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First comparative insight into the architecture of COI mitochondrial minicircle molecules of dicyemids reveals marked inter-species variation

Published online by Cambridge University Press:  16 April 2015

SARAH R. CATALANO ,
IAN D. WHITTINGTON ,
STEPHEN C. DONNELLAN ,
TERRY BERTOZZI  and
BRONWYN M. GILLANDERS
SARAH R. CATALANO*
Affiliation:
School of Biological Sciences, University of Adelaide, Adelaide SA 5005, Australia Southern Seas Ecology Laboratories, University of Adelaide, Adelaide SA 5005, Australia Australian Centre for Evolutionary Biology and Biodiversity, University of Adelaide, Adelaide SA 5005, Australia Evolutionary Biology Unit, South Australian Museum, Adelaide SA 5000, Australia
IAN D. WHITTINGTON
Affiliation:
Parasitology Section, South Australian Museum, Adelaide SA 5000, Australia
STEPHEN C. DONNELLAN
Affiliation:
Australian Centre for Evolutionary Biology and Biodiversity, University of Adelaide, Adelaide SA 5005, Australia Evolutionary Biology Unit, South Australian Museum, Adelaide SA 5000, Australia
TERRY BERTOZZI
Affiliation:
School of Biological Sciences, University of Adelaide, Adelaide SA 5005, Australia Australian Centre for Evolutionary Biology and Biodiversity, University of Adelaide, Adelaide SA 5005, Australia Evolutionary Biology Unit, South Australian Museum, Adelaide SA 5000, Australia
BRONWYN M. GILLANDERS
Affiliation:
School of Biological Sciences, University of Adelaide, Adelaide SA 5005, Australia Southern Seas Ecology Laboratories, University of Adelaide, Adelaide SA 5005, Australia Environment Institute, University of Adelaide, Adelaide SA 5005, Australia
*
* Corresponding author. North Terrace Campus, Evolutionary Biology Unit, University of Adelaide, Darling Building, DX 650 418, Adelaide, SA 5005, Australia. E-mail: [email protected]
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Summary

Dicyemids, poorly known parasites of benthic cephalopods, are one of the few phyla in which mitochondrial (mt) genome architecture departs from the typical ~16 kb circular metazoan genome. In addition to a putative circular genome, a series of mt minicircles that each comprises the mt encoded units (I–III) of the cytochrome c oxidase complex have been reported. Whether the structure of the mt minicircles is a consistent feature among dicyemid species is unknown. Here we analyse the complete cytochrome c oxidase subunit I (COI) minicircle molecule, containing the COI gene and an associated non-coding region (NCR), for ten dicyemid species, allowing for first time comparisons between species of minicircle architecture, NCR function and inferences of minicircle replication. Divergence in COI nucleotide sequences between dicyemid species was high (average net divergence = 31·6%) while within species diversity was lower (average net divergence = 0·2%). The NCR and putative 5′ section of the COI gene were highly divergent between dicyemid species (average net nucleotide divergence of putative 5′ COI section = 61·1%). No tRNA genes were found in the NCR, although palindrome sequences with the potential to form stem-loop structures were identified in some species, which may play a role in transcription or other biological processes.

