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Novel insertions in the mitochondrial maxicircle of Trypanosoma musculi, a mouse trypanosome

Published online by Cambridge University Press:  04 August 2022

Ju-Feng Wang
Affiliation:
Guangdong Provincial Key Laboratory of Aquatic Economic Animals, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, The People's Republic of China
Ruo-Hong Lin
Affiliation:
Guangdong Provincial Key Laboratory of Aquatic Economic Animals, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, The People's Republic of China
Xuan Zhang
Affiliation:
Guangdong Provincial Key Laboratory of Aquatic Economic Animals, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, The People's Republic of China
Geoff Hide
Affiliation:
Ecosystems and Environment Research Centre and Biomedical Research Centre, School of Science, Engineering and Environment, University of Salford, Salford M5 4WT, UK
Zhao-Rong Lun*
Affiliation:
Guangdong Provincial Key Laboratory of Aquatic Economic Animals, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, The People's Republic of China Ecosystems and Environment Research Centre and Biomedical Research Centre, School of Science, Engineering and Environment, University of Salford, Salford M5 4WT, UK
De-Hua Lai*
Affiliation:
Guangdong Provincial Key Laboratory of Aquatic Economic Animals, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, The People's Republic of China
*
Author for correspondence: Zhao-Rong Lun, E-mail: [email protected]; De-Hua Lai, E-mail: [email protected]
Author for correspondence: Zhao-Rong Lun, E-mail: [email protected]; De-Hua Lai, E-mail: [email protected]

Abstract

Trypanosoma musculi is a, globally distributed, mouse-specific haemoflagellate, of the family Trypanosomatidae, which shares similar characteristics in morphology with Trypanosoma lewisi. The kinetoplast (mitochondrial) DNA of Trypanosomatidae flagellates is comprised of catenated maxicircles and minicircles. However, genetic information on the T. musculi kinetoplast remains largely unknown. In this study, the T. musculi maxicircle genome was completely assembled, with PacBio and Illumina sequencing, and the size was confirmed at 34 606 bp. It consisted of 2 distinct parts: the coding region and the divergent regions (DRs, DRI and II). In comparison with other trypanosome maxicircles (Trypanosoma brucei, Trypanosoma cruzi and T. lewisi), the T. musculi maxicircle has a syntenic distribution of genes and shares 73.9, 78.0 and 92.7% sequence identity, respectively, over the whole coding region. Moreover, novel insertions in MURF2 (630 bp) and in ND5 (1278 bp) were found, respectively, which are homologous to minicircles. These findings support an evolutionary scenario similar to the one proposed for insertions in Trypanosoma cruzi, the pathogen of American trypanosomiasis. These novel insertions, together with a deletion (281 bp) in ND4, question the role of Complex I in T. musculi. A detailed analysis of DRII indicated that it contains numerous repeat motifs and palindromes, the latter of which are highly conservative and contain A5C elements. The comprehensively annotated kinetoplast maxicircle of T. musculi reveals a high degree of similarity between this parasite and the maxicircle of T. lewisi and suggests that the DRII could be a valuable marker for distinguishing these evolutionarily related species.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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Footnotes

*

Contributed equally.

