Version Changes
Revised. Amendments from Version 1
The new version of this data note specifies that the genome sequence is from a Schistosome-susceptible, albino B. glabrata NIMR strain snail. In response to comments from peer reviewers, we have also made changes to the Background text and clarified the use of different samples in the methods section.
Abstract
We present a genome assembly from an individual Biomphalaria glabrata NIMR strain (bloodfluke planorb; Mollusca; Gastropoda; Planorbidae). The genome sequence spans 850.60 megabases. Most of the assembly is scaffolded into 18 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 13.67 kilobases in length. Gene annotation of this assembly on Ensembl identified 25,327 protein-coding genes.
Keywords: Biomphalaria glabrata, bloodfluke planorb, genome sequence, chromosomal, Planorbidae
Species taxonomy
Eukaryota; Opisthokonta; Metazoa; Eumetazoa; Bilateria; Protostomia; Spiralia; Lophotrochozoa; Mollusca; Gastropoda; Heterobranchia; Euthyneura; Panpulmonata; Hygrophila; Lymnaeoidea; Planorbidae; Biomphalaria; Biomphalaria glabrata (Say, 1818) (NCBI:txid6526).
Background
The fresh-water air-breathing snail Biomphalaria glabrata is an intermediate host for Schistosoma mansoni (Lophotrochozoa, Platyhelminthes), one of the major human-infective blood fluke species that cause the neglected disease schistosomiasis.
The Biomphalaria genus includes approximately 18 species that are susceptible to S. mansoni ( DeJong et al., 2001). Most S. mansoni transmission occurs in Africa, where susceptible Biomphalaria spp are thought to have descended from neotropical Biomphalaria that were transferred to the continent. The neotropical species, B. glabrata, is the closest relative to the African species ( DeJong et al., 2001). The snails are simultaneous hermaphrodites that reproduce preferentially through outcrossing but also self-fertilisation ( Trigwell et al., 1997). Copulations are usually unidirectional, with one snail taking on a male role and the other assuming a female one ( Trigwell et al., 1997).
In addition to their reproductive biology, B. glabrata plays a central role in the life cycle of S. mansoni. Within the snails, parasite populations rapidly expand. Larval parasites penetrate the snail and develop into mother sporocysts that each produce daughter sporocysts ( Meuleman et al., 1980). The daughter sporocysts replicate, migrate throughout the snail and release a further larva stage called cercarie ( Meuleman et al., 1980). The cercariae erupt from the snails into the aquatic environment, to find and infect a mammalian definitive host and continue the life cycle. Parasite development inhibits snail reproduction – saving resources for the rapid asexual expansion of the parasite. Conversely, the immune system of B. glabrata aims to limit parasite infection. Snails have heritable differences in parasite resistance/susceptibility ( Richards & Shade, 1987) and understanding the basis of these differences is an important avenue for developing new schistosomiasis control strategies ( Bu et al., 2022a).
A draft genome (916 Mb, N50 = 48 kb) for the B. glabrata BB02 strain was previously sequenced ( Adema et al., 2017), followed by higher-contiguity genome assemblies ( Bu et al., 2022b) for the homozygous lines iM and iBS90 (N50s of 22.7 and 19.4 Mb, respectively), and most recently the chromosomes of iM have been assembled (karyotype 2 n = 36; N50 = 49.4 Mb; Zhong et al., 2024). This new annotated reference genome of a Schistosome-susceptible, albino B. glabrata NIMR strain snail will enhance ongoing efforts to understand the genomic basis of Biomphalaria-schistosome interactions and to identify potential strategies for parasite control.
Genome sequence report
The genome of an adult Biomphalaria glabrata ( Figure 1) was sequenced using Pacific Biosciences single-molecule HiFi long reads, generating a total of 16.16 Gb (gigabases) from 2.40 million reads, providing approximately 29-fold coverage. Primary assembly contigs were scaffolded with chromosome conformation Hi-C data from a different individual, which produced 78.06 Gbp from 516.92 million reads, yielding an approximate coverage of 92-fold. Specimen and sequencing information is summarised in Table 1.
Figure 1. Image of Biomphalaria glabrata (not the specimen used for genome sequencing) (Photograph by ( Lewis et al., 2008), cropped and retouched by User:Snek01., CC BY 2.5, https://commons.wikimedia.org/w/index.php?curid=7278526 ).
