The complete genome sequences of two species of seventeen-year cicadas: <i>Magicicada septendecim</i> and <i>Magicicada septendecula</i>

Harold B. White; Stacy Pirro

doi:10.12688/f1000research.27309.1

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Data Note

The complete genome sequences of two species of seventeen-year cicadas: Magicicada septendecim and Magicicada septendecula

[version 1; peer review: 2 approved with reservations]

Harold B. White¹, Stacy Pirro ²

PUBLISHED 16 Mar 2021

Author details Author details

¹ Department of Chemistry and Biochemistry, University of Delaware, Delaware, USA
² Department Biodiversity, Iridian Genomes, Bethesda, MD, 20817, USA

Harold B. White
Roles: Resources

Stacy Pirro
Roles: Data Curation, Investigation, Resources

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This article is included in the Genomics and Genetics gateway.

Abstract

The genus Magicicada (Hemiptera: Cicadidae) includes the periodical cicadas of Eastern North America. Spending the majority of their long lives underground, the adult cicadas emerge every 13 or 17 years to spend 4-6 weeks as adult to mate. We present the whole genome sequences of two species of 17-year cicadas, Magicicada septendecim and Magicicada septendecula. The reads were assembled by a de novo method followed by alignments to related species. Annotation was performed by GeneMark-ES. The raw and assembled data is available via NCBI Short Read Archive and Assembly databases.

Keywords

Genome, assembly, arthropoda, insecta, hemiptera

Corresponding author: Stacy Pirro

Competing interests: No competing interests were disclosed.

Grant information: This work was supported by Iridian Genomes (IRGEN-38085).

Copyright: © 2021 White HB and Pirro S. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: White HB and Pirro S. The complete genome sequences of two species of seventeen-year cicadas: Magicicada septendecim and Magicicada septendecula [version 1; peer review: 2 approved with reservations]. F1000Research 2021, 10:215 (https://doi.org/10.12688/f1000research.27309.1) First published: 16 Mar 2021, 10:215 (https://doi.org/10.12688/f1000research.27309.1) Latest published: 16 Mar 2021, 10:215 (https://doi.org/10.12688/f1000research.27309.1)

Editorial note

Editorial note (3rd July 2023): Peer review activity for this article has been discontinued following discussion and agreement between the authors and F1000 Editorial Team. As per our policies on discontinuing peer review, the article is now considered equivalent to a preprint and the authors have chosen to submit the manuscript to a journal for peer review and publication elsewhere.

Introduction

Periodical cicadas in North America spend 13 or 17 years in the larval stage underground, and emerge in very large numbers for 4–6 weeks to mate and lay eggs. This strategy, known as “predator satiation” is intended to ensure that after all predators have eaten as much as possible, most cicadas will survive. (Williams & Simon, 1995). The emergence occurring in prime-numbered years is thought to be a mechanism to avoid competition between species for egg-laying sites and accidental cross-species mating as the emergence of the 13- and 17-year cicadas would only coincide once every 221 years (Tanaka et al., 2009).

The length of time spent in the larval stage is thought to be dependent on a single gene, although this has not yet been demonstrated at the genomic level (Cox & Carlton, 1991).

Complete genome sequences for these two species will assist with studies on taxonomy, longevity, and the timing of long-term larval development.

Methods

Wild caught specimens of Magicicada septendecim and Magicicada septendecula from a small premature emergence of Brood X (2017) collected in Newark, Delaware, USA were used in this study. DNA extraction was performed using the Qiagen DNAeasy genomic extraction kit for tissue, using the standard process. A paired-end sequencing library was constructed using the Illumina TruSeq kit, according to the manufacturer’s instructions. The library was sequenced on an Illumina Hi-Seq platform in paired-end, 2 × 150bp format.

The resulting fastq files were trimmed of adapter/primer sequence and low-quality regions with Trimmomatic v0.33 (Bolger et al., 2014). The trimmed sequence was assembled by SPAdes v2.5 (Bankevich et al., 2012) followed by a finishing step using RagTag v1.0.0 (Alonge, 2020) to make additional contig joins based on conserved regions in related insect species: Rhopalosiphum maidis (GCA_003676215), Euschistus heros (GCA_003667255), and Aphis glycines (GCA_009928515). Default parameters were used for all assembly steps.

Annotation was performed using GeneMark-ES v2.0 (Lomsadze et al., 2005). Annotation was performed fully de novo without a curated training set and using default parameters.

