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. 2022 Aug 6;9:482. doi: 10.1038/s41597-022-01601-1

Chromosome-level genome assembly of largemouth bass (Micropterus salmoides) using PacBio and Hi-C technologies

Kuo He 1,#, Liulan Zhao 1,#, Zihao Yuan 2,3,#, Adelino Canario 4, Qiao Liu 1, Siyi Chen 1, Jiazhong Guo 1, Wei Luo 1, Haoxiao Yan 1, Dongmei Zhang 1, Lisen Li 4, Song Yang 1,✉
PMCID: PMC9357066  PMID: 35933561

Abstract

The largemouth bass (Micropterus salmoides) has become a cosmopolitan species due to its widespread introduction as game or domesticated fish. Here a high-quality chromosome-level reference genome of M. salmoides was produced by combining Illumina paired-end sequencing, PacBio single molecule sequencing technique (SMRT) and High-through chromosome conformation capture (Hi-C) technologies. Ultimately, the genome was assembled into 844.88 Mb with a contig N50 of 15.68 Mb and scaffold N50 length of 35.77 Mb. About 99.9% assembly genome sequences (844.00 Mb) could be anchored to 23 chromosomes, and 98.03% assembly genome sequences could be ordered and directed. The genome contained 38.19% repeat sequences and 2693 noncoding RNAs. A total of 26,370 protein-coding genes from 3415 gene families were predicted, of which 97.69% were functionally annotated. The high-quality genome assembly will be a fundamental resource to study and understand how M. salmoides adapt to novel and changing environments around the world, and also be expected to contribute to the genetic breeding and other research.

Subject terms: Genome, Agricultural genetics

Measurement(s) genome assemble
Technology Type(s) Illumina paired-end sequencing, PacBio single molecule sequencing technique (SMRT) and High-through chromosome conformation capture (Hi-C) technologies
Sample Characteristic - Organism Micropterus floridanus
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Background & Summary

The largemouth bass, Micropterus salmoides (Perciformes, Centrarchidae), is a native of North America introduced in other parts of the world, including the Iberian Peninsula, Italy, Mexico and China, either as a game or farmed fish1–3. It is now one of the top ten most common aquatic species in every continent, except Antarctica4,5, and has been listed among the top 100 invasive species6, with temperature and hydrologic changes as main predictors of its distribution1,7. Although its main habitat is freshwater lakes and rivers, it colonizes brackish waters, such as in the Gulf of Mexico and the Atlantic coasts of North America8. Largemouth bass has been introduced into China from the US in 19832, and it has become one of the main aquaculture species in China for its fast growth2,9.

The whole genome information is the basis for studying the nature of organisms, including advantages during biological invasions and adaptation to extreme environments such as hypoxia10–12, climate change13,14, temperature15,16 and salinity17,18. With the development of sequencing technology, genome research has been studied more deeply and accurately19. More and more fish genomes have been decoded, such as yellow perch (Perca flavescens)20, golden pompano (Trachinotus ovatus)21 and dark sleeper (Odontobutis potamophila)22, etc. Moreover, the Nile tilapia and Pacific bluefin tuna genome have been re-sequenced to improve the genome assembly and fill the previously missed gaps23,24. These genome studies have greatly elevated our understanding about genetics, environmental adaptive selection, and evolutionary history of the target species. These more detailed genomic data can also facilitate studies on nutritional requirements, disease control and prevention, and to improve traits of economic interest25–27.

In the present study, a novel high-quality chromosome-level genome assembly of largemouth bass was generated by single-molecule real-time sequencing combined with Illumina paired-end sequencing and Hi-C (Fig. 1). The final assembled genome size of M. salmoides was 844.88 Mb with an N50 contig length of 15.30 Mb and scaffold N50 length of 35.77 Mb. A total of 844.00 Mb assembled genome sequences were anchored on 23 chromosomes. The genome contained 38.19% repeat sequences and 2693 noncoding RNAs. A total of 26,370 protein-coding genes from 3415 gene families were predicted, of which 97.69% were functionally annotated.

Fig. 1.

Fig. 1

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The pipelines overview of the largemouth bass chromosome-level genome assembly. Chrs: chromosomes.

Methods

Ethics statement

All experiments were performed according to the Guidelines for the Care and Use of Laboratory Animals in China. The sampled fish in this study was approved by the Institutional Animal Care and Use Committee (IACUC) of the College of Animal Science and Technology of Sichuan Agricultural University, Sichuan, China, under permit No. DKY-YS13287.

