Version Changes
Revised. Amendments from Version 1
In Version 2 of this data note we have added information to the Background section to contextualise our sequencing project with respect to other molecular studies in Plecoptera, and as part of the Darwin Tree of Life project. We have expanded on the results of the sequencing runs (new Table 1), and added more detail to the assembly methods section. A new section on "Assembly quality assessment" has been added to the Methods. We have replaced Figure 5 with a new labelled version in PretextView for readability. In the Data availability section we added links to the Tree of Life production pipeline suite and to sequence and metadata for this species.
Abstract
We present a genome assembly from an individual male Isoperla grammatica (the Common Yellow Sally; Arthropoda; Insecta; Plecoptera; Perlodidae). The genome sequence is 874.6 megabases in span. Most of the assembly is scaffolded into 14 chromosomal pseudomolecules, including the assembled X 1 and X 2 chromosomes. The mitochondrial genome has also been assembled and is 16.2 kilobases in length. This assembly was generated as part of the Darwin Tree of Life project, which produces reference genomes for eukaryotic species found in Britain and Ireland.
Keywords: Isoperla grammatica, Common Yellow Sally, genome sequence, chromosomal, Plecoptera
Species taxonomy
Eukaryota; Metazoa; Ecdysozoa; Arthropoda; Hexapoda; Insecta; Pterygota; Neoptera; Polyneoptera; Plecoptera; Perloidea; Perlodidae; Isoperlinae; Isoperla; Isoperla grammatica (Poda, 1761) (NCBI:txid552050).
Background
Isoperla grammatica ( Figure 1) is a western Palaearctic species found across Europe from France to Romania, south to Sicily and north to the Baltic and Fennoscandia ( Dewalt et al., 2023). It is found throughout Britain and Ireland and can be very common in some watercourses.
Figure 1. Isoperla grammatica © Jon Mortin (CC BY) Source: https://www.inaturalist.org/photos/146228992.
It is considered a eurytherm ( Graf et al., 2009) and is typically occurs in high densities in all lotic water types with stable and unstable substrata, amongst moss, leaf packets and gravel, and is often present in rivers with slight organic enrichment ( Baars & Kelly-Quinn, 2006; Costello, 1988; Frost, 1942). The widespread distribution of this species indicates that it has no preference for particular pH conditions and has been found in both neutral and episodically acidic waters ( Feeley et al., 2011; Feeley, 2012; Feeley & Kelly-Quinn, 2014; Murphy et al., 2013).
Isoperla grammatica has a univoltine life cycle ( Frost, 1942; Smith et al., 2000) with larvae present for part of two summers and the intervening winter ( Elliott, 1967; Langford, 1971; Malmqvist & Sjöström, 1989; Ulfstrand, 1968). Research in Norway and Britain indicated that eggs need warm temperatures of 7 to 12°C to initiate development, but the optimum incubation temperature is 16°C ( Elliott, 1991; Elliott, 1995; Lillehammer et al., 1989; Saltveit & Lllehammer, 1984). Larvae occur all year round in small numbers and across various sizes, indicating variability in larval growth ( Langford, 1971; Malmqvist & Sjöström, 1989; Smith et al., 2000). However, larvae typically grow rapidly in autumn and spring, although winter growth has also been noted where water temperatures were suitable ( Malmqvist & Sjöström, 1989).
Although diatom and other algal matter are also ingested, the larvae of I. grammatica are carnivorous from very early instars ( Graf et al., 2009; Malmqvist & Sjöström, 1989; Malmqvist et al., 1991). Larvae are also highly selective in their prey items ( Williams, 1987). Of the prey items found, Chironomidae and Simuliidae seem to dominate ( Elliott, 2004; Malmqvist & Sjöström, 1989; Malmqvist et al., 1991), with Williams highlighting a preference for Baetidae in Wales ( Williams, 1987). Elliott ( 2000, 2004) indicated that the feeding behaviour was by active search and was limited to the hours of dusk and dawn, with little activity during the day or at night. The adults feed on a range of pollens, fungi and fine particulate organic matter ( Tierno de Figueroa & Sánchez-Ortega, 1999).
Another contig-level assembly for this species is also available (GCA_001676475.1; submitted by Hannah C Macdonald) (data obtained via NCBI datasets, O’Leary et al., 2024). In addition, work using transcriptome and whole genome sequencing to examine the evolutionary history and taxonomy of Plecoptera has been published ( Letsch et al., 2021; South et al., 2021).
