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1.
BMC Genomics ; 25(1): 192, 2024 Feb 19.
Artigo em Inglês | MEDLINE | ID: mdl-38373909

RESUMO

BACKGROUND: Control and elimination of schistosomiasis is an arduous task, with current strategies proving inadequate to break transmission. Exploration of genetic approaches to interrupt Schistosoma mansoni transmission, the causative agent for human intestinal schistosomiasis in sub-Saharan Africa and South America, has led to genomic research of the snail vector hosts of the genus Biomphalaria. Few complete genomic resources exist, with African Biomphalaria species being particularly underrepresented despite this being where the majority of S. mansoni infections occur. Here we generate and annotate the first genome assembly of Biomphalaria sudanica sensu lato, a species responsible for S. mansoni transmission in lake and marsh habitats of the African Rift Valley. Supported by whole-genome diversity data among five inbred lines, we describe orthologs of immune-relevant gene regions in the South American vector B. glabrata and present a bioinformatic pipeline to identify candidate novel pathogen recognition receptors (PRRs). RESULTS: De novo genome and transcriptome assembly of inbred B. sudanica originating from the shoreline of Lake Victoria (Kisumu, Kenya) resulted in a haploid genome size of ~ 944.2 Mb (6,728 fragments, N50 = 1.067 Mb), comprising 23,598 genes (BUSCO = 93.6% complete). The B. sudanica genome contains orthologues to all described immune genes/regions tied to protection against S. mansoni in B. glabrata, including the polymorphic transmembrane clusters (PTC1 and PTC2), RADres, and other loci. The B. sudanica PTC2 candidate immune genomic region contained many PRR-like genes across a much wider genomic region than has been shown in B. glabrata, as well as a large inversion between species. High levels of intra-species nucleotide diversity were seen in PTC2, as well as in regions linked to PTC1 and RADres orthologues. Immune related and putative PRR gene families were significantly over-represented in the sub-set of B. sudanica genes determined as hyperdiverse, including high extracellular diversity in transmembrane genes, which could be under pathogen-mediated balancing selection. However, no overall expansion in immunity related genes was seen in African compared to South American lineages. CONCLUSIONS: The B. sudanica genome and analyses presented here will facilitate future research in vector immune defense mechanisms against pathogens. This genomic/transcriptomic resource provides necessary data for the future development of molecular snail vector control/surveillance tools, facilitating schistosome transmission interruption mechanisms in Africa.


Assuntos
Biomphalaria , Esquistossomose mansoni , Animais , Humanos , Schistosoma mansoni/genética , Biomphalaria/genética , Transcriptoma , Genômica , Quênia
2.
PLoS Negl Trop Dis ; 18(2): e0011983, 2024 Feb.
Artigo em Inglês | MEDLINE | ID: mdl-38421953

RESUMO

Schistosomiasis is one of the world's most devastating parasitic diseases, afflicting 251 million people globally. The Neotropical snail Biomphalaria glabrata is an important intermediate host of the human blood fluke Schistosoma mansoni and a predominant model for schistosomiasis research. To fully exploit this model snail for biomedical research, here we report a haplotype-like, chromosome-level assembled and annotated genome of the homozygous iM line of B. glabrata that we developed at the University of New Mexico. Using multiple sequencing platforms, including Illumina, PacBio, and Omni-C sequencing, 18 sequence contact matrices representing 18 haploid chromosomes (2n = 36) were generated (337x genome coverage), and 96.5% of the scaffold sequences were anchored to the 18 chromosomes. Protein-coding genes (n = 34,559), non-coding RNAs (n = 2,406), and repetitive elements (42.52% of the genome) were predicted for the whole genome, and detailed annotations for individual chromosomes were also provided. Using this genomic resource, we have investigated the genomic structure and organization of the Toll-like receptor (TLR) and fibrinogen-domain containing protein (FReD) genes, the two important immune-related gene families. Notably, TLR-like genes are scattered on 13 chromosomes. In contrast, almost all (39 of 40) fibrinogen-related genes (FREPs) (immunoglobulin superfamily (IgSF) + fibrinogen (FBG)) are clustered within a 5-million nucleotide region on chromosome 13, yielding insight into mechanisms involved in the diversification of FREPs. This is the first genome of schistosomiasis vector snails that has been assembled at the chromosome level, annotated, and analyzed. It serves as a valuable resource for a deeper understanding of the biology of vector snails, especially Biomphalaria snails.


