Skip to main content
SpringerLink
Log in

Complete mitochondrial genomes of two deep-sea pandalid shrimps, Heterocarpus ensifer and Bitias brevis: insights into the phylogenetic position of Pandalidae (Decapoda: Caridea)

  • Biology
  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

The mitochondrial genome (mitogenome) analysis is a significant tool for investigating the evolutionary history of metazoan animals. The family Pandalidae is a diverse caridean group containing mainly deep-sea species. Until May 30 2019, only two complete mitogenomes are available in GenBank. Here we present the complete mitogenome sequences of two deep-sea pandalid shrimps, Heterocarpus ensifer and Bitias brevis through Illumina sequencing. The mitochondrial genomes were determined to be 15 939 bp and 15 891 bp long, and both consist of 13 protein-coding genes (PCGs), 23 transfer-RNA genes (tRNAs), two ribosomal-RNA genes (rRNAs), and one control region. The nucleotide composition is biased toward adenine and thymine. Overall, the gene contents and arrangements are consistent with the pancrustacean ground pattern. The alignment of the control regions of four pandalids reveals a conserved sequence block (CSB) (104 bp in length, average GC%=29.47% and 69.23% similarity). A phylogenetic analysis based on 51 Caridea complete mitogenomes revealed that the deep-sea pandalid shrimps are situated an intermediate lineage, with a tendency to originated from those living in shallow sea area.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data Availability Statement

The authors declare that all data supporting the findings of this study are available within the appendix sections.

References

  • Aznar-Cormano L, Brisset J, Chan T Y, Corbari L, Puillandre N, Utge J, Zbinden M, Zuccon D, Samadi S. 2015. An improved taxonomic sampling is a necessary but not sufficient condition for resolving inter-families relationships in Caridean decapods. Genetica, 143 (2): 195–205.

    Article  Google Scholar 

  • Benson G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research27 (2): 573–580.

    Article  Google Scholar 

  • Boore J L, Brown W M. 1998. Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Current Opinion in Genetics & Development, 8 (6): 668–674.

    Article  Google Scholar 

  • Boore J L, Medina M, Rosenberg L A. 2004. Complete sequences of the highly rearranged molluscan mitochondrial genomes of the Scaphopod Graptacme eborea and the Bivalve Mytilus edulis. Molecular Biology and Evolution, 21 (8): 1492–1503.

    Article  Google Scholar 

  • Boore J L. 1999. Animal mitochondrial genomes. Nucleic Acids Research, 27 (8): 1767–1780.

    Article  Google Scholar 

  • Bracken H D, De Grave S A M M Y, Felder D L. 2009. Phylogeny of the infraorder Caridea based on mitochondrial and nuclear genes (Crustacea: Decapoda). In: Martin J W, Crandall K A, Felder D L eds. Decapod Crustacean Phylogenetics. CRC Press, Boca Raton. p.1–305.

    Google Scholar 

  • Bulmer M. 1987. Coevolution of codon usage and transfer RNA abundance. Nature, 325 (6106): 728–730.

    Article  Google Scholar 

  • Cameron S L, Johnson K P, Whiting M F. 2007. The mitochondrial genome of the screamer louse Bothriometopus (Phthiraptera: Ischnocera): effects of extensive gene rearrangements on the evolution of the genome. Journal of Molecular Evolution65 (6): 589–604.

    Article  Google Scholar 

  • Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17 (4): 540–552.

    Article  Google Scholar 

  • Chai H N, Du Y Z, Zhai B P. 2012. Characterization of the complete mitochondrial genomes of Cnaphalocrocis medinalis and Chilo suppressalis (Lepidoptera: Pyralidae). International Journal of Biological Sciences8 (4): 561–579.

    Article  Google Scholar 

  • Chimnaronk S, Gravers Jeppesen M, Suzuki T, Nyborg J, Watanabe K. 2005. Dual-mode recognition of noncanonical tRNAs(Ser) by seryl-tRNA synthetase in mammalian mitochondria. European Molecular Biology Organization Journal, 24 (19): 3369–3379.

    Article  Google Scholar 

  • Crozier R H, Crozier Y C. 1993. The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics, 133 (1): 97–117.

    Google Scholar 

  • Curole J P, Kocher T D. 1999. Mitogenomics: digging deeper with complete mitochondrial genomes. Trends in Ecology & Evolution, 14 (10): 394–398.

    Article  Google Scholar 

  • De Grave S, Fransen C H J M. 2011. Carideorum Catalogus: the recent species of the dendrobranchiate, stenopodidean, procarididean and caridean shrimps (Crustacea: Decapoda). Zoologische Mededelingen, 85: 195–589.