Results

The genome assembly for Magicicada septendecim yielded a total sequence length of 1,579,033,894 with an N50 value of 983 kb and 27,124 gene models.

The genome assembly of Magicicada septendecula yielded 1,585,977,997 with an N50 value of 281 kb and 28,651 gene models.

Data availability

Genome data available from NCBI’s Short Read Archive (SRA):

Magicicada septendecim, Accession number SRR6782667: https://www.ncbi.nlm.nih.gov/sra/SRR6782667

Magicicada septendecula, Accession number SRR6792649: https://www.ncbi.nlm.nih.gov/sra/SRR6792649

Assembled genomes available from NCBI’s Assembly database:

Magicicada septendecim, Accession number GCA_011326945: https://www.ncbi.nlm.nih.gov/assembly/GCA_011326945.1/

Magicicada septendecula, Accession number GCA_011763675: https://www.ncbi.nlm.nih.gov/assembly/GCA_011763675.1/

Author information

Harold B. White is now retired from Department of Chemistry and Biochemistry, University of Delaware.

Faculty Opinions recommended

References

Alonge M: Ragtag: Reference-guided genome assembly correction and scaffolding. GitHub archive. 2020.
Bankevich A, Nurk S, Antipov D, et al.: SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J Comput Biol. 2012; 19(5): 455–477. PubMed Abstract | Publisher Full Text | Free Full Text
Bolger AM, Lohse M, Usadel B: Trimmomatic: A flexible trimmer for Illumina Sequence Data. Bioinformatics. 2014; 30(15): 2114–20. PubMed Abstract | Publisher Full Text | Free Full Text
Cox RT, Carlton CE: Evidence of genetic dominance of the 13-year life cycle in periodical cicadas (Homoptera: Cicadidae: Magicicada spp.). Am Midl Nat. 1991; 125(1): 63–74. Publisher Full Text
Lomsadze A, Ter-Hovhannisyan V, Chernoff YO, et al.: Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res. 2005; 33(20): 6494–6506. PubMed Abstract | Publisher Full Text | Free Full Text
Tanaka Y, Yoshimura J, Simon C, et al.: Allee effect in the selection for prime-numbered cycles in periodical cicadas. Proc Natl Acad Sci U S A. 2009; 106(22): 8975–8979. PubMed Abstract | Publisher Full Text | Free Full Text
Williams KS, Simon C: The ecology, behavior, and evolution of periodical cicadas. Annu Rev Entomol. 1995; 40(1): 269–295. Publisher Full Text

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Version 1

VERSION 1 PUBLISHED 16 Mar 2021

Author details Author details

¹ Department of Chemistry and Biochemistry, University of Delaware, Delaware, USA
² Department Biodiversity, Iridian Genomes, Bethesda, MD, 20817, USA

Harold B. White
Roles: Resources

Stacy Pirro
Roles: Data Curation, Investigation, Resources

Competing interests

No competing interests were disclosed.

Grant information

This work was supported by Iridian Genomes (IRGEN-38085).

Article Versions (1)

version 1

Published: 16 Mar 2021, 10:215

https://doi.org/10.12688/f1000research.27309.1

Copyright

© 2021 White HB and Pirro S. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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White HB and Pirro S. The complete genome sequences of two species of seventeen-year cicadas: Magicicada septendecim and Magicicada septendecula [version 1; peer review: 2 approved with reservations]. F1000Research 2021, 10:215 (https://doi.org/10.12688/f1000research.27309.1)

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PUBLISHED 16 Mar 2021

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Reviewer Report 12 May 2021

Shuai Zhan, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

Approved with Reservations

https://doi.org/10.5256/f1000research.30176.r83461

The fascinating life cycle of Periodical cicadas attracts public and scientific interests from around the globe. In this Data note, the authors report the genome references of two such cicadas species, Magicicada septendecim and M. septendecula. The available genomes would no ... Continue reading

The fascinating life cycle of Periodical cicadas attracts public and scientific interests from around the globe. In this Data note, the authors report the genome references of two such cicadas species, Magicicada septendecim and M. septendecula. The available genomes would no doubt benefit the community in various areas. However, it is difficult to judge the actual quality of the yielded genomes, due to the incomplete method description and lacking of necessary quality evaluation. I think this is important for the community to determine whether the resource is reliable and to what extent.