Table 1. Specimen and sequencing data for BioProject PRJEB52579.
| Platform | PacBio HiFi | Hi-C | RNA-seq |
|---|---|---|---|
| ToLID | xgBioGlab47 | xgBioGlab1 | xgBioGlab2 |
| Specimen ID | SAN3000165 | SAN3000136 | SAN3000140 |
| BioSample (source individual) | SAMEA10417684 | SAMEA111492540 | SAMEA10417660 |
| BioSample (tissue) | SAMEA10417747 | SAMEA111492541 | SAMEA10417723 |
| Tissue | whole organism | whole organism | whole organism |
| Instrument | Sequel IIe | Illumina NovaSeq 6000 | Illumina HiSeq 4000 |
| Run accessions | ERR9709327; ERR9709326 | ERR10395981 | ERR9682492 |
| Read count total | 4.11 million | 516.92 million | 44.27 million |
| Base count total | 25.89 Gb | 78.06 Gb | 6.68 Gb |
Manual assembly curation corrected 26 missing joins or mis-joins and 12 haplotypic duplications, reducing the assembly length by 0.47% and the scaffold number by 12.24%. The final assembly has a total length of 850.60 Mb in 43 sequence scaffolds with a scaffold N50 of 48.5 Mb ( Table 2). The snail plot in Figure 2 provides a summary of the assembly statistics, while the distribution of assembly scaffolds on GC proportion and coverage is shown in Figure 3. The cumulative assembly plot in Figure 4 shows curves for subsets of scaffolds assigned to different phyla. Most (99.46%) of the assembly sequence was assigned to 18 chromosomal-level scaffolds. Chromosome-scale scaffolds confirmed by the Hi-C data are named in order of size ( Figure 5; Table 3). While not fully phased, the assembly deposited is of one haplotype. Contigs corresponding to the second haplotype have also been deposited. The mitochondrial genome was also assembled and can be found as a contig within the multifasta file of the genome submission.
Table 2. Genome assembly data for Biomphalaria glabrata, xgBioGlab47.1.
| Genome assembly | ||
|---|---|---|
| Assembly name | xgBioGlab47.1 | |
| Assembly accession | GCA_947242115.1 | |
| Accession of alternate haplotype | GCA_947242385.1 | |
| Span (Mb) | 850.60 | |
| Number of contigs | 200 | |
| Contig N50 length (Mb) | 10.8 | |
| Number of scaffolds | 43 | |
| Scaffold N50 length (Mb) | 48.5 | |
| Longest scaffold (Mb) | 90.4 | |
| Assembly metrics * | Benchmark | |
| Consensus quality (QV) | Primary: 60.2; alternate: 60.5; combined: 60.4 | ≥ 40 |
| k-mer completeness | Primary: 75.41%; alternate: 56.54%; combined: 98.65% | ≥ 95% |
| BUSCO ** | C:94.3%[S:93.5%,D:0.8%],F:2.9%,
M:2.8%,n:5,295 |
C ≥ 95% |
| Percentage of assembly mapped to chromosomes | 99.46% | ≥ 90% |
| Organelles | Mitochondrial genome: 13.67 kb | complete single alleles |
| Genome annotation of assembly GCA_947242115.1 at Ensembl | ||
| Number of protein-coding genes | 25,327 | |
| Number of non-coding genes | 24,653 | |
| Number of gene transcripts | 92,945 | |
Assembly metric benchmarks are adapted from column VGP-2020 of “ Table 1: Proposed standards and metrics for defining genome assembly quality” from Rhie et al. (2021).
BUSCO scores based on the mollusca_odb10 BUSCO set using version 5.3.2. C = complete [S = single copy, D = duplicated], F = fragmented, M = missing, n = number of orthologues in comparison. A full set of BUSCO scores is available at https://blobtoolkit.genomehubs.org/view/CAMXHX01/dataset/CAMXHX01/busco.
Figure 2. Genome assembly of Biomphalaria glabrata, xgBioGlab47.1: metrics.
The BlobToolKit snail plot shows N50 metrics and BUSCO gene completeness. The main plot is divided into 1,000 size-ordered bins around the circumference with each bin representing 0.1% of the 850,633,761 bp assembly. The distribution of scaffold lengths is shown in dark grey with the plot radius scaled to the longest scaffold present in the assembly (90,404,365 bp, shown in red). Orange and pale-orange arcs show the N50 and N90 scaffold lengths (48,536,009 and 32,813,434 bp), respectively. The pale grey spiral shows the cumulative scaffold count on a log scale with white scale lines showing successive orders of magnitude. The blue and pale-blue area around the outside of the plot shows the distribution of GC, AT and N percentages in the same bins as the inner plot. A summary of complete, fragmented, duplicated and missing BUSCO genes in the mollusca_odb10 set is shown in the top right. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/CAMXHX01/dataset/CAMXHX01/snail.