Sequencing libraries

Tissues from a two-year-old adult female largemouth bass (body weight 1487 g, length 36 cm), obtained from an aquaculture farm of Chongzhou, Sichuan province, China, were used to construct genomic DNA sequencing libraries (muscle) and transcriptome sequencing libraries (liver, brain, muscle, heart, kidney, gill, and gonad). All the tissues were stored in liquid nitrogen until use.

For short-read sequencing, genomic DNA was extracted from 500 mg of muscle using cetyl trimethylammonium bromide (CTAB) before chloroform purification. The genomic DNA was sonicated to a fragment size of 350 bp and the paired-end genomic library was prepared following the Illumina standard protocol, including terminal repair, polyA and adaptor addition, target fragment selection and PCR processes (Illumina, San Diego, CA, USA). The resulted library was quality checked using Agilent Bioanalyser 2100 and qPCR, and sequenced on an Illumina NovaSeq 6000 sequencing platform with paired-end 150 bp read layout.

For long-read sequencing, genomic DNA (~8 µg) was sheared into a large fragment by g-TUBE (Covaris), purified and recovered by AMpure PB magnetic beads, and used to construct single-molecule real-time bell (SMRTbell) sequencing libraries by the SMRTbell Template Prep Kit 2.0 (PacBio)28. The end-repaired fragments were size-selected using the Blue Pippin Size-Selection System (Sage Science, MA, USA), and damage-repaired using the SMRTbell Damage Repair Kit (PacBio). Then the products were combined polymerase using the PacBio DNA/Polymerase Kit before sequenced on the PacBio Sequel platform.

The full-length transcriptome was used to generate RNA data for gene prediction from a sample pool consisting of muscle, liver, gonad, kidney, gut, blood, and gills. Total RNA was extracted by TRIzol extraction reagent (Invitrogen, USA) according to the manufacturer’s protocol. RNA purity was checked using the NanoPhotometer spectrophotometer (IMPLEN, CA, USA). RNA concentration was measured using Qubit RNA Assay Kit in Qubit 2.0 Flurometer (Life Technologies, CA, USA). Then, these tissues RNA were equally mixed to product cDNA using the SMARTer PCR cDNA Synthesis Kit and sequencing by one SMRT flow cell on the PacBio Sequel platform. Raw reads were processed into error corrected reads of insert (ROIs) using Iso-seq pipeline with minFullPass = 0 and minPredictedAccuracy = 0.90. Next, full-length, non-chemiric (FLNC) transcripts were determined by searching for the polyA tail signal and the 5′ and 3′ cDNA primers in ROIs. Full-length consensus sequences obtained from ICE (Iterative Clustering for Error Correction) were polished using Quiver. Finally, Full-length transcriptome sequencing yielded 20 Gb of clean data, including 26,369 high-quality consensus isoforms sequences with an average length of 2,895 bp.

Genome survey and assembly

The size, heterozygosity, and repetitive sequences in the M. salmoides genome were estimated by the analysis of k-mer frequency distribution of Illumina paired-end reads using the kmer_freq_stat script (Biomarker Technologies, Beijing, China), based on the formula G = (N k-mer - Nerror_k-mer)/D (where G: genome size; N k-mer: the number of k-mers; Nerror_k-mer: the number of depth 1 k-mers; D: the k-mer depth). After removing the k-mers with abnormal depth, a total of 49.16 M k-mers were obtained with a k-mers peak at a depth of 56 (Fig. 2). A total of 58.51 Gb high-quality filtered data was generated from the Illumina short read DNA library, with 66.94 × genome coverage, a Q20 of 96.63% and a Q30 of 91.36% (Table 1). The genome size was estimated at 874.14 Mb, with 0.12% heterozygosity, 30.03% repetitive sequences, and 40.88% GC content (Table 1).

Fig. 2.

Fig. 2

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K‐mer distribution of M. salmoides genome sequencing reads. The K-mers distribution (K = 19) was constructed using 350 bp library data. A total of 49,157,214,151 K-mers were used for genomic length estimation after the removal of the K-mers with abnormal depth. The peak 19‐mer depth was 56, and the genome size was calculated as 49,157,214,151/56 = 874.14 Mb.

Table 1.