References

Antipov, D, Hartwick, N, Shen, M, Raiko, M, Lapidus, A and Pevzner, PA (2016) plasmidSPAdes: assembling plasmids from whole genome sequencing data. Bioinformatics (Oxford, England) 32, 33803387.Google ScholarPubMed
Bailey, TL, Johnson, J, Grant, CE and Noble, WS (2015) The MEME suite. Nucleic Acids Research 43, W39W49.CrossRefGoogle ScholarPubMed
Baptista, CS, Vêncio, RZN, Abdala, S, Carranza, JC, Westenberger, SJ, Silva, MN, Pereira, CAdB, Galvão, LMC, Gontijo, ED, Chiari, E, Sturm, NR and Zingales, B (2006) Differential transcription profiles in Trypanosoma cruzi associated with clinical forms of Chagas disease: maxicircle NADH dehydrogenase subunit 7 gene truncation in asymptomatic patient isolates. Molecular and Biochemical Parasitology 150, 236248.CrossRefGoogle ScholarPubMed
Beattie, DS and Howton, MM (1996) The presence of rotenone-sensitive NADH dehydrogenase in the long slender bloodstream and the procyclic forms of Trypanosoma brucei brucei. European Journal of Biochemistry 241, 888894.CrossRefGoogle Scholar
Behr, MA, Mathews, SA and D'Alesandro, PA (1990) A medium for the continuous cultivation of bloodstream forms of Trypanosoma lewisi at 37°C. Journal of Parasitology 76, 711716.CrossRefGoogle Scholar
Benne, R, Van den Burg, J, Brakenhoff, JP, Sloof, P, Van Boom, JH and Tromp, MC (1986) Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46, 819826.CrossRefGoogle Scholar
Berná, L, Greif, G, Pita, S, Faral-Tello, P, Díaz-Viraqué, F, Souza, RDCMD, Vallejo, GA, Alvarez-Valin, F and Robello, C (2021) Maxicircle architecture and evolutionary insights into Trypanosoma cruzi complex. PLoS Neglected Tropical Diseases 15, e0009719.CrossRefGoogle ScholarPubMed
Blum, B and Simpson, L (1990) Guide RNAs in kinetoplastid mitochondria have a nonencoded 3′ oligo(U) tail involved in recognition of the preedited region. Cell 62, 391397.CrossRefGoogle ScholarPubMed
Bolger, AM, Lohse, M and Usadel, B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics (Oxford, England) 30, 21142120.Google ScholarPubMed
Borst, P, Fase-Fowler, F, Hoeijmakers, JH and Frasch, AC (1980) Variations in maxi-circle and mini-circle sequences in kinetoplast DNAs from different Trypanosoma brucei strains. Biochimica et Biophysica Acta (BBA) 610, 197210.CrossRefGoogle ScholarPubMed
Borst, P, Weijers, PJ and Brakenhoff, GJ (1982) Analysis by electron microscopy of the variable segment in the maxi-circle of kinetoplast DNA from Trypanosoma brucei. Biochimica et Biophysica Acta (BBA) 699, 272280.CrossRefGoogle ScholarPubMed
Bozzola, JJ (2014) Conventional specimen preparation techniques for transmission electron microscopy of cultured cells. In Kuo, J (ed.), Electron Microscopy: Methods and Protocols. Totowa, NJ: Humana Press, pp. 119.Google Scholar
Camacho, C, Coulouris, G, Avagyan, V, Ma, N, Papadopoulos, J, Bealer, K and Madden, TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10, 421.CrossRefGoogle ScholarPubMed
César Carranza, J, Kowaltowski, AJ, Mendonça, MAG, de Oliveira, TC, Gadelha, FR and Zingales, B (2009) Mitochondrial bioenergetics and redox state are unaltered in Trypanosoma cruzi isolates with compromised mitochondrial complex I subunit genes. Journal of Bioenergetics and Biomembranes 41, 299308.CrossRefGoogle Scholar
Duarte, M and Tomás, AM (2014) The mitochondrial complex I of trypanosomatids – an overview of current knowledge. Journal of Bioenergetics and Biomembranes 46, 299311.CrossRefGoogle ScholarPubMed
Flegontov, PN, Guo, Q, Ren, L, Strelkova, MV and Kolesnikov, AA (2006) Conserved repeats in the kinetoplast maxicircle divergent region of Leishmania sp. and Leptomonas seymouri. Molecular Genetics and Genomics 276, 322333.CrossRefGoogle ScholarPubMed