Keywords

Dicyemidamitochondrial DNAminicircle moleculescytochrome c oxidasemulti-species phylogenetic comparisonstaxonomic classification
Type
Research Article
Information
Parasitology , Volume 142 , Issue 8 , July 2015 , pp. 1066 - 1079
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Armstrong, M. R., Blok, V. C. and Phillips, M. S. (1999). A multipartite mitochondrial genome in the potato cyst nematode Globodera pallida . Genetics 154, 181–192.Google Scholar
Aruga, J., Odaka, Y. S., Kamiya, A. and Furuya, H. (2007). Dicyemid Pax6 and Zic: tool-kit genes in a highly simplified bilaterian. BMC Evolutionary Biology 7, 1–16.CrossRefGoogle Scholar
Awata, H., Noto, T. and Endoh, H. (2005). Differentiation of somatic mitochondria and the structured changes in mtDNA during development of the dicyemid Dicyema japonicum (Mesozoa). Molecular Genetics and Genomics 273, 441–449.Google Scholar
Barbrook, A. C., Symington, H., Nisbet, R. E. R., Larkum, A. and Howe, C. J. (2001). Organisation and expression of the plastid genome of the dinoflagellate Amphidinium operculatum . Molecular Genetics and Genomics 266, 632–638.Google Scholar
Boore, J. L. (1999). Animal mitochondrial genomes. Nucleic Acids Research 27, 1767–1780.Google Scholar
Burger, G., Gray, M. W. and Lang, B. F. (2003). Mitochondrial genomes: anything goes. Trends in Genetics 19, 709–716.Google Scholar
Burger, G., Jackson, C. J. and Waller, R. F. (2012). Unusual mitochondrial genomes and genes. In Organelle Genetics: Evolution of Organelle Genomes and Gene Expression (ed. Bullerwell, C. E.), pp. 41–77. Springer, Berlin, Heidelberg.Google Scholar
Cameron, S. L., Yoshizawa, K., Mizukoshi, A., Whiting, M. F. and Johnson, K. P. (2011). Mitochondrial genome deletions and minicircles are common in lice (Insecta: Phthiraptera). BMC Genomics 12, 1–15.CrossRefGoogle ScholarPubMed
Cantatore, P., Roberti, M., Rainaldi, G., Gadaleta, M. N. and Saccone, C. (1989). The complete nucleotide sequence, gene organization, and genetic code of the mitochondrial genome of Paracentrotus ziuidus . The Journal of Biological Chemistry 264, 10965–10975.CrossRefGoogle Scholar
Catalano, S. R. (2012). A review of the families, genera and species of Dicyemida Van Beneden, 1876. Zootaxa 3479, 1–32.CrossRefGoogle Scholar
Catalano, S. R. (2013 a). First descriptions of dicyemid mesozoans (Dicyemida: Dicyemidae) from Australian octopus (Octopodidae) and cuttlefish (Sepiidae) species, including a new record of Dicyemennea in Australian waters. Folia Parasitologica 60, 306–320.CrossRefGoogle ScholarPubMed
Catalano, S. R. (2013 b). Five new species of dicyemid mesozoans (Dicyemida: Dicyemidae) from two Australian cuttlefish species, with comments on dicyemid fauna composition. Systematic Parasitology 86, 125–151.Google Scholar
Catalano, S. R. and Furuya, H. (2013). Two new species of dicyemid (Dicyemida: Dicyemidae) from two Australian cephalopod species: Sepioteuthis australis (Mollusca: Cephalopoda: Loliginidae) and Sepioloidea lineolata (Mollusca: Cephalopoda: Sepiadariidae). Journal of Parasitology 99, 203–211.CrossRefGoogle ScholarPubMed
Catalano, S. R., Whittington, I. D., Donnellan, S. C. and Gillanders, B. M. (2014). Dicyemid fauna composition and infection patterns in relation to cephalopod host biology and ecology. Folia Parasitologica 61, 301–310.Google Scholar
Darling, J. A., Bagley, M. J., Roman, J., Tepolt, C. K. and Geller, J. B. (2008). Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus . Molecular Ecology 17, 4992–5007.CrossRefGoogle ScholarPubMed
Dong, W. E., Song, S., Guo, X. G., Jin, D. C., Yang, Q., Barker, S. C. and Shao, R. (2014 a). Fragmented mitochondrial genomes are present in both major clades of the blood-sucking lice (suborder Anoplura): evidence from two Hoplopleura rodent lice (family Hoplopleuridae). BMC Genomics 15, 751.Google Scholar
