP3 results in a phenotypic loss of resistance to Schistosoma mansoni infection in 15 of 70 (21.4%) snails of the resistant BS-90 strain of Biomphalaria glabrata. In contrast, none of the 64 control BS-90 snails receiving a GFP siRNA construct and then exposed to S. mansoni became infected. Furthermore, resistance to S. mansoni was overcome in 22 of 48 snails (46%) by pre-exposure to another digenetic trematode, Echinostoma paraensei. Loss of resistance in this case was shown by microarray analysis to be associated with strong down-regulation of FREP3, and other candidate immune molecules. Although many factors are certainly involved in snail defense from trematode infection, this study identifies for the first time the involvement of a specific snail gene, FREP3, in the phenotype of resistance to the medically important parasite, S. mansoni. The results have implications for revealing the underlying mechanisms involved in dictating the range of snail strains used by S. mansoni, and, more generally, for better understanding the phenomena of host specificity and host switching. It also highlights the role of a diversified invertebrate immune molecule in defense against a human pathogen. It suggests new lines of investigation for understanding how susceptibility of snails in areas endemic for S. mansoni could be manipulated and diminished.
[Show abstract][Hide abstract] ABSTRACT: One of the most poorly known of all schistosomes infecting mammals is Bivitellobilharzia loxodontae. Nearly all of our available information about this species comes from the original description of worms that were obtained from an animal park-maintained elephant in Germany, probably a forest elephant Loxodonta cyclotis, originating from the present-day Democratic Republic of Congo. We obtained schistosome eggs from faecal samples from wild forest elephants from the Central African Republic. The eggs, which were similar in size and shape to those of described B. loxodontae, were sequenced for the 28S nuclear ribosomal gene and the mitochondrial cytochrome oxidase I (cox1) gene. In a phylogenetic analysis of 28S sequences, our specimens grouped closely with B. nairi, the schistosome from the Indian elephant Elephas maximus, to the exclusion of schistosomes from other genera. However, the eggs were genetically distinct (12% distance cox1) from those of B. nairi. We conclude the specimens we recovered were of B. loxodontae and confirm this is a distinct Bivitellobilharzia species. In addition to providing the first sequence data for B. loxodontae, this report also supports Bivitellobilharzia as a monophyletic group and gives the relative phylogenetic position of the genus within the Schistosomatidae. We also provide a review of the biology of this poorly known schistosome genus.
Journal of Helminthology 02/2012; · 1.16 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: An emerging picture of the nature of immune systems across animal phyla reveals both conservatism of some features and the appearance among and within phyla of novel, lineage-specific defense solutions. The latter collectively represent a major and underappreciated form of animal diversity. Factors influencing this macroevolutionary (above the species level) pattern of novelty are considered and include adoption of different life styles, life histories, and body plans; a general advantage of being distinctive with respect to immune defenses; and the responses required to cope with parasites, many of which afflict hosts in a lineage-specific manner. This large-scale pattern of novelty implies that immunological phenomena can affect microevolutionary processes (at the population level within species) that can eventually lead to macroevolutionary events such as speciation, radiations, or extinctions. Immunologically based phenomena play a role in favoring intraspecific diversification, specialization and host specificity of parasites, and mechanisms are discussed whereby this could lead to parasite speciation. Host switching - the acquisition of new host species by parasites - is a major mechanism that drives parasite diversity and is frequently involved in disease emergence. It is also one that can be favored by reductions in immune competence of new hosts. Mechanisms involving immune phenomena favoring intraspecific diversification and speciation of host species are also discussed. A macroevolutionary perspective on immunology is invaluable in today's world, including the need to study a broader range of species with distinctive immune systems. Many of these species are faced with extinction, another macroevolutionary process influenced by immune phenomena.
