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The Kinetoplast DNA of the Australian Trypanosome, Trypanosoma Cope- Mani, Shares Features with Trypanosoma Cruzi and Trypanosoma Lewisi

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The Kinetoplast DNA of the Australian Trypanosome, Trypanosoma Cope- Mani, Shares Features with Trypanosoma Cruzi and Trypanosoma Lewisi This may be the author’s version of a work that was submitted/accepted for publication in the following source: Botero, Adriana, Kapeller, Irit, Cooper, Crystal, Clode, Peta L., Shlomai, Joseph, & Thompson, R.C. Andrew (2018) The kinetoplast DNA of the Australian trypanosome, Trypanosoma cope- mani, shares features with Trypanosoma cruzi and Trypanosoma lewisi. International Journal for Parasitology, 48(9-10), pp. 691-700. This file was downloaded from: https://eprints.qut.edu.au/204624/ c 2018 The Authors. This work is covered by copyright. Unless the document is being made available under a Creative Commons Licence, you must assume that re-use is limited to personal use and that permission from the copyright owner must be obtained for all other uses. If the docu- ment is available under a Creative Commons License (or other specified license) then refer to the Licence for details of permitted re-use. It is a condition of access that users recog- nise and abide by the legal requirements associated with these rights. If you believe that this work infringes copyright please provide details by email to [email protected] License: Creative Commons: Attribution 2.5 Notice: Please note that this document may not be the Version of Record (i.e. published version) of the work. Author manuscript versions (as Sub- mitted for peer review or as Accepted for publication after peer review) can be identified by an absence of publisher branding and/or typeset appear- ance. If there is any doubt, please refer to the published source. https://doi.org/10.1016/j.ijpara.2018.02.006 International Journal for Parasitology 48 (2018) 691–700 Contents lists available at ScienceDirect International Journal for Parasitology journal homepage: www.elsevier.com/locate/ijpara The kinetoplast DNA of the Australian trypanosome, Trypanosoma copemani, shares features with Trypanosoma cruzi and Trypanosoma lewisi q ⇑ Adriana Botero a, , Irit Kapeller b, Crystal Cooper c, Peta L. Clode c,d, Joseph Shlomai b, R.C Andrew Thompson a a School of Veterinary and Life Sciences, Murdoch University, South Street, Murdoch, WA 6150, Australia b Department of Microbiology and Molecular Genetics and the Kuvin Center for the Study of Infectious and Tropical Diseases, The Hebrew University- Hadassah Medical School, Jerusalem, Israel c Centre for Microscopy, Characterisation and Analysis, University of Western Australia, Stirling Hwy, Crawley, WA 6009, Australia d School of Biological Sciences, University of Western Australia, Stirling Hwy, Crawley, WA 6009, Australia article info abstract Article history: Kinetoplast DNA (kDNA) is the mitochondrial genome of trypanosomatids. It consists of a few dozen Received 20 December 2017 maxicircles and several thousand minicircles, all catenated topologically to form a two-dimensional Received in revised form 24 February 2018 DNA network. Minicircles are heterogeneous in size and sequence among species. They present one or Accepted 26 February 2018 several conserved regions that contain three highly conserved sequence blocks. CSB-1 (10 bp sequence) Available online 17 May 2018 and CSB-2 (8 bp sequence) present lower interspecies homology, while CSB-3 (12 bp sequence) or the Universal Minicircle Sequence is conserved within most trypanosomatids. The Universal Minicircle Keywords: Sequence is located at the replication origin of the minicircles, and is the binding site for the UMS binding Kinetoplast DNA protein, a protein involved in trypanosomatid survival and virulence. Here, we describe the structure and Universal minicircle sequence Universal minicircle binding protein organisation of the kDNA of Trypanosoma copemani, a parasite that has been shown to infect mammalian Maxicircle cells and has been associated with the drastic decline of the endangered Australian marsupial, the woylie Native wildlife (Bettongia penicillata). Deep genomic sequencing showed that T. copemani presents two classes of mini- circles that share sequence identity and organisation in the conserved sequence blocks with those of Trypanosoma cruzi and Trypanosoma lewisi. A 19,257 bp partial region of the maxicircle of T. copemani that contained the entire coding region was obtained. Comparative analysis of the T. copemani entire maxicir- cle coding region with the coding regions of T. cruzi and T. lewisi showed they share 71.05% and 71.28% identity, respectively. The shared features in the maxicircle/minicircle organisation and sequence between T. copemani and T. cruzi/T. lewisi suggest similarities in their process of kDNA replication, and are of significance in understanding the evolution of Australian trypanosomes. Ó 2018 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). 