Assuntos
Biomphalaria , Hemostáticos , Esquistossomose , Humanos , Animais , Biomphalaria/genética , Haplótipos , Fibrinogênio , Cromossomos/genética
3.
Int J Parasitol ; 54(5): 247-256, 2024 Apr.
Artigo em Inglês | MEDLINE | ID: mdl-38311021

RESUMO

Improvements in diagnostics for schistosomiasis in both humans and snail hosts are priorities to be able to reach the World Health Organization (WHO) goal of eliminating the disease as a public health problem by 2030. In this context, molecular isothermal amplification tests, such as Recombinase Polymerase Amplification (RPA), are promising for use in endemic areas at the point-of-need for their accuracy, robustness, simplicity, and time-effectiveness. The developed recombinase polymerase amplification assay targeting the Schistosoma mansoni mitochondrial minisatellite region (SmMIT-RPA) was used to detect S. mansoni DNA from both laboratory and field Biomphalaria snails. Laboratory snails were experimentally infected and used at one, seven, and 28 days post-exposure (dpe) to 10 S. mansoni miracidia to provide samples in the early pre-patent infection stage. Field samples of Biomphalaria spp. were collected from the Mucuri Valley and Jequitinhonha Valley regions in the state of Minas Gerais, Brazil, which are endemic for S. mansoni. The sensitivity and specificity of the SmMIT-RPA assay were analysed and compared with existing loop-mediated isothermal amplification (LAMP), PCR-based methods, parasitological examination of the snails, and nucleotide sequencing. The SmMIT-RPA assay was able to detect S. mansoni DNA in the experimentally infected Biomphalaria glabrata as early as one dpe to 10 miracidia. It also detected S. mansoni infections (55.5% prevalence) in the field samples with the highest accuracy (100% sensitivity and specificity) compared with the other molecular tests used as the reference. Results from this study indicate that the SmMIT-RPA assay is a good alternative test to be used for snail xenomonitoring of S. mansoni due to its high sensitivity, accuracy, and the possibility of detecting early pre-patent infection. Its simplicity and portability also make it a suitable methodology in low-resource settings.


Assuntos
Biomphalaria , Esquistossomose mansoni , Esquistossomose , Animais , Humanos , Schistosoma mansoni/genética , Recombinases/genética , Repetições Minissatélites , Biomphalaria/genética , Esquistossomose mansoni/diagnóstico , Esquistossomose mansoni/epidemiologia , Nucleotidiltransferases/genética , DNA de Helmintos/genética
4.
Sci Rep ; 14(1): 1820, 2024 01 20.
Artigo em Inglês | MEDLINE | ID: mdl-38245605

RESUMO

Vitellogenesis is the most important process in animal reproduction, in which yolk proteins play a vital role. Among multiple yolk protein precursors, vitellogenin (Vtg) is a well-known major yolk protein (MYP) in most oviparous animals. However, the nature of MYP in the freshwater gastropod snail Biomphalaria glabrata remains elusive. In the current study, we applied bioinformatics, tissue-specific transcriptomics, ovotestis-targeted proteomics, and phylogenetics to investigate the large lipid transfer protein (LLTP) superfamily and ferritin-like family in B. glabrata. Four members of LLTP superfamily (BgVtg1, BgVtg2, BgApo1, and BgApo2), one yolk ferritin (Bg yolk ferritin), and four soma ferritins (Bg ferritin 1, 2, 3, and 4) were identified in B. glabrata genome. The proteomic analysis demonstrated that, among the putative yolk proteins, BgVtg1 was the yolk protein appearing in the highest amount in the ovotestis, followed by Bg yolk ferritin. RNAseq profile showed that the leading synthesis sites of BgVtg1 and Bg yolk ferritin are in the ovotestis (presumably follicle cells) and digestive gland, respectively. Phylogenetic analysis indicated that BgVtg1 is well clustered with Vtgs of other vertebrates and invertebrates. We conclude that, vitellogenin (BgVtg1), not yolk ferritin (Bg yolk ferritin), is the major yolk protein precursor in the schistosomiasis vector snail B. glabrata.


Assuntos
Biomphalaria , Esquistossomose , Animais , Biomphalaria/genética , Vitelogeninas/genética , Vitelogeninas/metabolismo , Multiômica , Filogenia , Proteômica , Proteínas do Ovo/metabolismo , Ferritinas/genética , Schistosoma mansoni/metabolismo
5.
Gene ; 884: 147742, 2023 Oct 30.
Artigo em Inglês | MEDLINE | ID: mdl-37634882

RESUMO

BACKGROUND: Schistosomiasis is a neglected tropical disease caused by Schistosoma and affects over 240 million people worldwide. One of the most prominent causative agents is Schistosoma mansoni, which develops inside the intermediate host. Biomphalaria tenagophila is the second most important vector of schistosomiasis in Brazil and the Taim population is completely resistant to infection by S. mansoni. OBJECTIVE: This study aims to identify and characterize B. tenagophila microRNAs (miRNAs) and evaluate their differential expression in S. mansoni-susceptible and -resistant populations of B. tenagophila. METHODS: Two populations of B. tenagophila snails, susceptible and resistant to S. mansoni infection, were used to investigate the small RNA response of these snails after being infected with the parasite. Small RNA sequencing and quantitative real-time PCR were employed to identify and validate differentially expressed miRNAs. Bioinformatics analysis were performed to identify miRNA precursors and mature and evaluate their differential expression. FINDINGS: The study predicted 173 mature miRNAs and 123 precursors. Among them were six Lophotrochozoa-specific miRNAs, three mollusk-specific miRNAs, and six pre-miRNAs in a cluster. The small RNA sequencing and RT-PCR of B. tenagophila samples allowed assessing the expression patterns of miRNAs. MAIN CONCLUSIONS: The results obtained may support future studies in Biomphalaria spp., generating a global impact on disease control.