Gao, JM, Yi, SQ, Geng, GQ, Xu, ZS, Hide, G, Lun, ZR and Lai, DH (2021) Infection with Trypanosoma lewisi or Trypanosoma musculi may promote the spread of Toxoplasma gondii. Parasitology 148, 703711.CrossRefGoogle ScholarPubMed
Gerasimov, ES, Gasparyan, AA, Kaurov, I, Tichý, B, Logacheva, MD, Kolesnikov, AA, Lukeš, J, Yurchenko, V, Zimmer, SL and Flegontov, P (2018) Trypanosomatid mitochondrial RNA editing: dramatically complex transcript repertoires revealed with a dedicated mapping tool. Nucleic Acids Research 46, 765781.CrossRefGoogle ScholarPubMed
Gorbat, A, Maslov, DA, Peters, LS, Gaviernik, P, Viustenkhagen, T and Kolesnikov, AA (1990) Analysis of the sequence of repeats in divergent regions of maxi-circular DNA from kinetoplasts of Crithidia oncopelti. Molekuliarnaia Biologiia 24, 15391548.Google ScholarPubMed
Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hoare, CA (1972) The Trypanosomes of Mammals. A Zoological Monograph. Oxford, UK: Blackwell Scientific Publications.Google Scholar
Hong, XK, Zhang, X, Fusco, OA, Lan, YG, Lun, ZR and Lai, DH (2017) PCR-based identification of Trypanosoma lewisi and Trypanosoma musculi using maxicircle kinetoplast DNA. Acta Tropica 171, 207212.CrossRefGoogle ScholarPubMed
Kaufer, A, Stark, D and Ellis, J (2019) Evolutionary insight into the Trypanosomatidae using alignment-free phylogenomics of the kinetoplast. Pathogens (Basel, Switzerland) 8, 157.Google ScholarPubMed
Kay, C, Williams, TA and Gibson, W (2020) Mitochondrial DNAs provide insight into trypanosome phylogeny and molecular evolution. BMC Evolutionary Biology 20, 161.CrossRefGoogle ScholarPubMed
Kohl, L, Sherwin, T and Gull, K (1999) Assembly of the paraflagellar rod and the flagellum attachment zone complex during the Trypanosoma brucei cell cycle. Journal of Eukaryotic Microbiology 46, 105109.CrossRefGoogle ScholarPubMed
Koren, S, Walenz, BP, Berlin, K, Miller, JR, Bergman, NH and Phillippy, AM (2017) Canu: scalable and accurate long-read assembly via adaptive -mer weighting and repeat separation. Genome Research 27, 722736.CrossRefGoogle ScholarPubMed
Koslowsky, D, Sun, Y, Hindenach, J, Theisen, T and Lucas, J (2014) The insect-phase gRNA transcriptome in Trypanosoma brucei. Nucleic Acids Research 42, 18731886.CrossRefGoogle ScholarPubMed
Kostygov, AY, Karnkowska, A, Votýpka, J, Tashyreva, D, Maciszewski, K, Yurchenko, V and Lukeš, J (2021) Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses. Open Biology 11, 200407.CrossRefGoogle ScholarPubMed
Krampitz, HE (1969) Geographical distribution, host-parasite relationship and multiplication of Sicilian strains of Trypanosoma (Herpetosoma) duttoni Thiroux 1950 (Protozoa, Trypanosomatidae). Zeitschrift fur Parasitenkunde (Berlin, Germany) 32, 297315.Google ScholarPubMed
Krzywinski, M, Schein, J, Birol, I, Connors, J, Gascoyne, R, Horsman, D, Jones, SJ and Marra, MA (2009) Circos: an information aesthetic for comparative genomics. Genome Research 19, 16391645.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.CrossRefGoogle ScholarPubMed
Li, SJ, Zhang, X, Lukeš, J, Li, BQ, Wang, JF, Qu, LH, Hide, G, Lai, DH and Lun, ZR (2020) Novel organization of mitochondrial minicircles and guide RNAs in the zoonotic pathogen Trypanosoma lewisi. Nucleic Acids Research 48, 97479761.CrossRefGoogle ScholarPubMed
Lin, RH, Lai, DH, Zheng, LL, Wu, J, Lukeš, J, Hide, G and Lun, ZR (2015) Analysis of the mitochondrial maxicircle of Trypanosoma lewisi, a neglected human pathogen. Parasites & Vectors 8, 665.CrossRefGoogle ScholarPubMed