    Google Scholar 

  • De Grave S, Pentcheff N D, Ahyong S T, Chan T Y, Crandall K A, Dworschak P C, Felder D L, Feldmann R M, Fransen C H J M, Goulding L Y D, Lemaitre R, Low M E Y, Martin J W, Ng P K L, Schweitzer C E, Tan S H, Tshudy D, Wetzer R. 2009. A classification of living and fossil genera of decapod crustaceans. Raffles Bulletin of Zoology, (S21): 1–109.

    Google Scholar 

  • Drummond A J, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7 (1): 214.

    Article  Google Scholar 

  • Gage J D, Tyler P D. 1991. Deep-sea Biology: A Natural History of Organisms at the Deep-Sea Floor. Cambridge University Press, Cambridge, UK.

    Book  Google Scholar 

  • Gissi C, Iannelli F, Pesole G. 2008. Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity101 (4): 301–320.

    Article  Google Scholar 

  • Hao J S, Sun Q Q, Zhao H B, Sun X Y, Gai Y H, Yang Q. 2012. The complete mitochondrial genome of Ctenoptilum vasava (Lepidoptera: Hesperiidae: Pyrginae) and its phylogenetic implication. Comparative and Functional Genomics, 2012. 32. 049.

    Google Scholar 

  • Hebert P D N, Cywinska A, Ball S L, deWaard J R. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society B Biological Sciences270 (1512): 313–321.

    Article  Google Scholar 

  • Katoh K, Kuma K, Toh H, Miyata T. 2005. MAFFT versio. 5. improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33 (2): 511–518.

    Article  Google Scholar 

  • Kim M I, Baek J Y, Kim M J, Jeong H C, Kim K G, Bae C H, Han Y S, Jin B R, Kim I. 2009. Complete nucleotide sequence and organization of the mitogenome of the red-spotted apollo butterfly, Parnassius bremeri (Lepidoptera: Papilionidae) and comparison with other lepidopteran insects. Molecules and Cells, 28 (4): 347–363.

    Article  Google Scholar 

  • Kuhn K, Streit B, Schwenk K. 2008. Conservation of structural elements in the mitochondrial control region of Daphnia. Gene, 420 (2): 107–112.

    Article  Google Scholar 

  • Lanfear R, Calcott B, Ho S Y W, Guindon S. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution29 (6): 1695–1701.

    Article  Google Scholar 

  • Laslett D, Canbäck B. 2008. ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics, 24 (2): 172–175.

    Article  Google Scholar 

  • Lavrov D V, Boore J L, Brown W M. 2000. The complete mitochondrial DNA sequence of the horseshoe crab Limulus polyphemus. Molecular Biology and Evolution17 (5): 813–824.

    Article  Google Scholar 

  • Lee W J, Kocher T D. 1995. Complete sequence of a sea lamprey (Petromyzon marinus) mitochondrial genome: early establishment of the vertebrate genome organization. Genetics, 139 (2): 873.

    Google Scholar 

  • Lessinger A C, Junqueira A C M, Lemos T A, Kemper E L, da Silva F R, Vettore A L, Arruda P, Azeredo-Espin A M L. 2000. The mitochondrial genome of the primary screwworm fly Cochliomyia hominivorax (Diptera: Calliphoridae). Insect Molecular Biology, 9 (5): 521–529.

    Article  Google Scholar 

  • Li C P, De Grave S, Chan T Y, Lei H C, Chu K H. 2011. Molecular systematics of caridean shrimps based on five nuclear genes: implications for superfamily classification. Zoologischer Anzeiger—A Journal of Comparative Zoology, 250 (4): 270–279.

    Article  Google Scholar 

  • Li R Q, Zhu H M, Ruan J, Qian W B, Fang X D, Shi Z B, Li Y R, Li S T, Shan G, Kristiansen K, Li S G, Yang H M, Wang J, Wang J. 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Research, 20 (2): 265–272.

    Article  Google Scholar 

  • Liao Y S, De Grave S, Ho T W, Ip B H Y, Tsang L M, Chan T Y, Chu K H. 2017. Molecular phylogeny of Pasiphaeidae (Crustacea, Decapoda, Caridea) reveals systematic incongruence of the current classification. Molecular Phylogenetics and Evolution, 115: 171–180.

    Article  Google Scholar 

  • Liao Y S, Ma K Y, De Grave S, Komai T, Chan T Y, Chu K H. 2019. Systematic analysis of the caridean shrimp superfamily Pandaloidea (Crustacea: Decapoda) based on molecular and morphological evidence. Molecular Phylogenetics and Evolution, 134: 200–210.

