Skip to main content
NCBI home page
Biodiversity Data Journal logoLink to Biodiversity Data Journal
. 2022 Oct 18;10:e94051. doi: 10.3897/BDJ.10.e94051

The complete mitochondrial genome of the Antarctic fairy shrimp Branchinectagaini Daday, 1910 (Branchiopoda, Anostraca, Branchinectidae)

Euna Jo 1,2, Jin-Hyoung Kim 1,3, Young Wook Ko 1, Sanghee Kim 1, Seunghyun Kang 1,✉
PMCID: PMC9836622  PMID: 36761499

Abstract

The complete mitochondrial genome of Antarctic fairy shrimp Branchinectagaini Daday, 1910 was sequenced, assembled and annotated using next-generation sequencing technology. The mitogenome of B.gaini is circular at 15,536 bp in length, consisting of 13 protein-coding genes, 23 tRNAs, two rRNAs and two major non-coding regions. In particular, there are two tRNAGly genes and one non-coding region between these two tRNAGly genes. A phylogenetic tree was constructed using concatenated amino acid sequences of 13 protein-coding genes. It reveals that B.gaini is clustered with the Anostraca group within the Branchiopoda clade. This study helps us understand the evolution of Anostraca.

Keywords: Branchinectagaini , mitochondrial genome, Antarctica, fairy shrimp, Anostraca

Introduction

Branchinecta Verrill 1869 (Branchiopoda, Anostraca) is a genus of freshwater fairy shrimps. The genus contains approximately 50 species, which are distributed in all continents, except Africa and Australia (Rogers 2006). Amongst them, Branchinectagaini Daday 1910 is the only fairy shrimp found in the Antarctic Peninsula (Peck 2004, Hawes 2009). It is also distributed in South America and subantarctic islands. As for the biogeography of B.gaini, passive dispersal of dormant eggs into and across Antarctica via water, winds or birds has been suggested (Hawes 2009). Despite the predominance and importance of B.gaini in Antarctic freshwater ecosystems (Paggi 1996), molecular studies of B.gaini have been insufficient. Here, we report the complete mitochondrial genome of B.gaini and its phylogenetic relationships within Branchiopoda, based on available mitogenome sequences.

Material and Methods

Adult samples of B.gaini were collected from a freshwater pool located on Weaver Peninsula of King George Island, Antarctica (62°N and 58°E). The samples were captured using hand nets and disposable pipettes and then stored in ethanol solution. The specimens were deposited at the Korea Polar Research Institute (ID: BG-20). Total genomic DNA was extracted using the phenol/chloroform method. The quality and quantity of DNA was checked by gel electrophoresis and PicoGreen assay (Invitrogen, CA, USA), respectively. The sequencing library was prepared using a TruSeq Nano DNA kit (Illumina, CA, USA) and sequenced on an Illumina HiSeq X platform (2 × 151 bp) according to the manufacturer’s protocol. After removing adapters and low-quality sequences, the de novo assembly of the mitochondrial genome was conducted using the QIAGEN CLC Assembly Cell 4.2.1 programme (QIAGEN, CA, USA). Primary annotation was achieved with GeSeq (Tillich et al. 2017), followed by manual curation using Artemis (Carver et al. 2012). The mitochondrial gene map of the B.gaini was displayed by OrganellarGenomeDRAW (OGDRAW) version 1.3.1 (Greiner et al. 2019). For the phylogenetic analysis, General Reversible Mitochondrial (mtREV) with Frequencies (+F) model was selected as the best-fit amino acid substitution model. Maximum Likelihood (ML) tree was constructed with 1,000 bootstrap replications and the mtREV+F+G+I model (Adachi and Hasegawa 1996) using MEGA X software (Kumar et al. 2018). The mitogenome data used in the phylogenetic analysis were selected with reference to Yang and Chen (2020) and are presented in Table 1.

Table 1.

List of mitogenome data used in the phylogenetic analysis.

Species name Class Order Family GenBank number Reference
Artemiafranciscana Branchiopoda Anostraca Artemiidae NC_001620 Perez et al. (1994)
Branchinectagaini Branchiopoda Anostraca Branchinectidae MZ265218 This study
Branchinellakugenumaensis Branchiopoda Anostraca Thamnocephalidae NC_054250 Sun (2021)
Phallocryptustserensodnomi Branchiopoda Anostraca Thamnocephalidae NC_026710 Fan et al. (2016)
Streptocephalussirindhornae Branchiopoda Anostraca Streptocephalidae NC_026704 Liu et al. (2016)
Daphniamagna Branchiopoda Diplostraca Daphniidae NC_026914 Cheng et al. (2015) (unpublished)
Daphniapulex Branchiopoda Diplostraca Daphniidae NC_000844 Crease (1999)
Triopscancriformis Branchiopoda Notostraca Triopsidae NC_004465 Umetsu et al. (2002)
Triopslongicaudatus Branchiopoda Notostraca Triopsidae NC_006079 Cook et al. (2005)
Hutchinsoniellamacracantha Cephalocarida Brachypoda Hutchinsoniellidae AY456189 Lavrov et al. (2004)
Open in a new tab