[Show abstract][Hide abstract] ABSTRACT: The majority of parasite species exhibit host specificity. In general, our knowledge of why a particular parasite can infect some host species but fails to infect others is poor. To address this basic question, I will study the parasite Schistosoma mansoni which infects 200 million people in both Africa and the Neotropics. Its larval development occurs in certain species of snails of the genus Biomphalaria, but not in others: the Neotropical snail B. glabrata supports S. mansoni development whereas the closely-related North American species B. obstructa, does not. I will undertake a series of laboratory experiments to explore the underlying reasons for why B. obstructa is unable to serve as a host. To do this, I will manipulate snails to disable their protective hemocyte populations, as well as expose snails to other types of immunosuppressive parasites such as echinostomes and nematomorphs. Using RNA interference I will isolate and disable specific snail genes known to be involved in defense to see if this renders snails susceptible to infection. I will also take into consideration environmental conditions that could influence the snail's susceptibility, such as, temperature, pH, and levels of pollution in the water. These experiments will help define, for a medically important parasite, the basic factors that dictate host specificity and that prevent a North American snail from hosting this human parasite.
2011 Society for Advancement of Hispanics/Chicanos and Native Americans in Science National Conference; 10/2011
[Show abstract][Hide abstract] ABSTRACT: Coevolutionary dynamics in host-parasite interactions potentially lead to an arms race that results in compatibility polymorphism. The mechanisms underlying compatibility have remained largely unknown in the interactions between the snail Biomphalaria glabrata and Schistosoma mansoni, one of the agents of human schistosomiasis. This review presents a combination of data obtained from field and laboratory studies arguing in favor of a matching phenotype model to explain compatibility polymorphism. Investigations focused on the molecular determinants of compatibility have revealed two repertoires of polymorphic and/or diversified molecules that have been shown to interact: the parasite antigens S. mansoni polymorphic mucins and the B. glabrata fibrinogen-related proteins immune receptors. We hypothesize their interactions define the compatible/incompatible status of a specific snail/schistosome combination. This line of thought suggests concrete approaches amenable to testing in field-oriented studies attempting to control schistosomiasis by disrupting schistosome-snail compatibility.
Developmental and comparative immunology 09/2011; 37(1):1-8. · 3.29 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: A vaccine against schistosomiasis would contribute significantly to reducing the 3-70 million disability-adjusted life years lost annually to the disease. Towards this end, inoculation with the large extracellular loop (EC-2) of Schistosoma mansoni tetraspanin-2 protein (Sm-TSP-2) has proved effective in reducing worm and egg burdens in S. mansoni-infected mice. The EC-2 loop of Schistosoma japonicum TSP-2, however, has been found to be highly polymorphic, perhaps diminishing the likelihood that this antigen can be used for vaccination against this species. Here, we examine polymorphism of the EC-2 of Sm-TSP-2 in genetically unique worms derived from six individuals from Kisumu, Kenya.
International journal for parasitology 08/2011; 41(12):1249-52. · 3.39 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Here we provide the first North American report of a naturally infected snail, Gyraulus parvus, harboring the larval stages of the cosmopolitan, arterial schistosome, Dendritobilharzia pulverulenta. The relatively small cercariae of this species are shed in the early morning, are sticky, and adhere to the water's surface film. We also provide a report of the snail host, Physa gyrina, of the widespread North American passerine schistosome, Gigantobilharzia huronensis. Finally, we provide unambiguous documentation that Physa gyrina is a natural snail host for Trichobilharzia querquedulae, a schistosome primarily of dabbling ducks.
Journal of Parasitology 03/2011; 97(5):946-9. · 1.32 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The distribution of Schistosoma genotypes among individuals in snail populations provides insights regarding the dynamics of transmission and compatibility between schistosome and snail hosts. A survey of Biomphalaria alexandrina from Damietta (Nile Delta, Egypt), an area subjected to persistent schistosomiasis control efforts, provided only 17 snails infected with Schistosoma mansoni (6.1% overall prevalence), each shown by microsatellite analysis to have a single genotype infection. By contrast, recent studies of uncontrolled S. mansoni transmission foci in Kenya revealed that 4.3% Biomphalaria pfeifferi and 20-25% Biomphalaria sudanica snails had multiple genotype infections. Compared with the 3 Kenyan populations, the Egyptian population of S. mansoni also showed a lesser degree of genetic variability and was genetically differentiated from them. We suggest that tracking of genotype diversity in infected snails could be further developed to serve as an additional and valuable independent indicator of efficacy of schistosomiasis control in Egypt and elsewhere.