Assuntos
Biomphalaria , MicroRNAs , Humanos , Animais , Biomphalaria/genética , MicroRNAs/genética , Schistosoma mansoni/genética , Brasil , Biologia Computacional
6.
PLoS Negl Trop Dis ; 17(8): e0011506, 2023 08.
Artigo em Inglês | MEDLINE | ID: mdl-37578945

RESUMO

Intestinal schistosomiasis is hyperendemic in many sub-Saharan African countries. In Uganda, it is endemic at both Lake Albert (LA) and Lake Victoria (LV) and caused by S. mansoni that uses Biomphalaria snails as obligatory intermediate snail hosts. To shed light on local patterns of infection, we utilised two PCR-based methods to detect S. mansoni within Biomphalaria spp. as collected at the Ugandan shorelines of Lake Albert and Lake Victoria from 2009-2010. Overall, at our Lake Albert sites, the mean infection prevalence was 12.5% (15 of 120 snails), while at our Lake Victoria sites the prevalence was 5% (3 of 60 snails). At our Lake Albert sites, the highest infection prevalence of 13.3% (8 of 60 snails) was at Walukuba, while at our Lake Victoria sites, the highest infection prevalence of 10% (2 of 20 snails) was at Lwanika. Three species of Biomphalaria, B. pfeifferi, B. stanleyi and B. sudanica, were identified at our Lake Albert collection sites, while only a single species, B. choanomphala, was identified at our Lake Victoria collection sites. Biomphalaria stanleyi (2 of 20 snails; 15%) had the highest infection prevalence, followed by B. sudanica (5 of 60 snails; 13.3%), B. pfeifferi (4 of 40 snails; 10%) and B. choanomphala (3 of 60 snails; 5%). Of the Biomphalaria species identified, B. choanomphala had the highest haplotype (gene) diversity score, followed by B. stanleyi, B. sudanica and B. pfeifferi. Sites with a higher mean prevalence of S. mansoni infection had higher intra-species haplotype diversity scores than sites with a lower mean prevalence. The wet seasons (LA: 13.3%; LV: 8.7%) had a consistently higher mean infection prevalence of S. mansoni than the dry seasons (LA: 9.5%; LV: 5%) for all species and all sites tested at both Lake Albert (n = 480) and Lake Victoria (n = 320), though the difference was not statistically significant.


Assuntos
Biomphalaria , Esquistossomose mansoni , Humanos , Animais , Biomphalaria/genética , Esquistossomose mansoni/epidemiologia , Schistosoma mansoni/genética , Uganda/epidemiologia , Estações do Ano , Lagos , Caramujos
7.
Front Cell Infect Microbiol ; 13: 1167787, 2023.
Artigo em Inglês | MEDLINE | ID: mdl-37168391

RESUMO

Introduction: The genus Biomphalaria in Brazil includes 11 species and one subspecies, three of which are intermediate hosts of Schistosoma mansoni. Due to the recent evolution of this group, some species are difficult to identify based on morphological characters, making the use of genetic markers necessary for species identification. This study aimed to evaluate the use of partial sequences of the cytochrome c oxidase I (coi) gene for the identification of Biomphalaria species using phylogenetic reconstruction and species delimitation algorithms. The study tested the use of DNA barcoding technique for species delimitation within the genus. Methods: DNA barcoding was performed by sequencing a partial region of the coi gene from specimens, and the sequences were analyzed using phylogenetic reconstruction and algorithms to delimit Operational Taxonomic Units (OTUs). Results: The study found that the use of the coi gene in the reconstruction of the phylogeny of the genus might be an alternative for understanding the evolution and dispersion of species. However, this marker alone is not enough to solve complex taxonomic problems within the genus. A total of 223 sequences were analyzed, 102 of which could be separated using the barcode gap, enabling the correct identification of seven taxa. Discussion: The study demonstrated that accurate mollusk identification is necessary for effective schistosomiasis control. The DNA barcoding methodology was found to be promising for accurate mollusk identification, which is crucial for concentrating schistosomiasis control efforts in places where it is needed.