    Article  Google Scholar 

  • Lin F J, Yuan L, Sha Z L, Tsang L M, Chu K H, Chan T Y, Liu R Y, Cui Z X. 2012. Evolution and phylogeny of the mud shrimps (Crustacea: Decapoda) revealed from complete mitochondrial genomes. BMC Genomics, 13: 631.

    Article  Google Scholar 

  • Liu Y, Cui Z. 2010. Complete mitochondrial genome of the Asian paddle crab Charybdis japonica (Crustacea: Decapoda: Portunidae): gene rearrangement of the marine brachyurans and phylogenetic considerations of the decapods. Molecular Biology Reports37 (5): 2559–2569.

    Article  Google Scholar 

  • Liu Z K, Gao P, Ashraf M A, Wen J B. 2016. The complete mitochondrial genomes of two weevils, Eucryptorrhynchus chinensis and E brandti: conserved genome arrangement in Curculionidae and deficiency of tRNA-Ile gene. Open Life Sciences, 11 (1): 458–469.

    Article  Google Scholar 

  • Masta S E, Boore J L. 2004. The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. Molecular Biology and Evolution, 21 (5): 893–902.

    Article  Google Scholar 

  • Mindell D P, Sorenson M D, Dimcheff D E. 1998. Multiple independent origins of mitochondrial gene order in birds. Proceedings of the National Academy of Sciences of the United States of America, 95 (18). 1693–10697.

    Google Scholar 

  • Moritz C, Brown W M. 1987. Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proceedings of the National Academy of Sciences of the United States of America84 (20): 7183–7187.

    Article  Google Scholar 

  • Mueller R L, Boore J L. 2005. Molecular mechanisms of extensive mitochondrial gene rearrangement in plethodontid salamanders. Molecular Biology and Evolution, 22 (10): 2104–2112.

    Article  Google Scholar 

  • Ohtsuki T, Kawai G, Watanabe K. 2002. The minimal tRNA: unique structure of Ascaris suum mitochondrial tRNASerUCU having a short T arm and lacking the entire D arm. FEBS Letters, 514 (1): 37–43.

    Article  Google Scholar 

  • Ojala D, Montoya J, Attardi G. 1981. tRNA punctuation model of RNA processing in human mitochondria. Nature290 (5806): 470–474.

    Article  Google Scholar 

  • Oliveira M T, Barau J G, Junqueira A C M, Feijão P C, da Rosa A C, Abreu C F, Azeredo-Espin A M L, Lessinger A C. 2008. Structure and evolution of the mitochondrial genomes of Haematobia irritans and Stomoxys calcitrans: the Muscidae (Diptera: Calyptratae) perspective. Molecular Phylogenetics and Evolution, 48 (3): 850–857.

    Article  Google Scholar 

  • Perna N T, Kocher T D. 1995. Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution41 (3): 353–358.

    Article  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres D L, Darling A, Höhna S, Larget B, Liu L, Suchard M A, Huelsenbeck J P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3): 539–542.

    Article  Google Scholar 

  • Salvato P, Simonato M, Battisti A, Negrisolo E. 2008. The complete mitochondrial genome of the bag-shelter moth Ochrogaster lunifer (Lepidoptera, Notodontidae). BMC Genomics, 9 (1): 331.

    Article  Google Scholar 

  • Satoh T P, Sato Y, Masuyama N, Miya M, Nishida M. 2010. Transfer RNA gene arrangement and codon usage in vertebrate mitochondrial genomes: a new insight into gene order conservation. BMC Genomics, 11 (1): 479.

    Article  Google Scholar 

  • Serb J M, Lydeard C. 2003. Complete mtDNA sequence of the North American freshwater mussel, Lampsilis ornata (Unionidae): an examination of the evolution and phylogenetic utility of mitochondrial genome organization in Bivalvia (Mollusca). Molecular Biology and Evolution20 (11): 1854–1866.

    Article  Google Scholar 

  • Shen H, Braband A, Scholtz G. 2013. Mitogenomic analysis of decapod crustacean phylogeny corroborates traditional views on their relationships. Molecular Phylogenetics and Evolution, 66 (3): 776–789.

    Article  Google Scholar 

  • Simon C, Buckley T R, Frati F, Stewart J B, Beckenbach A T. 2006. Incorporating molecular evolution into phylogenetic analysis, and a new compilation of conserved polymerase chain reaction primers for animal mitochondrial DNA. Annual Review of Ecology Evolution and Systematics37 (1): 545–579.

    Article  Google Scholar 

  • Stokkan M, Jurado-Rivera J A, Juan C, Jaume D, Pons J. 2016. Mitochondrial genome rearrangements at low taxonomic levels: three distinct mitogenome gene orders in the genus Pseudoniphargus (Crustacea: Amphipoda). Mitochondrial DNA Part A, 27 (5): 3579–3589.