Figure 3. Genome assembly of Biomphalaria glabrata, xgBioGlab47.1: BlobToolKit GC-coverage plot.
Blob plot of base coverage in ERR9709327 against GC proportion for sequences in assembly CAMXHX01. Sequences are coloured by phylum. Circles are sized in proportion to sequence length. Histograms show the distribution of sequence length sum along each axis. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/CAMXHX01/dataset/CAMXHX01/blob.
Figure 4. Genome assembly of Biomphalaria glabrata xgBioGlab47.1: BlobToolKit cumulative sequence plot.
The grey line shows cumulative length for all sequences. Coloured lines show cumulative lengths of sequences assigned to each phylum using the buscogenes taxrule. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/CAMXHX01/dataset/CAMXHX01/cumulative.
Figure 5. Genome assembly of Biomphalaria glabrata xgBioGlab47.1: Hi-C contact map of the xgBioGlab47.1 assembly, visualised using HiGlass.
Chromosomes are shown in order of size from left to right and top to bottom. An interactive version of this figure may be viewed at https://genome-note-higlass.tol.sanger.ac.uk/l/?d=Wp9YLRn8QbGvprL5f5rpIA.
Table 3. Chromosomal pseudomolecules in the genome assembly of Biomphalaria glabrata, xgBioGlab47.
| INSDC accession | Name | Length (Mb) | GC% |
|---|---|---|---|
| OX365773.1 | 1 | 90.4 | 36.0 |
| OX365774.1 | 2 | 65.24 | 36.0 |
| OX365775.1 | 3 | 56.62 | 36.5 |
| OX365776.1 | 4 | 56.61 | 36.0 |
| OX365777.1 | 5 | 55.05 | 35.5 |
| OX365778.1 | 6 | 54.85 | 36.0 |
| OX365779.1 | 7 | 48.54 | 36.0 |
| OX365780.1 | 8 | 47.24 | 36.0 |
| OX365781.1 | 9 | 47.12 | 36.0 |
| OX365782.1 | 10 | 45.78 | 36.5 |
| OX365783.1 | 11 | 43.1 | 36.5 |
| OX365784.1 | 12 | 39.29 | 36.5 |
| OX365785.1 | 13 | 38.96 | 36.0 |
| OX365786.1 | 14 | 37.7 | 36.0 |
| OX365787.1 | 15 | 32.88 | 36.5 |
| OX365788.1 | 16 | 32.81 | 36.0 |
| OX365789.1 | 17 | 28.84 | 36.5 |
| OX365790.1 | 18 | 24.81 | 36.5 |
| OX365791.1 | MT | 0.01 | 25.5 |
The combined primary and alternate assemblies achieve an estimated QV of 60.4. The k-mer completeness is 75.41% for the primary assembly, 56.54% for the alternate haplotype, and 98.65% for the combined assemblies. The primary assembly has a BUSCO v5.3.2 completeness of 94.3% (single = 93.5%, duplicated = 0.8%), using the mollusca_odb10 reference set ( n = 5,295).
Metadata for specimens, BOLD barcode results, spectra estimates, sequencing runs, contaminants and pre-curation assembly statistics are given at https://links.tol.sanger.ac.uk/species/6526.
Genome annotation report
The Biomphalaria glabrata genome assembly (GCA_947242115.1) was annotated at the European Bioinformatics Institute (EBI) with Ensembl Rapid Release. The resulting annotation includes 92,945 transcribed mRNAs from 25,327 protein-coding and 24,653 non-coding genes. The average transcript length is 15,613.85, with an average of 1.86 coding transcripts per gene and 7.04 exons per transcript. The annotations may be downloaded from the Ensembl site.
Methods
Sample acquisition
Albino Biomphalaria glabrata snails (NIMR strain) were obtained from the laboratory of M. Doenhoff at the University of Nottingham and cultivated at the Wellcome Sanger Institute (WSI) for five years. Prior to transfer to WSI, the colony had been cultivated in the UK since 1962, having been established and maintained by S.R. Smithers at the National Institute for Medical Research (NIMR, Mill Hill, UK) from an albino line originally established in the US ( Newton, 1953). The specimens were flash-frozen prior to nucleic acid extraction.