Here are some specific concerns:

It is unclear to me how the genome is generated, which is critical to assess whether the assembling approach is reasonable. The authors should provide key information such as how many libraries being generated for a single species and the insert size information for the library(s). It seems that only one paired-end library was constructed, thus I cannot imagine that how a single library would yield genome assemblies for two species and how the assembly could reach a scaffold level with the N50 size as long as hundreds of Kb.
The authors claimed that the assembling approach includes the alignment step to related species, such as some aphids. This is uncommon for de novo assembling a genome reference, particularly for an insect species, given the high level of divergence between families and species.
The current note only presents the genome size and N50 size, but lacks of most other key properties to assess the quality of a genome assembly, such as the expected genome size, the completeness, the redundancy ratio, the GC ratio, the potential contamination ratio, etc.
The current gene prediction method is unsatisfying and could be substantially improved by applying an integrated approach. Using GeneMark alone is uncommon for annotating a large eukaryotic genome. Instead, this gene predictor is more common to be used as partial ab initio evidence of a comprehensive gene annotation, which is usually achieved by combing transcriptome, homology of related species, and several lines of ab initio signatures (e.g. GeneMark and other predictors).
I'm not sure whether 'data note' has a word limit or some special requirements, but the current form of the manuscript is obviously too dense. To allow replication by other researchers, the current method section should be provided with necessary details, such as the parameters for each software.

Is the rationale for creating the dataset(s) clearly described?

Partly
Are the protocols appropriate and is the work technically sound?

Partly
Are sufficient details of methods and materials provided to allow replication by others?

No
Are the datasets clearly presented in a useable and accessible format?

Yes

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Insect genomics

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

CITE

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26

Reviewer Report 12 Apr 2021

Hu Li, Department of Entomology and MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, China

Approved with Reservations

https://doi.org/10.5256/f1000research.30176.r81859

The authors presented the genome assembly of Magicicada septendecim and Magicicada septendecula using Illumina platform, which is of great help to the Magicicada evolution study. Using the RagTag method to correct, orient and scaffold the assembled sequence is a novel ... Continue reading

The authors presented the genome assembly of Magicicada septendecim and Magicicada septendecula using Illumina platform, which is of great help to the Magicicada evolution study. Using the RagTag method to correct, orient and scaffold the assembled sequence is a novel idea for the short reads assembly. However, there are still some limitations which might be improved.

In this manuscript, detailed information of sequencing samples counts, male or female, were not given. It also lacks the amount of data sequenced by Illumina platform, genome assembly and annotation completeness assessed by BUSCO, and repetitive sequence annotation.

Additionally, one of my major concerns is that, we usually use a long reads platform such as PacBio or ONT to sequence the genome; could short sequence be assembled completely? Although de novo method by using SPAdes and RagTag software in this study works well to assemble short sequences, when aligned to related species, contigs lower than 1 kb were filtered and some genome sequences might be lost.

Is the rationale for creating the dataset(s) clearly described?

Yes
Are the protocols appropriate and is the work technically sound?

Yes
Are sufficient details of methods and materials provided to allow replication by others?

Partly
Are the datasets clearly presented in a useable and accessible format?

Yes

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: comparative genomics, phylogenomics, population genomics

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

CITE

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Version 1

VERSION 1 PUBLISHED 16 Mar 2021

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Version 1 16 Mar 21	read	read

Hu Li, China Agricultural University, Beijing, China
Shuai Zhan, Chinese Academy of Sciences, Shanghai, China

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Reviewer Report

14 Views

12 May 2021 | for Version 1

Shuai Zhan, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

14 Views Cite this report Responses(0)

Approved With Reservations

The fascinating life cycle of Periodical cicadas attracts public and scientific interests from around the globe. In this Data note, the authors report the genome references of two such cicadas species, Magicicada septendecim and M. septendecula. The available genomes would no doubt benefit the community in various areas. However, it is difficult to judge the actual quality of the yielded genomes, due to the incomplete method description and lacking of necessary quality evaluation. I think this is important for the community to determine whether the resource is reliable and to what extent.