Results and Discussion

The complete mitochondrial genome of B.gaini Daday, 1910 (GenBank number: MZ265218) is 15,536 bp in length, containing 13 protein-coding genes, 23 transfer RNA genes (tRNAs), two ribosomal RNA genes (rRNAs) and two major non-coding regions (Fig. 1). Interestingly, B.gaini have two copies of tRNAGly genes and a 397 bp non-coding region between tRNAGly1 and tRNAGly2 genes. To exclude the possibility of assembly error, sequences including the two tRNAGly genes and non-coding region were reconfirmed through traditional Sanger sequencing. It was found that tRNAGly gene duplication did not appear in other anostracans or branchiopods species. The non-coding region between the tRNAGly genes was first identified in anosctacan species, although the cephalocarid crustacean Hutchinsoniellamacracantha was reported to have a 666 bp non-coding region between tRNAGly and nad3 genes (Lavrov et al. 2004). After more mitogenomes are revealed in closely-related species, further research is needed to explain why tRNAGly gene duplication has been occurred in B.gaini. The B.gaini mitogenome have a GC content of 35.2% and an AT content of 64.8%. Its protein-coding genes have four types of start codons (5 ATGs, 5 ATTs, 2 TTGs and 1 ATC) and three types of stop codons (6 TAAs, 2 TAGs and 5 incomplete T(AA)s).

Figure 1.

Figure 1.

Open in a new tab

Circular map of the mitochondrial genome of Branchinectagaini. Genes drawn inside the circle are transcribed in a clockwise and genes drawn outside the circle are transcribed in a counterclockwise direction. The inner grey circle shows the GC content.

Phylogenetic relationships of B.gaini with eight species within class Branchiopoda and one outgroup (H.macracantha) were analysed using concatenated amino acid sequences of 13 protein-coding genes (Fig. 2). The tree shows that B.gaini is situated in a monophyletic cluster formed by Anostraca species (Streptocephalussirindhornae, Branchinellakugenumaensis, Phallocryptustserensodnomi and Artemiafranciscana) within the Branchiopoda clade. This study reports the complete mitochondrial genome of B.gaini. It will help us understand the evolution of Anostraca.

Figure 2.

Figure 2.

Open in a new tab

Phylogenetic tree for Branchiopoda species, based on complete mitogenome data using the Maximum Likelihood (ML) method and General Reversible Mitochondrial (mtREV) with Frequencies (+F) +G+I model implemented in MEGA X. Scientific names and GenBank accession numbers are shown for each branch. The species in this study is marked in bold. The bootstrap values are displayed on each node. The scale bar represents the number of substitutions per site.

Acknowledgements

This work was supported by Korea Polar Research Institute (KOPRI) grant funded by the Ministry of Oceans and Fisheries (KOPRI PE22160).

Hosting institution

Korea Polar Research Institute.

Conflicts of interest

No potential conflict of interest was reported by the author(s).

Conflicts of interest

No potential conflict of interest was reported by the author(s).