Dong, W. E., Song, S., Jin, D. C., Guo, X. G. and Shao, R. (2014 b). Fragmented mitochondrial genomes of the rat lice, Polyplax asiatica and Polyplax spinulosa: intra-genus variation in fragmentation pattern and a possible link between the extent of fragmentation and the length of life cycle. BMC Genomics 15, 44.Google Scholar
Drummond, A. J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T. and Wilson, A. (2010). Geneious v5.3. http://www.geneious.com.Google Scholar
Elzanowski, A. and Ostell, J. (2013). The genetic codes. http://www.ncbi.nlm.nih.gov/Taxonomy/Utils/wprintgc.cgi#SG5.Google Scholar
Faller, M. (1999). EMBOSS: Palindrome. http://emboss.bioinformatics.nl/cgi/bin/emboss.palidrome.Google Scholar
Furuya, H., Hochberg, F. G. and Tsuneki, K. (2003). Reproductive traits in dicyemids. Marine Biology 142, 693–706.Google Scholar
Gelfand, R. and Attardi, G. (1981). Synthesis and turnover of mitochondrial ribonucleic acid in HeLa cells: the mature ribosomal and messenger ribonucleic acid species are metabolically unstable. Molecular and Cellular Biology 1, 497–511.Google Scholar
Gibson, T., Blok, V. C. and Dowton, M. (2007 a). Sequence and characterization of six mitochondrial subgenomes from Globodera rostochiensis: multipartite structure is conserved among close nematode relatives. Journal of Molecular Evolution 65, 308–315.CrossRefGoogle ScholarPubMed
Gibson, T., Blok, V. C., Phillips, M. S., Hong, G., Kumarasinghe, D., Riley, I. T. and Dowton, M. (2007 b). The mitochondrial subgenomes of the nematode Globodera pallida are mosaics: evidence of recombination in an animal mitochondrial genome. Journal of Molecular Evolution 64, 463–471.Google Scholar
Gibson, T., Farrugia, D., Barrett, J., Chitwood, D. J., Rowe, J., Subbotin, S. and Dowton, M. (2011). The mitochondrial genome of the soybean cyst nematode, Heterodera glycines . Genome 54, 565–574.CrossRefGoogle ScholarPubMed
Guindon, S. and Gascuel, O. (2003). A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.Google Scholar
Guindon, S., Dufayard, J. F., Lefort, V., Anisomova, M., Hordijk, W. and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.Google Scholar
Hasegawa, M., Kishino, H. and Yano, T. (1985). Dating of the human ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Ecology 22, 160–174.Google Scholar
Hochberg, F. G. (1982). The “kidneys” of cephalopods: a unique habitat for parasites. Malacologia 23, 121–134.Google Scholar
Hochberg, F. G. (1983). The parasites of cephalopods: a review. Memoirs of the National Museum Victoria 44, 108–145.CrossRefGoogle Scholar
Jiang, H., Barker, S. C. and Shao, R. (2013). Substantial variation in the extent of mitochondrial genome fragmentation among blood-sucking lice of mammals. Genome Biology and Evolution 5, 1298–1308.CrossRefGoogle ScholarPubMed
Kobayashi, M., Furuya, H. and Holland, P. W. H. (1999). Dicyemids are higher animals. Nature 401, 762.Google Scholar
Kobayashi, M., Furuya, H. and Wada, H. (2009). Molecular markers comparing the extremely simple body plan of dicyemids to that of lophotrochozoans: insight from the expression patterns of Hox, Otx, and brachyury . Evolution and Development 11, 582–589.Google Scholar
Lanfear, R., Calcott, B., Ho, S. Y. W. and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.CrossRefGoogle ScholarPubMed
Laslett, D. and Canback, B. (2004). ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Research 32, 11–16.Google Scholar
Laslett, D. and Canback, B. (2008). ARWEN, a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 24, 172–175.Google Scholar
Le, T. H., Blair, D. and McManus, D. P. (2002). Mitochondrial genomes of parasitic flatworms. Trends in Parasitology 18, 206–213.Google Scholar
Lowe, T. M. and Eddy, S. R. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25, 955–964.Google Scholar
Marande, W., Lukes, J. and Burger, G. (2005). Unique mitochondrial genome structure in diplonemids, the sister group of kinetoplastids. Eukaryotic Cell 4, 1137–1146.Google Scholar
McConnaughey, B. H. (1951). The life cycle of the dicyemid Mesozoa. University of California Publications in Zoology 55, 295–336.Google Scholar