M. salmoides genome sequencing statistics.

Library Sequencing platform Clean data (Gb) Depth (×) Contig N50 (Mb) GC content (%) Q20 (%) Q30 (%) Genome size (Mb)
Short reads Illumina NovaSeq 6000 58.51 66.94 — 40.88 96.63 91.36 874.14
Long reads PacBio Sequel 94.69 112.07 15.68 40.78 — — 844.88
Hi-C Illumina NovaSeq 6000 77.53 94.06 15.30 40.78 97.59 93.49 844.00
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For long-read sequencing, reads longer than 500 bp generated by the PacBio Sequel platform were collected and a de novo genome was assembled initially using SMARTdenovo29 based on the data corrected by Canu v. 1.530. Subsequently, three rounds of refinement of the de novo genome were performed using Pilon31 by Illumina short read sequencing data. Finally, the long-read SMRTbell library generated a total of 94.69 Gb (112.07 × genome coverage) with a reads N50 of 35.34 kb and an average read length of 24.75 kb. After error correction and assembly, an 844.88 Mb genome was assembled from 265 contigs with a N50 of 15.68 Mb (Table 1).

Hi-C analysis and chromosome assembly

Hi-C libraries were prepared as previously reported32,33. Briefly, muscle tissue cells were fixed with formaldehyde to maintain the 3D structure of DNA in cells and the cells were digested using restriction endonuclease Hind III. Then, biotin-labeled bases were introduced using the DNA terminal repair mechanism. DNA (4 µg) was fragmented by a Covaris S220 focused-ultrasonicator (Gene Company Limited, Hong Kong) and 300–700 bp fragments were recovered. The DNA fragments containing interaction relationships were captured by streptavidin immunomagnetic beads for library construction. Library concentration and insert size were determined using the Qubit 3.0 and LabChip GX platforms (PerkinElmer), respectively. qPCR was used to estimate the effective concentration of the library. High quality Hi-C libraries were sequenced on the Illumina NovaSeq 6000 sequencing platform, and the sequencing data were used for chromosome-level assembly34. The software Burrows-Wheeler Aligner (BWA-MEM v. 0.7.10-r789) was used to align the sequencing pair-end clean reads with the sequence of the assembled genome to obtain the uniquely mapped read pairs35. The uniquely mapped read pairs were processed using HiC-Pro36. The genome contigs, split into 50 kb segments, combined with uniquely matched Hi-C data, were clustered, ordered and directed onto the pseudochromosomes using LACHESIS34 with the following parameters: CLUSTER_MIN_RE_SITES = 30; CLUSTER_MAX_LINK_DENSITY = 2; CLUSTER_NONINFORMATIVE_RATIO = 2; ORDER_MIN_N_RES_IN_TRUN = 68; ORD-ER_MIN_N_RES_I-N_SHREDS = 67. Finally, the chromosome assemblies were cut into 100 kb bins of equal lengths and the interaction signals generated by the valid mapped read pairs between each bin were visualized in a heat map.

In total, 277.88 million read pairs (77.53 Gb clean data; 94.06 × coverage of the genome) were generated from the Hi-C library (Table 1), of which 77.26% were uniquely mapped on the assembled genome. Of the unique mapped read pairs, 60.67% were the valid interaction pairs (130.26 million), which were used for the next Hi-C assembly (Table S1). A total of 844.00 Mb (99.9%) assembled genome sequences were anchored on 23 chromosomes, and the order and direction of 827.39 Mb (98.03%) sequences could be determined. The detailed distribution of each chromosome sequence was shown in Table 2. The heat map of the Hi-C assembly interaction bins is consistent a genome assembly of excellent quality (Fig. 3). Finally, the genome size of M. salmoides was assembled at 844.88 Mb, while contig N50 and scaffold N50 were 15.30 Mb and 35.77 Mb, respectively (Table 1).

Table 2.

The sequence distribution of each chromosome using Hi-C technology.