Journal of Parasitology 02/2011; 97(1):156-9. · 1.32 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The intestinal microbiota of animals play an important role in their energy metabolism and resistance to pathogens, and thus in maintenance of animals in their environment. We surveyed the intestinal microbiota of three species of Planorbidae (Gastropoda: Pulmonata). Cultivation-independent molecular methods were used to investigate the community composition of intestinal bacteria from individual snails: three Biomphalaria pfeifferi (Africa), two Bulinus africanus (Africa) and three Helisoma duryi (North America). PCR amplification and sequencing of 612 bacterial 16S rRNA genes yielded 282 unique DNA sequences (97% sequence similarity) among the eight individual snails sampled. The observed bacterial diversity was distributed over 18 phyla, with the greatest number of 16S rRNA gene sequences derived from the Gammaproteobacteria, Bacteroidetes and Acidobacteria. These results document the presence of highly diverse gut bacterial communities in three snail species and indicate the need for additional study to determine the roles that gut microbes play in the physiology and immunology of planorbid snails.
Journal of Molluscan Studies 01/2011; · 1.36 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Invertebrates lack adaptive immune systems homologous to those of vertebrates, yet it is becoming increasingly clear that they can produce diversified antigen recognition molecules. We have previously noted that the snail Biomphalaria glabrata produces a secreted lectin, fibrinogen-related protein 3 (FREP3), unusual among invertebrate defense molecules because it is somatically diversified by gene conversion and point mutation. Here we implicate FREP3 in playing a central role in resistance to a major group of snail pathogens, digenetic trematodes. FREP3 is up-regulated in three models of resistance of B. glabrata to infection with Schistosoma mansoni or Echinostoma paraensei, and functions as an opsonin favoring phagocytosis by hemocytes. Knock-down of FREP3 in resistant snails using siRNA-mediated interference resulted in increased susceptibility to E. paraensei, providing a direct link between a gastropod immune molecule and resistance to trematodes. FREP3 up-regulation is also associated with heightened responsiveness following priming with attenuated digenetic trematodes (acquired resistance) in this model invertebrate immune system.
Proceedings of the National Academy of Sciences 11/2010; 107(49):21087-92. · 9.81 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Paramphistomiasis is a disease of domestic and wild ruminants caused by some digenetic trematodes of the superfamily Paramphistomoidea. Human infections with certain species of paramphistomes have been reported. Given their ubiquity and their abundance within hosts, it seems likely that the importance of these worms is underestimated globally. Based on the reported difficulties of morphological identification of paramphistomes, the development of alternative approaches to better delineate species is needed. Paramphistome samples examined during this study were cercariae, rediae from snail hosts and adult flukes obtained from slaughterhouses from Kenya, Tanzania, Egypt and Nepal. The results confirm that ITS2 is a good molecular marker for paramphistome identification and can be used to determine the affiliation of samples among the different taxa of Paramphistomoidea. Our 22 samples include eight species of paramphistomes. Ten samples of paramphistome larvae (cercariae or rediae) yielded seven species and the 12 samples of adult flukes from bovines yielded four, only one of which was not also represented among the larvae. We found three cases in which the sequences for adult worms and larvae matched, thus revealing the hosts involved locally in those particular life cycles. We interpret our specimens to include five species from Kenya, two from Nepal, two from Tanzania and one from Egypt. Bulinus forskalii was found infected with three species of paramphistomes. The results of the present study will help construct a framework to facilitate identification and eventually control of this underestimated cosmopolitan group of digeneans.