Assuntos
Biomphalaria , Animais , Biomphalaria/genética , Filogenia , Código de Barras de DNA Taxonômico/métodos , DNA , Schistosoma mansoni/genética
8.
Int J Mol Sci ; 24(5)2023 Mar 03.
Artigo em Inglês | MEDLINE | ID: mdl-36902324

RESUMO

Schistosomiasis, or also generally known as bilharzia or snail fever, is a parasitic disease that is caused by trematode flatworms of the genus Schistosoma. It is considered by the World Health Organisation as the second most prevalent parasitic disease after malaria and affects more than 230 million people in over 70 countries. People are infected via a variety of activities ranging from agricultural, domestic, occupational to recreational activities, where the freshwater snails Biomphalaria release Schistosoma cercariae larvae that penetrate the skin of humans when exposed in water. Understanding the biology of the intermediate host snail Biomphalaria is thus important to reveal the potential spread of schistosomiasis. In this article, we present an overview of the latest molecular studies focused on the snail Biomphalaria, including its ecology, evolution, and immune response; and propose using genomics as a foundation to further understand and control this disease vector and thus the transmission of schistosomiasis.


Assuntos
Biomphalaria , Esquistossomose mansoni , Esquistossomose , Animais , Humanos , Schistosoma mansoni/genética , Biomphalaria/genética , Caramujos , Genômica
9.
Molecules ; 28(2)2023 Jan 05.
Artigo em Inglês | MEDLINE | ID: mdl-36677618

RESUMO

UDP-Gal: glycoprotein-N-acetylgalactosamine ß-1,3-galactosyltransferase (T-synthase, EC 2.4.1.122) catalyses the transfer of the monosaccharide galactose from UDP-Gal to GalNAc-Ser/Thr, synthesizing the core 1 mucin type O-glycan. Such glycans play important biological roles in a number of recognition processes. The crucial role of these glycans is acknowledged for mammals, but a lot remains unknown regarding invertebrate and especially mollusc O-glycosylation. Although core O-glycans have been found in snails, no core 1 ß-1,3-galactosyltransferase has been described so far. Here, the sequence of the enzyme was identified by a BlastP search of the NCBI Biomphalaria glabrata database using the human T-synthase sequence (NP_064541.1) as a template. The obtained gene codes for a 388 amino acids long transmembrane protein with two putative N-glycosylation sites. The coding sequence was synthesised and expressed in Sf9 cells. The expression product of the putative enzyme displayed core 1 ß-1,3-galactosyltransferase activity using pNP-α-GalNAc as the substrate. The enzyme showed some sequence homology (49.40% with Homo sapiens, 53.69% with Drosophila melanogaster and 49.14% with Caenorhabditis elegans) and similar biochemical parameters with previously characterized T-synthases from other phyla. In this study we present the identification, expression and characterisation of the UDP-Gal: glycoprotein-N-acetylgalactosamine ß-1,3-galactosyltransferase from the fresh-water snail Biomphalaria glabrata, which is the first cloned T-synthase from mollusc origin.


Assuntos
Biomphalaria , Galactosiltransferases , Animais , Humanos , Acetilgalactosamina , Sequência de Aminoácidos , Biomphalaria/enzimologia , Biomphalaria/genética , Caenorhabditis elegans , Drosophila melanogaster , Galactosiltransferases/genética , Galactosiltransferases/química , Mucinas , Polissacarídeos/química , Difosfato de Uridina
10.
Trans R Soc Trop Med Hyg ; 117(5): 401-402, 2023 05 02.
Artigo em Inglês | MEDLINE | ID: mdl-36594275

RESUMO

The interaction between snails and species of Schistosoma results from an evolutionary process with an intrinsic host-parasite specificity to the snail genus. Faced with this fact, the recent molecular-based report on the potential infection of the thiarid Melanoides tuberculata with human schistosome should be cautiously interpreted. The high sensibility of molecular tools can result in false positives, perhaps by amplifying DNA from an external (contaminant) or invasive stage of schistosome found in this non-permissive snail host. Thus, parasitological data are mandatory to extrapolate the importance of the finding for the epidemiology and control of schistosomiasis.


Assuntos
Biomphalaria , Esquistossomose , Animais , Humanos , Biomphalaria/genética , Biomphalaria/parasitologia , Caramujos , Schistosoma/genética , Esquistossomose/epidemiologia , Schistosoma mansoni
11.
Ann Parasitol ; 68(3): 473-481, 2022.
Artigo em Inglês | MEDLINE | ID: mdl-36508500

RESUMO

In the study of the biology of trematode species, the knowledge of the larval stages in snail hosts is important to elucidate their complete life cycle. The goal of the present study was to describe a new tetracotyle-type metacercaria found in the freshwater mollusk Biomphalaria straminea sampled in a rice field from Corrientes province, Argentina. To this end, 1,768 snails were collected from the cultivated plots and irrigated channels during the flooding periods (from the time of sowing to soon after rice harvesting) between December 2016 and May 2017. We used morphological and molecular analysis to characterize the tetracotyle-type metacercariae. Its morphological traits and the internal transcribed spacers (ITS1 and ITS2 plus 5.8S; ~1200 pb) from nuclear ribosomal DNA (rDNA) were amplified and sequenced. From 1,768 specimens of B. straminea screened, 52 were found infected with metacercariae of tetracotyle type (2.9%) that were identified as Cotylurus genus. A total of 218 metacercariae were found encysted in the ovotestis or between the mantle and viscera of B. straminea. Bioinformatic analysis showed that the metacercarial rDNA sequences shared 94% identity with those of Cotylurus gallinulae from Mexico and 100% identity with those of Cotylurus sp. from Brazil. In this study, the morphological descriptions are supplemented with the first molecular identification of a metacercaria related to Cotylurus parasitizing planorbids from Argentina. Also, our study provides a new morphological description in B. straminea, thus broadening the geographical distribution. The life cycle of this Cotylurus metacercariae is unknown and there are no reports of adult stages parasitizing waterfowl in Argentina.