We report a chromosome-level complete genome sequence for Isoperla grammatica. This assembly was generated as part of the Darwin Tree of Life Project, which aims to generate high-quality reference genomes for all named eukaryotic species in Britain and Ireland to support research, conservation, and the sustainable use of biodiversity ( Blaxter et al., 2022).
Genome sequence report
Sequencing data
PacBio sequencing of the Isoperla grammatica specimen generated 25.55 Gb (gigabases) from 2.94 million reads, which were used to assemble the genome. GenomeScope2.0 analysis estimated the haploid genome size at 672.52 Mb, with a heterozygosity of 3.14% and repeat content of 47.49%. These estimates guided expectations for the assembly. Based on the estimated genome size, the sequencing data provided approximately 34× coverage. Hi-C sequencing produced 109.98 Gb from 728.32 million reads, which were used to scaffold the assembly. RNA sequencing data were also generated and are available in public sequence repositories, but not used in the assembly. Table 1 summarises the specimen and sequencing details.
Table 1. Specimen and sequencing data for BioProject PRJEB53729.
| Platform | PacBio HiFi | Hi-C | RNA-seq |
|---|---|---|---|
| ToLID | ipIsoGram3 | ipIsoGram4 | ipIsoGram7 |
| Specimen ID | NHMUK014360609 | NHMUK014360651 | NHMUK014361594 |
| BioSample (source individual) | SAMEA7520999 | SAMEA7521000 | SAMEA7521375 |
| BioSample (tissue) | SAMEA7521099 | SAMEA7521100 | SAMEA7521453 |
| Tissue | whole organism | whole organism | whole organism |
| Instrument | Sequel II | Illumina NovaSeq 6000 | Illumina HiSeq 4000 |
| Run accessions | ERR9878388; ERR9878387 | ERR9881687 | ERR9881692 |
| Read count total | 2.94 million | 728.32 million | 29.52 million |
| Base count total | 25.55 Gb | 109.98 Gb | 4.46 Gb |
Assembly statistics
Manual assembly curation of the assembly was done to to confirm chromosome boundaries. We also corrected 400 missing or mis-joins and removed 47 haplotypic duplications, reducing the assembly length by 1.18% and the scaffold number by 24.31%, and increasing the scaffold N50 by 27.94%.
The final assembly has a total length of 874.6 Mb in 682 sequence scaffolds with a scaffold N50 of 56.8 Mb ( Table 2). Most (95.16%) of the assembly sequence was assigned to 14 chromosomal-level scaffolds, representing 12 autosomes, and the X 1 and X 2 sex chromosomes. Chromosome-scale scaffolds confirmed by the Hi-C data have been named in order of size. ( Figure 2– Figure 5; Table 3). The scaffold order and orientation are uncertain in the following regions: chromosome 8 (29.54–40.94 Mb), chromosome 9 (2.58–20.91 Mb), and chromosome 11 (24.65–31.18 Mb). While not fully phased, the assembly deposited is of one haplotype. Contigs corresponding to the second haplotype have also been deposited.
Figure 2. Genome assembly of Isoperla grammatica, ipIsoGram3.1: metrics.
The BlobToolKit Snailplot 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 874,600,353 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 (137,496,831 bp, shown in red). Orange and pale-orange arcs show the N50 and N90 scaffold lengths (56,757,646 and 40,559,246 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 insecta_odb10 set is shown in the top right. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/ipIsoGram3.1/dataset/CAMDTW01/snail.
Figure 5. Genome assembly of Isoperla grammatica, ipIsoGram3.1: Hi-C contact map.
Hi-C contact map of the ipIsoGram3.1 assembly, visualised using PretextView and PretextSnapshot. Chromosomes are shown in order of size from left to right and top to bottom. An interactive version of this figure may be viewed in HiGlass at https://genome-note-higlass.tol.sanger.ac.uk/l/?d=FHx1cM8_RE6963zmzuaDVw.