Group Cluster Num Cluster Len Order Num Order Len
Chr01 5 40,821,207 4 40,732,462
Chr02 15 42,659,052 9 42,039,393
Chr03 7 37,588,897 6 37,343,944
Chr04 13 40,393,715 9 39,732,765
Chr05 15 39,747,164 6 38,411,921
Chr06 10 36,025,099 6 35,600,334
Chr07 9 34,881,373 6 34,516,066
Chr08 2 37,271,896 2 37,271,896
Chr09 5 37,188,422 4 37,114,295
Chr10 4 36,011,566 3 35,768,921
Chr11 11 33,902,165 5 33,113,071
Chr12 15 35,527,541 8 34,268,756
Chr13 5 33,494,735 4 33,265,410
Chr14 11 34,134,741 8 33,564,293
Chr15 24 37,902,394 11 35,937,762
Chr16 9 32,104,916 6 31,675,598
Chr17 7 32,964,910 4 32,674,911
Chr18 26 34,562,858 13 33,055,325
Chr19 31 41,218,652 16 38,871,204
Chr20 6 32,259,510 5 32,214,040
Chr21 3 28,886,792 3 28,886,792
Chr22 18 56,175,891 7 54,208,627
Chr23 15 28,271,698 8 27,127,050
Total (Ratio %) 266 (97.08) 843995194 (99.9) 153 (57.52) 827394836 (98.03)
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Note: Chr01-23 represent 23 chromosomes; Cluster Num: the number of sequences located on a chromosome; Cluster Len: the length of sequence located on a chromosome; Order Num: the number of sequences of the direction can be determined; Order Len: the sequence length of the direction can be determined.

Fig. 3.

Fig. 3

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Hi-C assembly of chromosome interactive heat map. Chr01 - Chr23 are the abbreviations of 23 Chromosome. The abscissa and ordinate represent the order of each bin on the corresponding chromosome group. The colour block illuminates the intensity of interaction from yellow (low) to red (high).

Repeats prediction

The repetitive elements of the M. salmoides genome were identified and annotated using RepeatModeler2 containing RECON37 and RepeatScout38. The derived repetitive sequences were searched against curated libraries and the repetitive DNA element databases Repbase39, REXdb40 and Dfam41. The LTR retrotransposon retriever42 was applied to identify the output from LTRharvest43 and LTR_FINDER44. The results were combined and deduplicated, and the repetitive elements were finalized by RepeatMasker45. About 38.19% M. salmoides genome was repetitive sequences, composed mainly of class II transposable elements (Table 3).

Table 3.

The repeat sequence statistics of assembled genome.

Type Number Length (bp) Rate (%)
Class I: Retroelement 522983 121796357 14.42
  DIRS 20880 6630621 0.78
  LINE 234381 60698831 7.18
  LTR/Caulimovirus 88 7962 0.00
  LTR/Copia 12013 2607825 0.31
  LTR/ERV 47996 6147308 0.73
  LTR/Gypsy 103367 26357115 3.12
  LTR/Ngaro 16775 2880533 0.34
  LTR/Pao 13115 2271034 0.27
  LTR/Unknown 37371 10223745 1.21
  LTR/Viper 61 3732 0.00
  SINE 36936 3967651 0.47
Class II: DNA transposon 1033511 198005683 23.44
  Academ 1422 193616 0.02
  CACTA 77241 10508494 1.24
  Crypton 16505 2182911 0.26
  Dada 7317 1072578 0.13
  Ginger 4624 459506 0.05
  Helitron 24163 10814282 1.28
  IS3EU 3766 495816 0.06
  Kolobok 31541 7047090 0.83
  MITE 33 1774 0.00
  Maverick 6547 1489673 0.18
  Merlin 3162 472124 0.06
  Mutator 6833 746138 0.09
  Novosib 12838 1115265 0.13
  P 15516 3779929 0.45
  PIF-Harbinger 72041 15425212 1.83
  PiggyBac 14753 2257482 0.27
  Sola 7027 701813 0.08
  Stowaway 1 57 0.00
  Tc1-Mariner 115093 29999050 3.55
  Unknown 128215 21996228 2.60
  Zator 1443 282595 0.03
  Zisupton 26754 4017294 0.48
  hAT 456676 82946756 9.82
  Satellite 4604 769122 0.09
Unknown 11211 2133201 0.25
Total 1572309 322704363 38.19
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Note: Type: the type of repetitive sequence (Class I: retrotransposons; Class II: DNA transposon); Number: the number of repetitive sequences; Length: the total length of predicted repetitive sequences; Rate (%): the proportion of repetitive sequences in the total genome.