Assuntos
Biomphalaria , Trematódeos , Animais , Biomphalaria/genética , Metacercárias/genética , Trematódeos/genética , Caramujos , Estágios do Ciclo de Vida , Filogenia
12.
PeerJ ; 10: e13971, 2022.
Artigo em Inglês | MEDLINE | ID: mdl-36117535

RESUMO

Background: Biomphalaria glabrata is a snail intermediate host for Schistosoma mansoni, a trematode responsible for human schistosomiasis. BS90 is one of the most well studied strains of B. glabrata owing to its high resistance to infection by most strains of S. mansoni. An F2 mapping study from 1999 identified two RAPD markers that associated with what appeared to be single-locus, dominant resistance by the BS90 population relative to the susceptible M-line population. One marker cannot be mapped, but the other, OPM-04, maps to within 5 Mb of PTC2, a region we recently showed has a very large effect on resistance within another snail population challenged by the same strain of parasite (PR1). Here we tested the hypothesis that the PTC2 region contains the causal gene/s that explain the iconic resistance of BS90 snails. Methods: We used marker-assisted backcrossing to drive the BS90 version of the PTC2 region (+/-~1 Mb on either side) into an M-line (susceptible strain) genetic background, and the M-line version into a BS90 genetic background. We challenged the offspring with PR1-strain schistosomes and tested for effects of allelic variation in the PTC2 region in a common genetic background. Results: Relative to M-line haplotypes, the BS90 haplotype actually confers enhanced susceptibility. So we reject our original hypothesis. One possible explanation for our result was that the causal gene linked to OPM-04 is near, but not in the PTC2 block that we introgressed into each line. So we used an F2 cross to independently test the effects of the PTC2 and OPM-04 regions in a randomized genetic background. We confirmed that the BS90 haplotype confers increased susceptibility, and we see a similar, although non-significant effect at OPM-04. We discuss possible reasons why our results differed so dramatically from those of the 1999 study. We also present Pacbio assemblies of the PTC2 and flanking region in BS90 and M-line, compare with previously published PTC2 haplotypes, and discuss candidate genes that might be behind the enhanced susceptibility of the BS90 haplotype.


Assuntos
Biomphalaria , Schistosoma mansoni , Animais , Humanos , Schistosoma mansoni/genética , Biomphalaria/genética , Técnica de Amplificação ao Acaso de DNA Polimórfico , Interações Hospedeiro-Parasita/genética , Caramujos/genética , Genótipo
13.
Pestic Biochem Physiol ; 186: 105154, 2022 Aug.
Artigo em Inglês | MEDLINE | ID: mdl-35973759

RESUMO

Organophosphorus pesticides like Chlorpyrifos 48%EC were widely used to control agricultural pests. The present study aimed to evaluate the toxic effects of Chlorpyrifos 48%EC on B. alexandrina snails, the intermediate host of Schistosoma mansoni. After exposure of snails to serial concentrations to determine the LC50, thirty snails for each sublethal concentration (LC10 2.1 and LC25 5.6 mg/l) in each group were exposed for 24 h followed by another 24 h for recovery. After recovery random samples were collected from hemolymph and tissue to measure the impacts on Phagocytic index, histological, biochemical, and molecular parameters. The current results showed a toxic effect of Chlorpyrifos 48%EC on adult B. alexandrina snails after 24 h of exposure at LC50 9.6 mg/l. After exposure to the sub-lethal concentrations of this pesticide, it decreased the total number of hemocytes and the percentage of small cells, while increased the percentage of hyalinocytes. The granulocyte percentage was increased after exposure to LC10, while after LC25, it was decreased compared to the control group. Also, the light microscopical examination showed that some granulocytes have plenty of granules, vacuoles and filopodia. Some hyalinocytes were contained shrinked nuclei, incomplete cell division and forming pseudopodia. Besides, the phagocytic index of hemocytes was significantly increased than control in all treated groups. Also, these sub-lethal concentrations increased MDA and SOD activities, while, tissue NO, GST and TAC contents were significantly decreased after exposure. Levels of Testosterone (T) and Estradiol (E) were increased significantly after exposure compared with control group. The present results showed that the concentration of DNA and RNA was highly decreased after exposure to LC10, 25 than the control group. Therefore, B. alexandrina snails could be used as a bio monitor of the chemical pollution. Besides, this pesticide could reduce the transmission of schistosomiasis as it altered the biological system of these snails.