Specimen SAN3000165 (ToLID xgBioGlab47) was used for PacBio HiFi sequencing, xgBioGlab1 was used for Illumina Hi-C sequencing, and specimen SAN3000140 (ToLID xgBioGlab2) was used for RNA sequencing.
Nucleic acid extraction
The workflow for high molecular weight (HMW) DNA extraction at the Wellcome Sanger Institute (WSI) Tree of Life Core Laboratory includes a sequence of core procedures: sample preparation; sample homogenisation, DNA extraction, fragmentation, and clean-up. In sample preparation, the xgBioGlab47 sample was weighed and dissected on dry ice ( Jay et al., 2023). For sample homogenisation, whole organism tissue was cryogenically disrupted using the Covaris cryoPREP ® Automated Dry Pulverizer ( Narváez-Gómez et al., 2023). HMW DNA was extracted using the Automated MagAttract v2 protocol ( Oatley et al., 2023a). DNA was sheared into an average fragment size of 12–20 kb in a Megaruptor 3 system ( Bates et al., 2023). Sheared DNA was purified by solid-phase reversible immobilisation ( Oatley et al., 2023b): in brief, the method employs AMPure PB beads to eliminate shorter fragments and concentrate the DNA. The concentration of the sheared and purified DNA was assessed using a Nanodrop spectrophotometer and Qubit Fluorometer using the Qubit dsDNA High Sensitivity Assay kit. Fragment size distribution was evaluated by running the sample on the FemtoPulse system.
RNA was extracted from tissue of a different individual, xgBioGlab2, in the Tree of Life Laboratory at the WSI using the RNA Extraction: Automated MagMax™ mirVana protocol ( do Amaral et al., 2023). The RNA concentration was assessed using a Nanodrop spectrophotometer and a Qubit Fluorometer using the Qubit RNA Broad-Range Assay kit. Analysis of the integrity of the RNA was done using the Agilent RNA 6000 Pico Kit and Eukaryotic Total RNA assay.
Protocols developed by the WSI Tree of Life laboratory are publicly available on protocols.io ( Denton et al., 2023).
Sequencing
Pacific Biosciences HiFi circular consensus DNA sequencing libraries were constructed according to the manufacturers’ instructions. Poly(A) RNA-Seq libraries were constructed using the NEB Ultra II RNA Library Prep kit. DNA and RNA sequencing was performed by the Scientific Operations core at the WSI on Pacific Biosciences Sequel IIe (HiFi) and Illumina HiSeq 4000 (RNA-Seq) instruments. Hi-C data were also generated from tissue of xgBioGlab1 using the Arima-HiC v2 kit. The Hi-C sequencing was performed using paired-end sequencing with a read length of 150 bp on the Illumina NovaSeq 6000 instrument.
Genome assembly, curation and evaluation
Assembly
The original assembly of HiFi reads was performed using Hifiasm ( Cheng et al., 2021) with the --primary option. Haplotypic duplications were identified and removed with purge_dups ( Guan et al., 2020). Hi-C reads are further mapped with bwa-mem2 ( Vasimuddin et al., 2019) to the primary contigs, which are further scaffolded using the provided Hi-C data ( Rao et al., 2014) in YaHS ( Zhou et al., 2023) using the --break option. Scaffolded assemblies are evaluated using Gfastats ( Formenti et al., 2022), BUSCO ( Manni et al., 2021) and MERQURY.FK ( Rhie et al., 2020).
The mitochondrial genome was assembled using MitoHiFi ( Uliano-Silva et al., 2023), which runs MitoFinder ( Allio et al., 2020) and uses these annotations to select the final mitochondrial contig and to ensure the general quality of the sequence.
Assembly curation
The assembly was decontaminated using the Assembly Screen for Cobionts and Contaminants (ASCC) pipeline (article in preparation). Manual curation was primarily conducted using PretextView ( Harry, 2022), with additional insights provided by JBrowse2 ( Diesh et al., 2023) and HiGlass ( Kerpedjiev et al., 2018). Scaffolds were visually inspected and corrected as described by Howe et al. (2021). Any identified contamination, missed joins, and mis-joins were corrected, and duplicate sequences were tagged and removed. The process is documented at https://gitlab.com/wtsi-grit/rapid-curation .
