https://eutils.ncbi.nlm.nih.gov/entrez/eutils/efetch.fcgi?db=pubmed&id=33660779&retmode=xml&tool=Litmetric&email=readroberts32@gmail.com&api_key=61f08fa0b96a73de8c900d749fcb997acc09 336607792021051220240221
1362-49624962021Apr06Nucleic acids researchNucleic Acids ResComplete minicircle genome of Leptomonas pyrrhocoris reveals sources of its non-canonical mitochondrial RNA editing events.335433703354-337010.1093/nar/gkab114Uridine insertion/deletion (U-indel) editing of mitochondrial mRNA, unique to the protistan class Kinetoplastea, generates canonical as well as potentially non-productive editing events. While the molecular machinery and the role of the guide (g) RNAs that provide required information for U-indel editing are well understood, little is known about the forces underlying its apparently error-prone nature. Analysis of a gRNA:mRNA pair allows the dissection of editing events in a given position of a given mitochondrial transcript. A complete gRNA dataset, paired with a fully characterized mRNA population that includes non-canonically edited transcripts, would allow such an analysis to be performed globally across the mitochondrial transcriptome. To achieve this, we have assembled 67 minicircles of the insect parasite Leptomonas pyrrhocoris, with each minicircle typically encoding one gRNA located in one of two similar-sized units of different origin. From this relatively narrow set of annotated gRNAs, we have dissected all identified mitochondrial editing events in L. pyrrhocoris, the strains of which dramatically differ in the abundance of individual minicircle classes. Our results support a model in which a multitude of editing events are driven by a limited set of gRNAs, with individual gRNAs possessing an inherent ability to guide canonical and non-canonical editing.© The Author(s) 2021. Published by Oxford University Press on behalf of Nucleic Acids Research.GerasimovEvgeny SESFaculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia.Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov University, Moscow 119435, Russia.Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow 127051, Russia.GasparyanAnna AAAFaculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia.AfoninDmitry ADAFaculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia.ZimmerSara LSLDepartment of Biomedical Sciences, University of Minnesota Medical School, Duluth Campus, Duluth, MN 55812, USA.KraevaNatalyaNLife Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic.LukešJuliusJInstitute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice (Budweis), Czech Republic.Faculty of Science, University of South Bohemia, 370 05 České Budějovice (Budweis), Czech Republic.YurchenkoVyacheslavVMartsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov University, Moscow 119435, Russia.Life Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic.KolesnikovAlexanderAFaculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia.engJournal ArticleResearch Support, Non-U.S. Gov't
EnglandNucleic Acids Res04110110305-10480RNA, Messenger0RNA, MitochondrialIMGenome, ProtozoanPhylogenyRNA EditingRNA, MessengermetabolismRNA, MitochondrialmetabolismTranscriptomeTrypanosomatinageneticsmetabolismRNA, Guide, CRISPR-Cas Systems
2021292021232020816202135602021513602021348402021228ppublish33660779PMC803462910.1093/nar/gkab1146154491Reiter N.J., Osterman A., Torres-Larios A., Swinger K.K., Pan T., Mondragon A.. Structure of a bacterial ribonuclease P holoenzyme in complex with tRNA. Nature. 2010; 468:784–789.PMC305890821076397Sanford J.R., Caceres J.F.. Pre-mRNA splicing: life at the centre of the central dogma. J. Cell Sci. 2004; 117:6261–6263.15591240Shi Y. Mechanistic insights into precursor messenger RNA splicing by the spliceosome. Nat. Rev. Mol. Cell Biol. 2017; 18:655–670.28951565Lukeš J., Kaur B., Speijer D.. RNA editing in mitochondria and plastids: weird and widespread. Trends Genet. 2021; 37:99–102.33203574Kaur B., Záhonová K., Valach M., Faktorová D., Prokopchuk G., Burger G., Lukeš J.. Gene fragmentation and RNA editing without borders: eccentric mitochondrial genomes of diplonemids. Nucleic Acids Res. 2020; 48:2694–2708.PMC704970031919519Lukeš J., Butenko A., Hashimi H., Maslov D.A., Votýpka J., Yurchenko V.. Trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. Trends Parasitol. 2018; 34:466–480.29605546Jensen R.E., Englund P.T.. Network news: the replication of kinetoplast DNA. Annu. Rev. Microbiol. 