1. Introduction dozen identical copies. Their size ranges from approximately 20–40 Kb, depending upon the species, and they encode mitochon- The kinetoplast is a network of circular DNA (kDNA) inside a drial gene products (Shlomai, 2004). Maxicircles are composed of large mitochondrion. It contains the mitochondrial genome, which two regions; the first region is a coding region that contains homo- consists of thousands of interlocked DNA circles of two types, logs of mitochondrial genes characteristic of other eukaryotes maxicircles and minicircles that form a complex network (Simpson et al., 1987) and a variable non-coding region, also (Lukeš et al., 2002; Jensen and Euglund, 2012). Maxicircles com- known as the divergent region (DR). The coding region contains prise only a small portion of the kDNA network, with only a few two rRNA genes (12S rRNA and 9S rRNA), 14 protein coding genes (ND8, ND9, ND7, COIII, Cyb, ATPase6, MURF1 now known to be ND2, ND1, COII, COI, ND4, ND3, RSP12 and ND5), four genes of q Note: Nucleotide sequence data reported in this paper are available in the unknown function (MURF2, MURF5, CR3 and CR4), and a few guide GenBank database under the accession numbers MG948554, MG948555, RNAs (gRNAs) (Blom et al., 1990; Kannan and Burger, 2008; MG948556 and MG948557. ⇑ Corresponding author. Fax: +61 8 93602466. Ruvalcaba-Trejo and Sturm, 2011). Minicircles comprise the major E-mail address: [email protected] (A. Botero). portion of the kDNA network and are present in several thousand https://doi.org/10.1016/j.ijpara.2018.02.006 0020-7519/Ó 2018 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). 692 A. Botero et al. / International Journal for Parasitology 48 (2018) 691–700 copies that differ in size and sequence between species (Ray, 1998; Smith et al., 2008; Austen et al., 2009; Averis et al., 2009; 1987). They encode gRNAs that contain the genetic information McInnes et al., 2009, 2011; Paparini et al., 2011; Botero et al., for editing of mitochondrial RNA transcripts (Aphasizhev and 2013, 2016b; Thompson et al., 2013; Austen et al., 2011; Barbosa Aphasizheva, 2014). et al., 2016). Interestingly, T. copemani has been shown to invade A considerable diversity in kDNA structure and conformation cells, and has been associated with pathological changes in wildlife has been demonstrated within different kinetoplastids, including hosts that are similar to those seen with the human pathogen, parasitic trypanosomatids and free-living bodonids. A classical T. cruzi (Botero et al., 2013, 2016a). Moreover, T. copemani has been disk-shaped kDNA network has been reported in several species, found to infect numerous endangered and threatened species of including Trypanosoma cruzi, Trypanosoma brucei, Leishmania taren- wildlife, and has been associated with the drastic decline of the tolae, and Crithidia fasciculata. Minicircles within the network are critically endangered woylie (Bettongia penicillata)(Austen et al., catenated, and are released from the network through decatena- 2009; McInnes et al., 2011; Botero et al., 2013, 2016a). Despite tion by a type II DNA topoisomerase (yet to be discovered) prior the importance of the kDNA in trypanosomatid survival and to their replication (Shapiro and Englund, 1995). In contrast, the regulation of virulence (Milman et al., 2007; Singh et al., 2016), minicircles in species of more primitive kinetoplastids such as Bodo there is a complete lack of knowledge about the kinetoplast and caudatus and others from the family Bodonidae are not organised the organisation of the kDNA within this organelle in Australian in a network. Instead, they are distributed in diverse forms across trypanosomes. the mitochondrial matrix known as poly-kDNA, pan-kDNA, The aim of this study was to investigate the ultrastructure and mega-kDNA, and pro-kDNA (Vickerman, 1990; Lukeš et al., organisation of kDNA in the Australian wildlife trypanosome, 2002). Correlations between these diverse patterns of kDNA T. copemani. In particular, the organisation of the maxicircles and organisation and genetic analysis based on nuclear rRNA genes minicircles, and the presence of the UMS element and the UMSBP have contributed to a better understanding of the evolution of were investigated. kDNA and have facilitated the establishment of phylogenetic relationships between kinetoplastids (Lukeš et al., 2002). 2. Materials and methods A common feature within minicircles is the presence of a conserved region that contains three highly conserved sequence 2.1. Parasites blocks (CSBs). CSB-1 (10 bp sequence)
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