Milbury, C. A. and Gaffney, P. M. (2005). Complete mitochondrial DNA sequence of the eastern oyster Crassostrea virginica . Marine Biotechnology 7, 697–712.Google Scholar
Morrison, D. A. (2010). How and where to look for tRNAs in Metazoan mitochondrial genomes, and what you might find when you get there. In Online Archive arXiv.org, <arXiv:1001:3813v1>. Cornell University Library..+Cornell+University+Library.>Google Scholar
Paland, S. and Lynch, M. (2006). Transitions to asexuality result in excess amino acid substitutions. Science 311, 990–992.Google Scholar
Prescott, D. M. (1994). The DNA of ciliated protozoa. Microbiological Reviews 58, 233–267.Google Scholar
Rambaut, A. (2010). FigTree, version 1.3.1 Institute of Evolutionary Biology, University of Edinburgh. http://tree.bio.ed.ac.uk/software/figtree/.Google Scholar
Rambaut, A. and Drummond, A. J. (2007). Tracer v1.4. http://beast.bio.ed.ac.uk/Tracer.Google Scholar
Rodŕiguez, F., Oliver, J. F., Maŕin, A. and Medina, J. R. (1990). The general stochastic model of nucleotide substitutions. Journal of Theoretical Biology 142, 485–501.Google Scholar
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A. and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Ryan, K. P., Shapiro, T. A., Rauch, C. A. and Englund, P. T. (1988). Replication of kinetoplast DNA in trypanosomes. Annual Review of Microbiology 42, 339–358.Google Scholar
Schipp, R., von Boletzky, S. and Doell, G. (1975). Ultrastructural and cytochemical investigations on the renal appendages and their concrements in dibranchiate cephalopods (Mollusca, Cephalopoda). Zeitschrift für Morphologie der Tiere 81, 279–304.Google Scholar
Shao, R., Kirkness, E. F. and Barker, S. C. (2009). The single mitochondrial chromosome typical of animals has evolved into 18 minichromosomes in the human body louse, Pediculus humanus . Genome Research 19, 904–912.Google Scholar
Shao, R., Zhu, X. Q., Barker, S. C. and Herd, K. (2012). Evolution of extensively fragmented mitochondrial genomes in the lice of humans. Genome Biology and Evolution 4, 1088–1101.CrossRefGoogle ScholarPubMed
Shapiro, T. A. and Englund, P. T. (1995). The structure and replication of kinetoplast DNA. Annual Reviews in Microbiology 49, 117–143.Google Scholar
Smith, D. R., Kayal, E., Yanagihara, A. A., Collins, A. G., Pirro, S. and Keeling, P. J. (2012). First complete mitochondrial genome sequence from a box jellyfish reveals a highly fragmented linear architecture and insights into telomere evolution. Genome Biology and Evolution 4, 58–58.Google Scholar
Song, S. D., Barker, S. C. and Shao, R. (2014). Variation in mitochondrial minichromosome composition between blood-sucking lice of the genus Haematopinus that infest horses and pigs. Parasites and Vectors 7, 144.Google Scholar
Stuart, K. and Feagin, J. E. (1992). Mitochondrial DNA of kinetoplastids. International Review of Cytology 141, 65–87.Google Scholar
Suzuki, T. G., Ogino, K., Tsuneki, K. and Furuya, H. (2010). Phylogenetic analysis of dicyemid mesozoans (Phylum Dicyemida) from innexin amino acid sequences: dicyemids are not related to Platyhelminthes. Journal of Parasitology 96, 614–625.Google Scholar
Taanman, J. (1999). The mitochondrial genome: structure, transcription, translation and replication. Biochimica et Biophysica Acta 1410, 103–123.CrossRefGoogle ScholarPubMed
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA 6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Watanabe, K. I., Bessho, Y., Kawasaki, M. and Hori, H. (1999). Mitochondrial genes are found on minicircle DNA molecules in the mesozoan animal Dicyema . Journal of Molecular Biology 286, 645–650.Google Scholar
Zhang, Z., Green, B. R. and Cavalier-Smith, T. (1999). Single gene circles in dinoflagellate chloroplast genomes. Nature 400, 155–159.Google Scholar
Zhang, Z., Cavalier-Smith, T. and Green, B. R. (2002). Evolution of dinoflagellate unigenic minicircles and the partially concerted divergence of their putative replicon origins. Molecular Biology and Evolution 19, 489–500.Google Scholar