2012; 66:473–491.22994497Lukeš J., Guilbride D.L., Votýpka J., Zíková A., Benne R., Englund P.T.. Kinetoplast DNA network: evolution of an improbable structure. Eukaryot. Cell. 2002; 1:495–502.PMC11799912455998Shlomai J. The structure and replication of kinetoplast DNA. Curr. Mol. Med. 2004; 4:623–647.15357213Read L.K., Lukeš J., Hashimi H.. Trypanosome RNA editing: the complexity of getting U in and taking U out. Wiley Interdiscip. Rev. RNA. 2016; 7:33–51.PMC483569226522170Maslov D.A., Opperdoes F.R., Kostygov A.Y., Hashimi H., Lukeš J., Yurchenko V.. Recent advances in trypanosomatid research: genome organization, expression, metabolism, taxonomy and evolution. Parasitology. 2019; 146:1–27.29898792Sturm N.R., Simpson L.. Kinetoplast DNA minicircles encode guide RNAs for editing of cytochrome oxidase subunit III mRNA. Cell. 1990; 61:879–884.1693097Cruz-Reyes J., Mooers B.H.M., Doharey P.K., Meehan J., Gulati S. Dynamic RNA holo-editosomes with subcomplex variants: Insights into the control of trypanosome editing. Wiley Interdiscip. Rev. RNA. 2018; 9:e1502.PMC618580130101566Aphasizheva I., Alfonzo J., Carnes J., Cestari I., Cruz-Reyes J., Goringer H.U., Hajduk S., Lukeš J., Madison-Antenucci S., Maslov D.A.et al. .. Lexis and grammar of mitochondrial RNA processing in trypanosomes. Trends Parasitol. 2020; 36:337–355.PMC708377132191849Zimmer S.L., Simpson R.M., Read L.K.. High throughput sequencing revolution reveals conserved fundamentals of U-indel editing. Wiley Interdiscip. Rev. RNA. 2018; 9:e1487.PMC628988329888550Koslowsky D.J., Bhat G.J., Read L.K., Stuart K.. Cycles of progressive realignment of gRNA with mRNA in RNA editing. Cell. 1991; 67:537–546.1718605Ammerman M.L., Presnyak V., Fisk J.C., Foda B.M., Read L.K.. TbRGG2 facilitates kinetoplastid RNA editing initiation and progression past intrinsic pause sites. RNA. 2010; 16:2239–2251.PMC295706220855539Simpson R.M., Bruno A.E., Bard J.E., Buck M.J., Read L.K.. High-throughput sequencing of partially edited trypanosome mRNAs reveals barriers to editing progression and evidence for alternative editing. RNA. 2016; 22:677–695.PMC483664326908922Gerasimov E.S., Gasparyan A.A., Kaurov I., Tichý B., Logacheva M.D., Kolesnikov A.A., Lukeš J., Yurchenko V., Zimmer S.L., Flegontov P.. Trypanosomatid mitochondrial RNA editing: dramatically complex transcript repertoires revealed with a dedicated mapping tool. Nucleic Acids Res. 2018; 46:765–781.PMC577846029220521David V., Flegontov P., Gerasimov E., Tanifuji G., Hashimi H., Logacheva M.D., Maruyama S., Onodera N.T., Gray M.W., Archibald J.M.et al. .. Gene loss and error-prone RNA editing in the mitochondrion of Perkinsela, an endosymbiotic kinetoplastid. mBio. 2015; 6:e01498-15.PMC466938126628723Maslov D.A., Simpson L.. The polarity of editing within a multiple gRNA-mediated domain is due to formation of anchors for upstream gRNAs by downstream editing. Cell. 1992; 70:459–467.1379519Aravin A.A., Yurchenko V., Merzlyak E., Kolesnikov A.A.. The mitochondrial ND8 gene from Crithidia oncopelti is not pan-edited. FEBS Lett. 1998; 431:457–460.9714563Gerasimov E.S., Kostygov A.Y., Yan S., Kolesnikov A.A.. From cryptogene to gene? ND8 editing domain reduction in insect trypanosomatids. Eur. J. Protistol. 2012; 48:185–193.22014411Cooper S., Wadsworth E.S., Ochsenreiter T., Ivens A., Savill N.J., Schnaufer A.. Assembly and annotation of the mitochondrial minicircle genome of a differentiation-competent strain of Trypanosoma brucei. Nucleic Acids Res. 2019; 47:11304–11325.PMC686843931665448Simpson L., Douglass S.M., Lake J.A., Pellegrini M., Li F.. Comparison of the mitochondrial genomes and steady state transcriptomes of two strains of the trypanosomatid parasite, Leishmania tarentolae. PLoS Negl. Trop. Dis. 2015; 9:e0003841.PMC451269326204118Camacho E., Rastrojo A., Sanchiz A., Gonzalez-de la Fuente S., Aguado B., Requena J.M.. Leishmania mitochondrial genomes: maxicircle structure and heterogeneity of minicircles. Genes (Basel). 2019; 10:758.PMC682640131561572Yurchenko V., Kolesnikov A.A.. Minicircular kinetoplast DNA of Trypanosomatidae. Mol. Biol. (Mosk). 2001; 35:3–13.11234380Yurchenko V., Hobza R., Benada O., Lukeš J.. Trypanosoma avium: large minicircles in the kinetoplast DNA. Exp. Parasitol. 