Lowry, JE, Leonhardt, JA, Yao, C, Belden, EL and Andrews, GP (2014) Infection of C57BL/6 mice by Trypanosoma musculi modulates host immune responses during Brucella abortus cocolonization. Journal of Wildlife Diseases 50, 1120.CrossRefGoogle ScholarPubMed
Lukes, J, Guilbride, DL, Votýpka, J, Zíková, A, Benne, R and Englund, PT (2002) Kinetoplast DNA network: evolution of an improbable structure. Eukaryotic Cell 1, 495502.CrossRefGoogle ScholarPubMed
Lukeš, J, Wheeler, R, Jirsová, D, David, V and Archibald, JM (2018) Massive mitochondrial DNA content in diplonemid and kinetoplastid protists. IUBMB Life 70, 12671274.CrossRefGoogle ScholarPubMed
Maslov, DA, Kolesnikov, AA and Zaitseva, GN (1984) Conservative and divergent base sequence regions in the maxicircle kinetoplast DNA of several trypanosomatid flagellates. Molecular and Biochemical Parasitology 12, 351364.CrossRefGoogle ScholarPubMed
Muhich, ML, Simpson, L and Simpson, AM (1983) Comparison of maxicircle DNAs of Leishmania tarentolae and Trypanosoma brucei. Proceedings of the National Academy of Sciences of the United States of America 80, 40604064.CrossRefGoogle ScholarPubMed
Myler, PJ, Glick, D, Feagin, JE, Morales, TH and Stuart, KD (1993) Structural organization of the maxicircle variable region of Trypanosoma brucei: identification of potential replication origins and topoisomerase II binding sites. Nucleic Acids Research 21, 687694.CrossRefGoogle ScholarPubMed
Nebohácová, M, Kim, CE, Simpson, L and Maslov, DA (2009) RNA editing and mitochondrial activity in promastigotes and amastigotes of Leishmania Donovani. International Journal for Parasitology 39, 635644.CrossRefGoogle ScholarPubMed
Noé, L and Kucherov, G (2005) YASS: enhancing the sensitivity of DNA similarity search. Nucleic Acids Research 33, W540W543.CrossRefGoogle ScholarPubMed
Nzoumbou-Boko, R, De Muylder, G, Semballa, S, Lecordier, L, Dauchy, FA, Gobert, AP, Holzmuller, P, Lemesre, JL, Bras-Gonçalves, R, Barnabé, C, Courtois, P, Daulouède, S, Beschin, A, Pays, E and Vincendeau, P (2017) Trypanosoma musculi infection in mice critically relies on mannose receptor-mediated arginase induction by a TbKHC1 kinesin H chain homolog. Journal of Immunology 199, 17621771.CrossRefGoogle ScholarPubMed
Opperdoes, FR and Michels, PAM (2008) Complex I of Trypanosomatidae: does it exist? Trends in Parasitology 24, 310317.CrossRefGoogle ScholarPubMed
Pérez-Morga, D and Englund, PT (1993) The structure of replicating kinetoplast DNA networks. Journal of Cell Biology 123, 10691079.CrossRefGoogle ScholarPubMed
Ray, DS (1989) Conserved sequence blocks in kinetoplast minicircles from diverse species of trypanosomes. Molecular and Cellular Biology 9, 13651367.Google ScholarPubMed
Ryan, KA, Shapiro, TA, Rauch, CA and Englund, PT (1988) Replication of kinetoplast DNA in trypanosomes. Annual Review of Microbiology 42, 339358.CrossRefGoogle ScholarPubMed
Sarataphan, N, Vongpakorn, M, Nuansrichay, B, Autarkool, N, Keowkarnkah, T, Rodtian, P, Stich, RW and Jittapalapong, S (2007) Diagnosis of a Trypanosoma lewisi-like (Herpetosoma) infection in a sick infant from Thailand. Journal of Medical Microbiology 56, 11181121.CrossRefGoogle Scholar
Sievers, F, Wilm, A, Dineen, D, Gibson, TJ, Karplus, K, Li, W, Lopez, R, McWilliam, H, Remmert, M, Söding, J, Thompson, JD and Higgins, DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology 7, 539.CrossRefGoogle ScholarPubMed
Simpson, L, Neckelmann, N, de la Cruz, VF, Simpson, AM, Feagin, JE, Jasmer, DP and Stuart, K (1987) Comparison of the maxicircle (mitochondrial) genomes of Leishmania tarentolae and Trypanosoma brucei at the level of nucleotide sequence. Journal of Biological Chemistry 262, 61826196.CrossRefGoogle ScholarPubMed