Assuntos
Biomphalaria , Clorpirifos , Moluscocidas , Praguicidas , Animais , Biomphalaria/genética , Clorpirifos/toxicidade , Hemócitos , Moluscocidas/toxicidade , Compostos Organofosforados/farmacologia , Praguicidas/farmacologia
14.
Front Immunol ; 13: 903158, 2022.
Artigo em Inglês | MEDLINE | ID: mdl-35967434

RESUMO

Schistosomiasis is a disease caused by trematode parasites of the genus Schistosoma that affects approximately 200 million people worldwide. Schistosomiasis has been a persistent problem in endemic areas as there is no vaccine available, currently used anti-helmintic medications do not prevent reinfection, and most concerning, drug resistance has been documented in laboratory and field isolates. Thus, alternative approaches to curtail this human disease are warranted. Understanding the immunobiology of the obligate intermediate host of these parasites, which include the freshwater snail Biomphalaria glabrata, may facilitate the development of novel methods to stop or reduce transmission to humans. Molecules from the thioester-containing protein (TEP) superfamily have been shown to be involved in immunological functions in many animals including corals and humans. In this study we identified, characterized, and compared TEP transcripts and their expression upon S. mansoni exposure in resistant and susceptible strains of B. glabrata snails. Results showed the expression of 11 unique TEPs in B. glabrata snails. These transcripts present high sequence identity at the nucleotide and putative amino acid levels between susceptible and resistant strains. Further analysis revealed differences in several TEPs' constitutive expression levels between resistant and susceptible snail strains, with C3-1, C3-3, and CD109 having higher constitutive expression levels in the resistant (BS90) strain, whereas C3-2 and TEP-1 showed higher constitutive expression levels in the susceptible (NMRI) strain. Furthermore, TEP-specific response to S. mansoni miracidia exposure reiterated their differential expression, with resistant snails upregulating the expression of both TEP-4 and TEP-3 at 2 h and 48 h post-exposure, respectively. Further understanding the diverse TEP genes and their functions in invertebrate animal vectors will not only expand our knowledge in regard to this ancient family of immune proteins, but also offer the opportunity to identify novel molecular targets that could aid in the efforts to develop control methods to reduce schistosomiasis transmission.


Assuntos
Biomphalaria , Schistosoma mansoni , Animais , Biomphalaria/genética , Biomphalaria/metabolismo , Biomphalaria/parasitologia , Suscetibilidade a Doenças , Expressão Gênica , Proteínas/genética , Schistosoma mansoni/genética , Schistosoma mansoni/metabolismo , Fatores de Transcrição/genética
15.
BMC Genomics ; 23(1): 543, 2022 Jul 29.
Artigo em Inglês | MEDLINE | ID: mdl-35906538

RESUMO

The immune repertoires of mollusks beyond commercially important organisms such as the pacific oyster Crassostrea gigas or vectors for human pathogens like the bloodfluke planorb Biomphalaria glabrata are understudied. Despite being an important model for neural aging and the role of inflammation in neuropathic pain, the immune repertoire of Aplysia californica is poorly understood. Recent discovery of a neurotropic nidovirus in Aplysia has highlighted the need for a better understanding of the Aplysia immunome. To address this gap in the literature, the Aplysia reference genome was mined using InterProScan and OrthoFinder for putative immune genes. The Aplysia genome encodes orthologs of all critical components of the classical Toll-like receptor (TLR) signaling pathway. The presence of many more TLRs and TLR associated adapters than known from vertebrates suggest yet uncharacterized, novel TLR associated signaling pathways. Aplysia also retains many nucleotide receptors and antiviral effectors known to play a key role in viral defense in vertebrates. However, the absence of key antiviral signaling adapters MAVS and STING in the Aplysia genome suggests divergence from vertebrates and bivalves in these pathways. The resulting immune gene set of this in silico study provides a basis for interpretation of future immune studies in this important model organism.


Assuntos
Biomphalaria , Crassostrea , Animais , Aplysia/genética , Biomphalaria/genética , Crassostrea/genética , Genoma , Humanos , Imunidade Inata , Transdução de Sinais
16.
Sci Rep ; 12(1): 8243, 2022 05 17.
Artigo em Inglês | MEDLINE | ID: mdl-35581232