Table 2. Genome assembly statistics.
| Assembly name | ipIsoGram3.1 |
| Assembly accession | GCA_945910005.1 |
| Alternate haplotype accession | GCA_945909985.1 |
| Assembly level | chromosome |
| Span (Mb) | 874.58 |
| Number of chromosomes | 14 |
| Number of contigs | 2,826 |
| Contig N50 | 0.65 Mb |
| Number of scaffolds | 682 |
| Scaffold N50 | 56.76 Mb |
| Sex chromosomes | X 1 and X 2 |
| Organelles | Mitochondrion: 16.16 kb |
| Metric (benchmark) | Values achieved |
| Consensus quality QV (≥ 40) | Primary: 55.3; alternate: 56.2; combined: 55.8 |
| k-mer completeness (≥ 95%) | Primary: 68.59%; alternate: 56.02%; combined: 98.25% |
| BUSCO * (S > 90%; D < 5%) | C:99.3%[S:96.6%,D:2.7%],
F:0.3%,M:0.4%,n:1,367 |
|
Percentage of assembly
assigned to chromosomes (≥ 90%) |
95.16% |
* BUSCO scores based on the insecta_odb10 BUSCO set using 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/ipIsoGram3.1/dataset/CAMDTW01/busco.
Figure 3. Genome assembly of Isoperla grammatica, ipIsoGram3.1: BlobToolKit Blob plot.
Scaffolds are coloured by phylum. Circles are sized in proportion to scaffold length. Histograms show the distribution of scaffold length sum along each axis. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/ipIsoGram3.1/dataset/CAMDTW01/blob.
Figure 4. Genome assembly of Isoperla grammatica, ipIsoGram3.1: cumulative sequence.
BlobToolKit cumulative sequence plot. The grey line shows cumulative length for all scaffolds. Coloured lines show cumulative lengths of scaffolds assigned to each phylum using the buscogenes taxrule. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/ipIsoGram3.1/dataset/CAMDTW01/cumulative.
Table 3. Chromosomal pseudomolecules in the genome assembly of Isoperla grammatica, ipIsoGram3.
| INSDC accession | Chromosome | Size (Mb) | GC% |
|---|---|---|---|
| OX246737.1 | 1 | 137.5 | 39.3 |
| OX246745.1 | X1 | 45.93 | 39.7 |
| OX246738.1 | 2 | 115.38 | 39 |
| OX246739.1 | 3 | 75.84 | 39.6 |
| OX246746.1 | X2 | 45.27 | 38.6 |
| OX246740.1 | 4 | 60.58 | 39.5 |
| OX246741.1 | 5 | 56.76 | 39.9 |
| OX246742.1 | 6 | 48.65 | 41 |
| OX246743.1 | 7 | 48.25 | 41 |
| OX246744.1 | 8 | 46.81 | 41.3 |
| OX246747.1 | 9 | 41.61 | 41.5 |
| OX246748.1 | 10 | 41.44 | 40.8 |
| OX246749.1 | 11 | 40.56 | 42.4 |
| OX246750.1 | 12 | 26.74 | 39.9 |
| OX246751.1 | MT | 0.02 | 31.3 |
| - | unplaced | 43.26 | 40 |
The mitochondrial genome was also assembled (length 16.16 kb, OX246751.1). This sequence is included as a contig in the multifasta file of the genome submission and as a standalone record.
The primary assembly has a BUSCO v5.3.2 ( Manni et al., 2021) completeness of 99.3% (single 96.6%, duplicated 2.7%), using the insecta_odb10 reference set. The combined primary and alternate assemblies achieve an estimated QV of 55.8. The k-mer completeness is 68.59% for the primary assembly, 56.02% for the alternate haplotype, and 98.25% for the combined assemblies.
Methods
Sample acquisition and nucleic acid extraction
Two Isoperla grammatica specimens (specimen ID NHMUK014360609, ToLID ipIsoGram3 and specimen ID NHMUK014360651, ToLID ipIsoGram4) were collected from River Test, Great Bridge, Hampshire (latitude 51.00, longitude –1.50) on 19 March 2019. The specimens were taken from freshwater by Emma McSwan (Environment Agency) using a kick-net. The specimen was also identified by Emma McSwan and snap-frozen in a dry shipper at the Natural History Museum, London. A specimen used for RNA sequencing (specimen ID NHMUK014361594, ToLID ipIsoGram7) was collected by Caleala Clifford (Natural Resources Wales) from River Taff Fawr, Garwnant, UK (latitude 51.81, longitude –-3.44) on 19 March 2019, and snap-frozen in a dry shipper at the Natural History Museum, London.