References

  1. Adachi Jun, Hasegawa Masami. Model of amino acid substitution in proteins encoded by mitochondrial DNA. Journal of Molecular Evolution. 1996;42(4):459–468. doi: 10.1007/BF02498640. [DOI] [PubMed] [Google Scholar]
  2. Carver Tim, Harris Simon R, Berriman Matthew, Parkhill Julian, McQuillan Jacqueline A. Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics. 2012;28(4):464–469. doi: 10.1093/bioinformatics/btr703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cook Charles E, Yue Qiaoyun, Akam Michael. Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic. Proceedings of the Royal Society B: Biological Sciences. 2005;272(1569):1295–1304. doi: 10.1098/rspb.2004.3042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Crease Teresa J. The complete sequence of the mitochondrial genome of Daphniapulex (Cladocera: Crustacea) Gene. 1999;233(1-2):89–99. doi: 10.1016/S0378-1119(99)00151-1. [DOI] [PubMed] [Google Scholar]
  5. Daday Eugen. Quelques Phyllopodes Anostracés nouveaux. Appendice a la monographie systématique des Phyllopodes Anostracés; Annales des Sciences Naturelles Zoologie et Biologie Animale; 1910. 23 [Google Scholar]
  6. Fan Yu-Peng, Lu Bo, Yang Jin-Shu. The complete mitogenome of the fairy shrimp Phallocryptustserensodnomi (Crustacea: Anostraca: Thamnocephalidae) Mitochondrial DNA Part A. 2016;27(5):3113–3114. doi: 10.3109/19401736.2015.1007290. [DOI] [PubMed] [Google Scholar]
  7. Greiner Stephan, Lehwark Pascal, Bock Ralph. OrganellarGenomeDRAW (OGDRAW) version 1.3. 1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Research. 2019;47(W1) doi: 10.1093/nar/gkz238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hawes T. C. Origins and dispersal of the Antarctic fairy shrimp. Antarctic Science. 2009;21(5) doi: 10.1017/S095410200900203X. [DOI] [Google Scholar]
  9. Kumar Sudhir, Stecher Glen, Li Michael, Knyaz Christina, Tamura Koichiro. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution. 2018;35(6) doi: 10.1093/molbev/msy096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lavrov Dennis V, Brown Wesley M, Boore Jeffrey L. Phylogenetic position of the Pentastomida and (pan) crustacean relationships. Proceedings of the Royal Society of London. Series B: Biological Sciences. 2004;271(1538):537–544. doi: 10.1098/rspb.2003.2631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Liu Xue-Chen, Li Hua-Wei, Jermnak Usuma, Yang Jin-Shu. The complete mitogenome of the freshwater fairy shrimp Streptocephalussirindhornae (Crustacea: Anostraca: Streptocephalidae) Mitochondrial DNA Part A. 2016;27(5):3189–3191. doi: 10.3109/19401736.2015.1007329. [DOI] [PubMed] [Google Scholar]
  12. Paggi J. C. Feeding ecology of Branchinectagaini (Crustacea: Anostraca) in ponds of south Shetland Islands, Antarctica. Polar Biology. 1996;16(1):13–18. doi: 10.1007/BF02388730. [DOI] [Google Scholar]
  13. Peck Lloyd S. Physiological flexibility: the key to success and survival for Antarctic fairy shrimps in highly fluctuating extreme environments. Freshwater Biology. 2004;49(9):1195–1205. doi: 10.1111/j.1365-2427.2004.01264.x. [DOI] [Google Scholar]
  14. Perez Maria Luz, Valverde José Ramón, Batuecas Beatriz, Amat Francisco, Marco Roberto, Garesse Rafael. Speciation in the Artemia genus: mitochondrial DNA analysis of bisexual and parthenogenetic brine shrimps. Journal of Molecular Evolution. 1994;38(2):156–168. doi: 10.1007/BF00166162. [DOI] [PubMed] [Google Scholar]
  15. Rogers D CHRISTOPHER. Three new species of Branchinecta (Crustacea: Branchiopoda: Anostraca) from the nearctic. Zootaxa. 2006;1126(1):35–51. doi: 10.11646/zootaxa.1126.1.3. [DOI] [Google Scholar]
  16. Sun Xiaoyan. Divergence across the mitogenomes of Branchinellakugenumaensis (Anostraca: Thamnocephalidae) with implications for species delimitation. Mitochondrial DNA Part B. 2021;6(2):631–633. doi: 10.1080/23802359.2021.1876537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Tillich Michael, Lehwark Pascal, Pellizzer Tommaso, Ulbricht-Jones Elena S, Fischer Axel, Bock Ralph, Greiner Stephan. GeSeq–versatile and accurate annotation of organelle genomes. Nucleic Acids Research. 2017;45(W1) doi: 10.1093/nar/gkx391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Umetsu Kazuo, Iwabuchi Naruki, Yuasa Isao, Saitou Naruya, Clark Paul F, Boxshall Geoff, Osawa Motoki, Igarashi Keiji. Complete mitochondrial DNA sequence of a tadpole shrimp (Triopscancriformis) and analysis of museum samples. Electrophoresis. 2002;23(24):4080–4084. doi: 10.1002/elps.200290024. [DOI] [PubMed] [Google Scholar]
  19. Verrill Addison Emery. Contributions to zoology from the Museum of Yale College; No. III, Descriptions of some new American phyllopod Crustacea. American Journal of Science. 1869;2(143):244–254. doi: 10.2475/ajs.s2-48.143.244. [DOI] [Google Scholar]
  20. Yang Ri-Sheng, Chen Yi-Tao. The complete mitochondrial genome of the freshwater fairy shrimp Branchinellakugenumaensis Ishikawa 1894 (Crustacea: Anostraca: Thamnocephalidae) Mitochondrial DNA Part B. 2020;5(1):1048–1049. doi: 10.1080/23802359.2020.1721367. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biodiversity Data Journal are provided here courtesy of Pensoft Publishers

RESOURCES