Here are some specific concerns:

It is unclear to me how the genome is generated, which is critical to assess whether the assembling approach is reasonable. The authors should provide key information such as how many libraries being generated for a single species and the insert size information for the library(s). It seems that only one paired-end library was constructed, thus I cannot imagine that how a single library would yield genome assemblies for two species and how the assembly could reach a scaffold level with the N50 size as long as hundreds of Kb.
The authors claimed that the assembling approach includes the alignment step to related species, such as some aphids. This is uncommon for de novo assembling a genome reference, particularly for an insect species, given the high level of divergence between families and species.
The current note only presents the genome size and N50 size, but lacks of most other key properties to assess the quality of a genome assembly, such as the expected genome size, the completeness, the redundancy ratio, the GC ratio, the potential contamination ratio, etc.
The current gene prediction method is unsatisfying and could be substantially improved by applying an integrated approach. Using GeneMark alone is uncommon for annotating a large eukaryotic genome. Instead, this gene predictor is more common to be used as partial ab initio evidence of a comprehensive gene annotation, which is usually achieved by combing transcriptome, homology of related species, and several lines of ab initio signatures (e.g. GeneMark and other predictors).
I'm not sure whether 'data note' has a word limit or some special requirements, but the current form of the manuscript is obviously too dense. To allow replication by other researchers, the current method section should be provided with necessary details, such as the parameters for each software.

Is the rationale for creating the dataset(s) clearly described?

Partly
Are the protocols appropriate and is the work technically sound?

Partly
Are sufficient details of methods and materials provided to allow replication by others?

No
Are the datasets clearly presented in a useable and accessible format?

Yes

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Insect genomics

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

Respond to this report

Responses (0)

Back to all reports

Reviewer Report

26 Views

12 Apr 2021 | for Version 1

Hu Li, Department of Entomology and MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, China

26 Views Cite this report Responses(0)

Approved With Reservations

The authors presented the genome assembly of Magicicada septendecim and Magicicada septendecula using Illumina platform, which is of great help to the Magicicada evolution study. Using the RagTag method to correct, orient and scaffold the assembled sequence is a novel idea for the short reads assembly. However, there are still some limitations which might be improved.

In this manuscript, detailed information of sequencing samples counts, male or female, were not given. It also lacks the amount of data sequenced by Illumina platform, genome assembly and annotation completeness assessed by BUSCO, and repetitive sequence annotation.

Additionally, one of my major concerns is that, we usually use a long reads platform such as PacBio or ONT to sequence the genome; could short sequence be assembled completely? Although de novo method by using SPAdes and RagTag software in this study works well to assemble short sequences, when aligned to related species, contigs lower than 1 kb were filtered and some genome sequences might be lost.

Is the rationale for creating the dataset(s) clearly described?

Yes
Are the protocols appropriate and is the work technically sound?

Yes
Are sufficient details of methods and materials provided to allow replication by others?

Partly
Are the datasets clearly presented in a useable and accessible format?

Yes

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

comparative genomics, phylogenomics, population genomics

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

Respond to this report

Responses (0)

[1] Alonge M: Ragtag: Reference-guided genome assembly correction and scaffolding. GitHub archive. 2020.

[2] Bankevich A, Nurk S, Antipov D, et al.: SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J Comput Biol. 2012; 19(5): 455–477. PubMed Abstract | Publisher Full Text | Free Full Text

[3] Bolger AM, Lohse M, Usadel B: Trimmomatic: A flexible trimmer for Illumina Sequence Data. Bioinformatics. 2014; 30(15): 2114–20. PubMed Abstract | Publisher Full Text | Free Full Text

[4] Cox RT, Carlton CE: Evidence of genetic dominance of the 13-year life cycle in periodical cicadas (Homoptera: Cicadidae: Magicicada spp.). Am Midl Nat. 1991; 125(1): 63–74. Publisher Full Text

[5] Lomsadze A, Ter-Hovhannisyan V, Chernoff YO, et al.: Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res. 2005; 33(20): 6494–6506. PubMed Abstract | Publisher Full Text | Free Full Text

[6] Tanaka Y, Yoshimura J, Simon C, et al.: Allee effect in the selection for prime-numbered cycles in periodical cicadas. Proc Natl Acad Sci U S A. 2009; 106(22): 8975–8979. PubMed Abstract | Publisher Full Text | Free Full Text

[7] Williams KS, Simon C: The ecology, behavior, and evolution of periodical cicadas. Annu Rev Entomol. 1995; 40(1): 269–295. Publisher Full Text

The complete genome sequences of two species of seventeen-year cicadas: Magicicada septendecim and Magicicada septendecula

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