RESUMO

Schistosomiasis is a medically significant disease caused by helminth parasites of the genus Schistosoma. The schistosome life cycle requires chemically mediated interactions with an intermediate (aquatic snail) and definitive (human) host. Blocking parasite development within the snail stage requires improved understanding of the interactions between the snail host and the Schistosoma water-borne free-living form (miracidium). Innovations in snail genomics and aquatic chemical communication provide an ideal opportunity to explore snail-parasite coevolution at the molecular level. Rhodopsin G protein-coupled receptors (GPCRs) are of particular interest in studying how trematode parasites navigate towards their snail hosts. The potential role of GPCRs in parasites makes them candidate targets for new antihelminthics that disrupt the intermediate host life-cycle stages, thus preventing subsequent human infections. A genomic-bioinformatic approach was used to identify GPCR orthologs between the snail Biomphalaria glabrata and miracidia of its obligate parasite Schistosoma mansoni. We show that 8 S. mansoni rhodopsin GPCRs expressed within the miracidial stage share overall amino acid similarity with 8 different B. glabrata rhodopsin GPCRs, particularly within transmembrane domains, suggesting conserved structural features. These GPCRs include an orphan peptide receptor as well as several with strong sequence homologies with rhabdomeric opsin receptors, a serotonin receptor, a sulfakinin (SK) receptor, an allatostatin-A (buccalin) receptor and an FMRFamide receptor. Buccalin and FMRFa peptides were identified in water conditioned by B. glabrata, and we show synthetic buccalin and FMRFa can stimulate significant rates of change of direction and turn-back responses in S. mansoni miracidia. Ortholog GPCRs were identified in S. mansoni miracidia and B. glabrata. These GPCRs may detect similar ligands, including snail-derived odorants that could facilitate miracidial host finding. These results lay the foundation for future research elucidating the mechanisms by which GPCRs mediate host finding which can lead to the potential development of novel anti-schistosome interventions.


Assuntos
Biomphalaria , Parasitos , Esquistossomose mansoni , Animais , Biomphalaria/genética , Interações Hospedeiro-Parasita , Humanos , Peptídeos , Feromônios , Receptores Acoplados a Proteínas G/genética , Rodopsina/genética , Schistosoma mansoni , Esquistossomose mansoni/parasitologia , Caramujos , Água
17.
Microbiol Spectr ; 10(2): e0184321, 2022 04 27.
Artigo em Inglês | MEDLINE | ID: mdl-35254167

RESUMO

Biomphalaria glabrata transmits schistosomiasis mansoni which poses considerable risks to hundreds of thousands of people worldwide, and is widely used as a model organism for studies on the snail-schistosome relationship. Gut microbiota plays important roles in multiple aspects of host including development, metabolism, immunity, and even behavior; however, detailed information on the complete diversity and functional profiles of B. glabrata gut microbiota is still limited. This study is the first to reveal the gut microbiome of B. glabrata based on metagenome-assembled genome (MAG). A total of 28 gut samples spanning diet and age were sequenced and 84 individual microbial genomes with ≥ 70% completeness and ≤ 5% contamination were constructed. Bacteroidota and Proteobacteria were the dominant bacteria in the freshwater snail, unlike terrestrial organisms harboring many species of Firmicutes and Bacteroidota. The microbial consortia in B. glabrata helped in the digestion of complex polysaccharide such as starch, hemicellulose, and chitin for energy supply, and protected the snail from food poisoning and nitrate toxicity. Both microbial community and metabolism of B. glabrata were significantly altered by diet. The polysaccharide-degrading bacterium Chryseobacterium was enriched in the gut of snails fed with high-digestibility protein and high polysaccharide diet (HPHP). Notably, B. glabrata as a mobile repository can escalate biosafety issues regarding transmission of various pathogens such as Acinetobacter nosocomialis and Vibrio parahaemolyticus as well as multiple antibiotic resistance genes in the environment and to other organisms. IMPORTANCE The spread of aquatic gastropod Biomphalaria glabrata, an intermediate host of Schistosoma mansoni, exacerbates the burden of schistosomiasis disease worldwide. This study provides insights into the importance of microbiome for basic biological activities of freshwater snails, and offers a valuable microbial genome resource to fill the gap in the analysis of the snail-microbiota-parasite relationship. The results of this study clarified the reasons for the high adaptability of B. glabrata to diverse environments, and further illustrated the role of B. glabrata in accumulation of antibiotic resistance in the environment and spread of various pathogens. These findings have important implications for further exploration of the control of snail dissemination and schistosomiasis from a microbial perspective.


Assuntos
Biomphalaria , Esquistossomose , Animais , Biomphalaria/genética , Biomphalaria/parasitologia , Carboidratos , Interações Hospedeiro-Parasita/genética , Humanos , Metagenoma , Nitrogênio
18.
Gigascience ; 112022 02 15.
Artigo em Inglês | MEDLINE | ID: mdl-35166339