    Article  Google Scholar 

  • Stothard P, Wishart D S. 2005. Circular genome visualization and exploration using CGView. Bioinformatics21 (4): 537–539.

    Article  Google Scholar 

  • Sun S E, Hui M, Wang M X, Sha Z L. 2018. The complete mitochondrial genome of the alvinocaridid shrimp Shinkaicaris leurokolos (Decapoda, Caridea): insight into the mitochondrial genetic basis of deep-sea hydrothermal vent adaptation in the shrimp. Comparative Biochemistry and Physiology Part D: Genomics Proteomics25: 42–52.

    Google Scholar 

  • Sun Z, Wan D G, Murphy R W, Ma L, Zhang S H, Huang D V. 2009. Comparison of base composition and codon usage in insect mitochondrial genomes. Genes and Genomics31 (1): 65–71.

    Article  Google Scholar 

  • Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology56 (4): 564–577.

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28 (10): 2731–2739.

    Article  Google Scholar 

  • Trifinopoulos J, Nguyen L T, von Haeseler A, Minh B Q. 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research44 (W1): W232–W235.

    Article  Google Scholar 

  • Walberg M W, Clayton D A. 1981. Sequence and properties of the human KB cell and mouse L cell D-loop regions of mitochondrial DNA. Nucleic Acids Research9 (20): 5411–5421.

    Article  Google Scholar 

  • Wolstenholme D R. 1992. Genetic novelties in mitochondrial genomes of multicellular animals. Current Opinion in Genetics and Development, 2 (6): 918–925.

    Article  Google Scholar 

  • Wyman S K, Jansen R K, Boore J L. 2004. Automatic annotation of organellar genomes with DOGMA. Bioinformatics, 20 (17): 3 252–3 255.

    Article  Google Scholar 

  • Xia X H. 2005. Mutation and selection on the anticodon of tRNA genes in vertebrate mitochondrial genomes. Gene345 (1): 13–20.

    Article  Google Scholar 

  • Xia X, Lemey P. 2009. Assessing substitution saturation with DAMBE. In: Lemey, Philippe, Salemi, Marco, Vandamme, Anne-Mieke (Eds.), The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny, 2nd edition. Cambridge University Press. p.615–630.

    Chapter  Google Scholar 

  • Xia X, Xie Z, Salemi M, Chen L, Wang Y. 2003. An index of substitution saturation and its application. Molecular Phylogenetics and Evolution, 26 (1): 1–7.

    Article  Google Scholar 

  • Yang J, Ye F, Huang Y. 2016. Mitochondrial genomes of four katydids (Orthoptera: Phaneropteridae): New gene rearrangements and their phylogenetic implications. Gene, 575: 702–711.

    Article  Google Scholar 

  • Yuan Y, Li Q, Yu H, Kong L F. 2012. The complete mitochondrial genomes of six heterodont bivalves (Tellinoidea and Solenoidea): Variable gene arrangements and phylogenetic implications. PLoS One, 7 (2): e32353.

    Article  Google Scholar 

  • Zhang D X, Hewitt G M. 1997. Insect mitochondrial control region: A review of its structure, evolution and usefulness in evolutionary studies. Biochemical Systematics and Ecology, 25 (2): 99–120.

    Article  Google Scholar 

  • Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research31 (13): 3406–3415.

    Article  Google Scholar 

Download references

Acknowledgment

The samples were collected by R/V Kexue.

Author information

Authors and Affiliations

  1. Department of Marine Organism Taxonomy and Phylogeny, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Shao’e Sun, Jiao Cheng, Song Sun & Zhongli Sha

  2. Deep Sea Research Center, Institute of Oceanology, Chinese Academy of Science, Qingdao, 266071, China

    Shao’e Sun, Jiao Cheng & Zhongli Sha

  3. University of Chinese Academy of Sciences, Beijing, 100049, China

    Song Sun & Zhongli Sha

Authors
  1. Shao’e Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiao Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Song Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhongli Sha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhongli Sha.

Additional information

Supported by the Key Research Program of Frontier Sciences, Chinese Academy of Sciences (CAS) (No. QYZDB-SSW-DQC036), the Strategic Priority Research Program of CAS (No. XDA22050302), the Senior User Project of R/V Kexue (No. KEXUE2019GZ02), and the National Natural Science Foundation of China (No. 31872215)

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, S., Cheng, J., Sun, S. et al. Complete mitochondrial genomes of two deep-sea pandalid shrimps, Heterocarpus ensifer and Bitias brevis: insights into the phylogenetic position of Pandalidae (Decapoda: Caridea). J. Ocean. Limnol. 38, 816–825 (2020). https://doi.org/10.1007/s00343-019-9040-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-019-9040-x

Keyword

Search

Navigation