DNA was extracted at the Tree of Life laboratory, Wellcome Sanger Institute (WSI). The ipIsoGram3 specimen was weighed and dissected on dry ice. The tissue was cryogenically disrupted to a fine powder using a Covaris cryoPREP Automated Dry Pulveriser, receiving multiple impacts. High molecular weight (HMW) DNA was extracted using the Qiagen MagAttract HMW DNA extraction kit. HMW DNA was sheared into an average fragment size of 12–20 kb in a Megaruptor 3 system with speed setting 30. Sheared DNA was purified by solid-phase reversible immobilisation using AMPure PB beads with a 1.8X ratio of beads to sample to remove the shorter fragments and concentrate the DNA sample. The concentration of the sheared and purified DNA was assessed using a Nanodrop spectrophotometer and Qubit Fluorometer and 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 ipIsoGram7 in the Tree of Life Laboratory at the WSI using TRIzol, according to the manufacturer’s instructions. RNA was then eluted in 50 μl RNAse-free water and its concentration assessed using a Nanodrop spectrophotometer and Qubit Fluorometer using the Qubit RNA Broad-Range (BR) Assay kit. Analysis of the integrity of the RNA was done using Agilent RNA 6000 Pico Kit and Eukaryotic Total RNA assay.
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 II (HiFi) and Illumina HiSeq 4000 (RNA-Seq). Hi-C data were also generated from ipIsoGram4 using the Arima v2 kit and sequenced on the NovaSeq 6000 instrument.
Genome assembly and curation
Prior to assembly of the PacBio HiFi reads, a database of k-mer counts ( k = 31) was generated from the filtered reads using FastK. GenomeScope2 ( Ranallo-Benavidez et al., 2020) was used to analyse the k-mer frequency distributions, providing estimates of genome size, heterozygosity, and repeat content.
Assembly of PacBio HiFi reads was carried out with Hifiasm ( Cheng et al., 2021) and haplotypic duplication was identified and removed with purge_dups ( Guan et al., 2020). The Hi-C reads ( Rao et al., 2014) were mapped to the primary contigs using bwa-mem2 ( Vasimuddin et al., 2019) and then scaffolded using YaHS ( Zhou et al., 2023). The assembly was checked for contamination and corrected as described previously ( Howe et al., 2021). Manual curation was performed using HiGlass ( Kerpedjiev et al., 2018) and PretextView ( Harry, 2022). The curation process is documented at https://gitlab.com/wtsi-grit/rapid-curation. PretextSnapshot was used to generate a Hi-C contact map of the final assembly.
The mitochondrial genome was assembled using MitoHiFi ( Uliano-Silva et al., 2023), which performed annotation using MitoFinder ( Allio et al., 2020).
Assembly quality assessment
The Merqury.FK tool (Rhie et al., 2020) was run in a Singularity container ( Kurtzer et al., 2017) to evaluate k-mer completeness and assembly quality for the primary and alternate haplotypes using the k-mer databases ( k = 31) computed prior to genome assembly. The analysis outputs included assembly QV scores and completeness statistics.
The genome was analysed within the BlobToolKit environment ( Challis et al., 2020) and BUSCO scores ( Manni et al., 2021) were calculated. 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).
Table 4 contains a list of relevant software tool versions and sources.
Table 4. Software tools and versions used.
Ethics and compliance issues
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. 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. All efforts are undertaken to minimise the suffering of animals used for sequencing. 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.
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: 1 approved, 3 approved with reservations]
Data availability
European Nucleotide Archive: Isoperla grammatica (common yellow sally). Accession number PRJEB53729; https://identifiers.org/ena.embl/PRJEB53729.
The genome sequence is released openly for reuse by the Wellcome Sanger Institute. The Isoperla grammatica 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. The genome will be annotated using available RNA-Seq data and presented through the Ensembl pipeline at the European Bioinformatics Institute. Raw data and assembly accession identifiers are reported in Table 1 and Table 2.
Production code used in genome assembly at the WSI Tree of Life is available at https://github.com/sanger-tol. And 4 are
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/552050.
Author information
Members of the Natural History Museum Genome Acquisition Lab are listed here: https://doi.org/10.5281/zenodo.4790043.
Members of the Darwin Tree of Life Barcoding collective are listed here: https://doi.org/10.5281/zenodo.4893703.
Members of the Wellcome Sanger Institute Tree of Life programme are listed here: https://doi.org/10.5281/zenodo.4783585.
Members of Wellcome Sanger Institute Scientific Operations: DNA Pipelines collective are listed here: https://doi.org/10.5281/zenodo.4790455.
Members of the Tree of Life Core Informatics collective are listed here: https://doi.org/10.5281/zenodo.5013541.
Members of the Darwin Tree of Life Consortium are listed here: https://doi.org/10.5281/zenodo.4783558.
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