Genes prediction and annotation

The prediction of the genome gene structure was based on three different strategies: ab initio-based, homolog-based, and unigene-based. Genscan46, Augustus v2.447, GlimmerHMM v3.0.448, GeneID v1.449 and SNAP (version 2006-07-28)50 were used to perform ab initio-based prediction. GeMoMa v1.3.151,52 was used for prediction based on homologous species. Hisat v2.0.453 and Stringtie v1.2.354 were used for assembly based on reference transcripts, and TransDecoder v2.0 and GeneMarkS -t v5.155 were used for gene prediction. PASA v2.0.256 was used to predict unigene sequences based on unreferenced assembly of full-length transcriptome data. Finally, EVM v1.1.157 was used to integrate the prediction results obtained by the above three methods, and PASA v2.0.2 was used to modify the final gene models. A total of 26,370 protein-coding genes were predicted by integrating the prediction of ab initio, homology-based and RNA-seq strategies (Table S2), with average gene length of 14,483 bp, exon length of 2,601 bp, coding sequence of 1,724 bp and intron length of 11,882 bp (Table 4). Finally, 25,760 genes (97.69% of the total) were successfully annotated GO, KEGG, KOG, TrEMBL, and NR database (Table S3).

Table 4.

The basic information statistics of assembled genome.

Item Count
Gene Number 26,370
Gene Length (bp) 381,932,021
Average Gene Length (bp) 14,483.58
Exon Length (bp) 68,599,926
Average Exon Length (bp) 2,601.44
Exon Number 260,466
Average Exon Number 9.88
CDS Length (bp) 45,485,238
Average CDS Length (bp) 1,724.89
CDS Number 253,748
Average CDS Number 9.62
Intron Length (bp) 313,332,095
Average Intron Length (bp) 11,882.14
Intron Number 234,096
Average Intron Number 8.88
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Blastn searches using the Rfam database58, as input against the M. salmoides genome was used to identify microRNA and rRNA and tRNAscan-SE59 was used to identify tRNA. Non-coding RNAs were predicted to be 2,639, including 633 microRNAs (miRNA) of 84 families, 230 rRNA genes of 4 families and 1,830 tRNA genes of 25 families (Table S4). Pseudogenes were predicted in the following way. The predicted protein sequences were used to search for homologous gene sequences (putative genes) through BLAT alignment60. Then GeneWise61 was used to search for immature termination codons and code-shifting mutations in the gene sequences to obtain pseudogenes. In total, 986 pseudogenes were identified with a total length of 5,885,501 bp and an average length of 5,969 bp (Table S4).

Data Records

The sequencing data (Full-length transcriptome, Hi-C, Illumina and PacBio) have been deposited in SRA (Sequence Read Archive) database as SRR1288657562, SRR1288657663, SRR1288657764, and SRR1288657865. The assembly genome data was deposited in GenBank66. The assembly genome data, gene CDS and Exon data and functional annotations were also stored in Figshare67.

Technical Validation

The assembly was evaluated using three criteria: the mapping of Illumina reads, core gene integrity, and BUSCO assessment. The Benchmarking Universal Single Copy Orthologs were searched in CEGMA v2.568 and BUSCO v 3.069 to evaluate the conserved core genes in the genome. The Illumina reads fully (99.54%) mapped to the assembled genome, including 97.78% of paired-end reads. A total of 445 out of in 458 conserved eukaryotic core genes from the CEGMA database were found in the assembled genome (Table S5). Finally, 97.49% of the complete BUSCOs were included in the assembled genome (Table S5). In summary, this is a high-quality de novo assembly reference genome.

Supplementary information

SupplementaryTables (27.1KB, docx)

Author contributions

Song Yang managed the grants, supervised the laboratory work, and led the design of this study. Kuo He, Liulan Zhao and Zihao Yuan performed bioinformatics and also drafted the manuscript. Adelino Canario, Qiao Liu, Siyi Chen, Jiazhong Guo, Wei Luo, and Lisen Li revised the manuscript. Dongmei Zhang, Haoxiao Yan participated in the tissue sampling. All authors read and approved the final manuscript.

Code availability

All commands and pipelines used in data processing were executed according to the manual and protocols of the corresponding bioinformatics software.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

These authors contributed equally: Kuo He, Liulan Zhao, Zihao Yuan.

Supplementary information

The online version contains supplementary material available at 10.1038/s41597-022-01601-1.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Citations

  1. 2021. NCBI Sequence Read Archive. SRR12886575
  2. 2021. NCBI Sequence Read Archive. SRR12886576
  3. 2021. NCBI Sequence Read Archive. SRR12886577
  4. 2021. NCBI Sequence Read Archive. SRR12886578
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Supplementary Materials

SupplementaryTables (27.1KB, docx)

Data Availability Statement

All commands and pipelines used in data processing were executed according to the manual and protocols of the corresponding bioinformatics software.

Articles from Scientific Data are provided here courtesy of Nature Publishing Group

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