RESUMO

BACKGROUND: Schistosomiasis, or bilharzia, is a parasitic disease caused by trematode flatworms of the genus Schistosoma. Infection by Schistosoma mansoni in humans results when cercariae emerge into water from freshwater snails in the genus Biomphalaria and seek out and penetrate human skin. The snail Biomphalaria straminea is native to South America and is now also present in Central America and China, and represents a potential vector host for spreading schistosomiasis. To date, genomic information for the genus is restricted to the neotropical species Biomphalaria glabrata. This limits understanding of the biology and management of other schistosomiasis vectors, such as B. straminea. FINDINGS: Using a combination of Illumina short-read, 10X Genomics linked-read, and Hi-C sequencing data, our 1.005 Gb B. straminea genome assembly is of high contiguity, with a scaffold N50 of 25.3 Mb. Transcriptomes from adults were also obtained. Developmental homeobox genes, hormonal genes, and stress-response genes were identified, and repeat content was annotated (40.68% of genomic content). Comparisons with other mollusc genomes (including Gastropoda, Bivalvia, and Cephalopoda) revealed syntenic conservation, patterns of homeobox gene linkage indicative of evolutionary changes to gene clusters, expansion of heat shock protein genes, and the presence of sesquiterpenoid and cholesterol metabolic pathway genes in Gastropoda. In addition, hormone treatment together with RT-qPCR assay reveal a sesquiterpenoid hormone responsive system in B. straminea, illustrating that this renowned insect hormonal system is also present in the lophotrochozoan lineage. CONCLUSION: This study provides the first genome assembly for the snail B. straminea and offers an unprecedented opportunity to address a variety of phenomena related to snail vectors of schistosomiasis, as well as evolutionary and genomics questions related to molluscs more widely.


Assuntos
Biomphalaria , Esquistossomose mansoni , Esquistossomose , Animais , Biomphalaria/genética , Biomphalaria/parasitologia , Vetores de Doenças , Humanos , Schistosoma mansoni/genética , Esquistossomose mansoni/parasitologia
19.
Mol Ecol ; 31(8): 2242-2263, 2022 04.
Artigo em Inglês | MEDLINE | ID: mdl-35152493

RESUMO

Schistosoma mansoni, a snail-borne, blood fluke that infects humans, was introduced into the Americas from Africa during the Trans-Atlantic slave trade. As this parasite shows strong specificity to the snail intermediate host, we expected that adaptation to South American Biomphalaria spp. snails would result in population bottlenecks and strong signatures of selection. We scored 475,081 single nucleotide variants in 143 S. mansoni from the Americas (Brazil, Guadeloupe and Puerto Rico) and Africa (Cameroon, Niger, Senegal, Tanzania, and Uganda), and used these data to ask: (i) Was there a population bottleneck during colonization? (ii) Can we identify signatures of selection associated with colonization? (iii) What were the source populations for colonizing parasites? We found a 2.4- to 2.9-fold reduction in diversity and much slower decay in linkage disequilibrium (LD) in parasites from East to West Africa. However, we observed similar nuclear diversity and LD in West Africa and Brazil, suggesting no strong bottlenecks and limited barriers to colonization. We identified five genome regions showing selection in the Americas, compared with three in West Africa and none in East Africa, which we speculate may reflect adaptation during colonization. Finally, we infer that unsampled populations from central African regions between Benin and Angola, with contributions from Niger, are probably the major source(s) for Brazilian S. mansoni. The absence of a bottleneck suggests that this is a rare case of a serendipitous invasion, where S. mansoni parasites were pre-adapted to the Americas and able to establish with relative ease.


Assuntos
Biomphalaria , Parasitos , América , Animais , Biomphalaria/genética , Biomphalaria/parasitologia , Humanos , Schistosoma mansoni/genética , Senegal/epidemiologia , Caramujos/genética , Tanzânia
20.
Immunogenetics ; 74(1): 77-98, 2022 02.
Artigo em Inglês | MEDLINE | ID: mdl-34854945

RESUMO

The immune cells of the snail Biomphalaria glabrata are classified into hyalinocyte and granulocyte subtypes. Both subtypes are essential for the proper functioning of the snail immune response, which we understand best within the context of how it responds to challenge with the human parasite Schistosoma mansoni. Granulocytes are adherent phagocytic cells that possess conspicuous granules within the cell cytoplasm. Hyalinocytes, on the other hand, are predominantly non-adherent and are known to produce a handful of anti-S. mansoni immune effectors. While our understanding of these cells has progressed, an in-depth comparison of the functional capabilities of each type of immune cell has yet to be undertaken. Here, we present the results of a single-cell RNA-seq study in which single granulocytes and hyalinocytes from S. mansoni-susceptible M-line B. glabrata and S. mansoni-resistant BS-90 B. glabrata are compared without immune stimulation. This transcriptomic analysis supports a role for the hyalinocytes as producers of immune effectors such as biomphalysin and thioester-containing proteins. It suggests that granulocytes are primarily responsible for producing fibrinogen-related proteins and are armed with various pattern-recognition receptors such as toll-like receptors with a confirmed role in the anti-S. mansoni immune response. This analysis also confirms that the granulocytes and hyalinocytes of BS-90 snails are generally more immunologically prepared than their M-line counterparts. As the first single-cell analysis of the transcriptional profiles of B. glabrata immune cells, this study provides crucial context for understanding the B. glabrata immune response. It sets the stage for future investigations into how each immune cell subtype differs in its response to various immunological threats.


Assuntos
Biomphalaria , Animais , Biomphalaria/genética , Biomphalaria/parasitologia , Perfilação da Expressão Gênica , Humanos , Proteínas , RNA-Seq , Schistosoma mansoni/genética
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