Simpson, L, Douglass, SM, Lake, JA, Pellegrini, M and Li, F (2015) Comparison of the mitochondrial genomes and steady state transcriptomes of two strains of the trypanosomatid parasite, Leishmania tarentolae. PLoS Neglected Tropical Diseases 9, e0003841.CrossRefGoogle ScholarPubMed
Sloof, P, de Haan, A, Eier, W, van Iersel, M, Boel, E, van Steeg, H and Benne, R (1992) The nucleotide sequence of the variable region in Trypanosoma brucei completes the sequence analysis of the maxicircle component of mitochondrial kinetoplast DNA. Molecular and Biochemical Parasitology 56, 289299.CrossRefGoogle ScholarPubMed
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 13121313.Google ScholarPubMed
Stuart, KD and Gelvin, SB (1982) Localization of kinetoplast DNA maxicircle transcripts in bloodstream and procyclic form Trypanosoma brucei. Molecular and Cellular Biology 2, 845852.Google ScholarPubMed
Stuart, K, Allen, TE, Heidmann, S and Seiwert, SD (1997) RNA editing in kinetoplastid protozoa. Microbiology and Molecular Biology Reviews 61, 105120.Google ScholarPubMed
Stuart, KD, Schnaufer, A, Ernst, NL and Panigrahi, AK (2005) Complex management: RNA editing in trypanosomes. Trends in Biochemical Sciences 30, 97105.CrossRefGoogle ScholarPubMed
Surve, S, Heestand, M, Panicucci, B, Schnaufer, A and Parsons, M (2012) Enigmatic presence of mitochondrial complex I in Trypanosoma brucei bloodstream forms. Eukaryotic Cell 11, 183193.CrossRefGoogle ScholarPubMed
Talavera, G and Castresana, J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564577.CrossRefGoogle ScholarPubMed
Vasil'eva, MA, Bessolitsina, EA, Merzlyak, EM and Kolesnikov, AA (2004) Identification of the 12S rRNA gene promoter in Leptomonas seymouri mitochondrial DNA. Molecular Biology 38, 839843.CrossRefGoogle ScholarPubMed
Vaux, R, Schnoeller, C, Berkachy, R, Roberts, LB, Hagen, J, Gounaris, K and Selkirk, ME (2016) Modulation of the immune response by nematode secreted acetylcholinesterase revealed by heterologous expression in Trypanosoma musculi. PLoS Pathogens 12, e1005998.CrossRefGoogle ScholarPubMed
Verma, A, Manchanda, S, Kumar, N, Sharma, A, Goel, M, Banerjee, PS, Garg, R, Singh, BP, Balharbi, F, Lejon, V, Deborggraeve, S, Singh Rana, UV and Puliyel, J (2011) Trypanosoma lewisi or T. lewisi-like infection in a 37-day-old Indian infant. American Journal of Tropical Medicine and Hygiene 85, 221224.CrossRefGoogle ScholarPubMed
Verner, Z, Čermáková, P, Škodová, I, Kriegová, E, Horváth, A and Lukeš, J (2011) Complex I (NADH:ubiquinone oxidoreductase) is active in but non-essential for procyclic Trypanosoma brucei. Molecular and Biochemical Parasitology 175, 196200.CrossRefGoogle ScholarPubMed
Wadkins, RM (2000) Targeting DNA secondary structures. Current Medicinal Chemistry 7, 115.CrossRefGoogle ScholarPubMed
Walker, BJ, Abeel, T, Shea, T, Priest, M, Abouelliel, A, Sakthikumar, S, Cuomo, CA, Zeng, Q, Wortman, J, Young, SK and Earl, AM (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PloS One 9, e112963.CrossRefGoogle ScholarPubMed
Westenberger, SJ, Cerqueira, GC, El-Sayed, NM, Zingales, B, Campbell, DA and Sturm, NR (2006) Trypanosoma cruzi mitochondrial maxicircles display species- and strain-specific variation and a conserved element in the non-coding region. BMC Genomics 7, 60.CrossRefGoogle Scholar
Zhang, X, Hong, XK, Li, SJ, Lai, DH, Hide, G, Lun, ZR and Wen, YZ (2018) The effect of normal human serum on the mouse trypanosome Trypanosoma musculi in vitro and in vivo. Experimental Parasitology 184, 115120.CrossRefGoogle ScholarPubMed
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