Evaluation of the final assembly
A Hi-C map for the final assembly was produced using bwa-mem2 ( Vasimuddin et al., 2019) in the Cooler file format (Abdennur & Mirny, 2020). To assess the assembly metrics, the k-mer completeness and QV consensus quality values were calculated in Merqury ( Rhie et al., 2020). The genome readmapping pipeline was developed using the nf-core tooling ( Ewels et al., 2020), use MultiQC ( Ewels et al., 2016), and makes extensive use of the Conda package manager, the Bioconda initiative ( Grüning et al., 2018), the Biocontainers infrastructure (da Veiga Leprevost et al., 2017), and the Docker ( Merkel, 2014) and Singularity ( Kurtzer et al., 2017) containerisation solutions. The genome was also analysed within the BlobToolKit environment ( Challis et al., 2020) and BUSCO scores ( Manni et al., 2021) were calculated.
Table 4 contains a list of relevant software tool versions and sources.
Table 4. Software tools: versions and sources.
| Software tool | Version | Source |
|---|---|---|
| BlobToolKit | 4.2.1 | https://github.com/blobtoolkit/blobtoolkit |
| BUSCO | 5.3.2 | https://gitlab.com/ezlab/busco |
| Hifiasm | 0.16.1-r375 | https://github.com/chhylp123/hifiasm |
| HiGlass | 1.11.6 | https://github.com/higlass/higlass |
| Merqury.FK | 1.1.2 | https://github.com/thegenemyers/MERQURY.FK |
| MitoHiFi | 2 | https://github.com/marcelauliano/MitoHiFi |
| PretextView | 0.2 | https://github.com/wtsi-hpag/PretextView |
| purge_dups | 1.2.3 | https://github.com/dfguan/purge_dups |
| YaHS | yahs-1.1.91eebc2 | https://github.com/c-zhou/yahs |
Wellcome Sanger Institute – Legal and Governance
The materials that have contributed to this genome note have been supplied by a Darwin Tree of Life Partner. The submission of materials by a Darwin Tree of Life Partner is subject to the ‘Darwin Tree of Life Project Sampling Code of Practice’, which can be found in full on the Darwin Tree of Life website here. By agreeing with and signing up to the Sampling Code of Practice, the Darwin Tree of Life Partner agrees they will meet the legal and ethical requirements and standards set out within this document in respect of all samples acquired for, and supplied to, the Darwin Tree of Life Project.
Further, the Wellcome Sanger Institute employs a process whereby due diligence is carried out proportionate to the nature of the materials themselves, and the circumstances under which they have been/are to be collected and provided for use. The purpose of this is to address and mitigate any potential legal and/or ethical implications of receipt and use of the materials as part of the research project, and to ensure that in doing so we align with best practice wherever possible. The overarching areas of consideration are:
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•
Ethical review of provenance and sourcing of the material
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•
Legality of collection, transfer and use (national and international)
Each transfer of samples is further undertaken according to a Research Collaboration Agreement or Material Transfer Agreement entered into by the Darwin Tree of Life Partner, Genome Research Limited (operating as the Wellcome Sanger Institute), and in some circumstances other Darwin Tree of Life collaborators.
Data availability
European Nucleotide Archive: Biomphalaria glabrata. Accession number PRJEB52579; https://identifiers.org/ena.embl/PRJEB52579 ( Wellcome Sanger Institute, 2022). The genome sequence is released openly for reuse. The Biomphalaria glabrata genome sequencing initiative is part of the Darwin Tree of Life (DToL) project. All raw sequence data and the assembly have been deposited in INSDC databases. Raw data and assembly accession identifiers are reported in Table 1 and Table 2.
Author information
Members of the Wellcome Sanger Institute Tree of Life Management, Samples and Laboratory team are listed here: https://doi.org/10.5281/zenodo.12162482.
Members of Wellcome Sanger Institute Scientific Operations: Sequencing Operations are listed here: https://doi.org/10.5281/zenodo.12165051.
Members of the Wellcome Sanger Institute Tree of Life Core Informatics team are listed here: https://doi.org/10.5281/zenodo.12160324.
Members of the Tree of Life Core Informatics collective are listed here: https://doi.org/10.5281/zenodo.12205391.
Members of the Darwin Tree of Life Consortium are listed here: https://doi.org/10.5281/zenodo.4783558.
Funding Statement
This work was supported by Wellcome through core funding to the Wellcome Sanger Institute [206194, <a href=https://doi.org/10.35802/206194>https://doi.org/10.35802/206194</a>] and the Darwin Tree of Life Discretionary Award [218328, <a href=https://doi.org/10.35802/218328>https://doi.org/10.35802/218328 </a>].
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
[version 2; peer review: 4 approved]
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