1999; 92:215–218.10403763Li S.J., Zhang X., Lukeš J., Li B.Q., Wang J.F., Qu L.H., Hide G., Lai D.H., Lun Z.R.. Novel organization of mitochondrial minicircles and guide RNAs in the zoonotic pathogen Trypanosoma lewisi. Nucleic Acids Res. 2020; 48:9747–9761.PMC751571232853372Blum B., Bakalara N., Simpson L.. A model for RNA editing in kinetoplastid mitochondria: “guide” RNA molecules transcribed from maxicircle DNA provide the edited information. Cell. 1990; 60:189–198.1688737Tylec B.L., Simpson R.M., Kirby L.E., Chen R., Sun Y., Koslowsky D.J., Read L.K.. Intrinsic and regulated properties of minimally edited trypanosome mRNAs. Nucleic Acids Res. 2019; 47:3640–3657.PMC646816530698753Carnes J., McDermott S., Anupama A., Oliver B.G., Sather D.N., Stuart K.. In vivo cleavage specificity of Trypanosoma brucei editosome endonucleases. Nucleic Acids Res. 2017; 45:4667–4686.PMC541683728334821Simpson R.M., Bruno A.E., Chen R., Lott K., Tylec B.L., Bard J.E., Sun Y., Buck M.J., Read L.K.. Trypanosome RNA Editing Mediator Complex proteins have distinct functions in gRNA utilization. Nucleic Acids Res. 2017; 45:7965–7983.PMC573752928535252Kirby L.E., Koslowsky D. Cell-line specific RNA editing patterns in Trypanosoma brucei suggest a unique mechanism to generate protein variation in a system intolerant to genetic mutations. Nucleic Acids Res. 2020; 48:1479–1493.PMC702663831840176Flegontov P., Butenko A., Firsov S., Kraeva N., Eliáš M., Field M.C., Filatov D., Flegontova O., Gerasimov E.S., Hlaváčová J.et al. .. Genome of Leptomonas pyrrhocoris: a high-quality reference for monoxenous trypanosomatids and new insights into evolution of Leishmania. Sci. Rep. 2016; 6:23704.PMC481037027021793Gerasimov E.S., Gasparyan A.A., Litus I.A., Logacheva M.D., Kolesnikov A.A.. Minicircle kinetoplast genome of insect trypanosomatidLeptomonas pyrrhocoris. Biochemistry (Mosc). 2017; 82:572–578.28601067Bolger A.M., Lohse M., Usadel B.. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30:2114–2120.PMC410359024695404Bushnell B., Rood J., Singer E.. BBMerge - accurate paired shotgun read merging via overlap. PLoS One. 2017; 12:e0185056.PMC565762229073143Ray D.S. Conserved sequence blocks in kinetoplast minicircles from diverse species of trypanosomes. Mol. Cell. Biol. 1989; 9:1365–1367.PMC3627342542768Langmead B., Salzberg S.L.. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 2012; 9:357–359.PMC332238122388286Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R.Genome Project Data Processing, S. . The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009; 25:2078–2079.PMC272300219505943Li W., Godzik A.. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006; 22:1658–1659.16731699Kraeva N., Butenko A., Hlaváčová J., Kostygov A., Myškova J., Grybchuk D., Leštinová T., Votýpka J., Volf P., Opperdoes F.et al. .. Leptomonas seymouri: adaptations to the dixenous life cycle analyzed by genome sequencing, transcriptome profiling and co-infection with Leishmania donovani. PLoS Pathog. 2015; 11:e1005127.PMC455278626317207Bankevich A., Nurk S., Antipov D., Gurevich A.A., Dvorkin M., Kulikov A.S., Lesin V.M., Nikolenko S.I., Pham S., Prjibelski A.D.et al. .. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 2012; 19:455–477.PMC334251922506599Bailey T.L., Boden M., Buske F.A., Frith M., Grant C.E., Clementi L., Ren J., Li W.W., Noble W.S.. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009; 37:W202–W208.PMC270389219458158Gerasimov E.S., Zamyatnina K.A., Matveeva N.S., Rudenskaya Y.A., Kraeva N., Kolesnikov A.A., Yurchenko V.. Common structural patterns in the maxicircle divergent region of Trypanosomatidae. Pathogens. 2020; 9:100.PMC716941332033466Kolpakov R., Bana G., Kucherov G.. Mreps: efficient and flexible detection of tandem repeats in DNA. Nucleic Acids Res. 2003; 31:3672–3678.PMC16919612824391Rice P., Longden I., Bleasby A.. EMBOSS: the European molecular biology open software suite. Trends Genet. 2000; 16:276–277.10827456Noé L., Kucherov G.. YASS: enhancing the sensitivity of DNA similarity search. Nucleic Acids Res. 2005; 33:W540–W543.PMC116023815980530Kurtz S., Phillippy A., Delcher A.L., Smoot M., Shumway M., Antonescu C., Salzberg S.L.. Versatile and open software for comparing large genomes. Genome Biol. 2004; 5:R12.PMC39575014759262Huerta-Cepas J., Serra F., Bork P.. ETE 3: reconstruction, analysis, and visualization of phylogenomic data. Mol. Biol. Evol. 2016; 33:1635–1638.PMC486811626921390Sievers F., Wilm A., Dineen D., Gibson T.J., Karplus K., Li W., Lopez R., McWilliam H., Remmert M., Soding J.et al. .. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 2011; 7:539.PMC326169921988835Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014; 30:1312–1313.PMC399814424451623Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J.. Basic local alignment search tool. J. Mol. Biol. 1990; 215:403–410.2231712Kostygov A., Dobáková E., Grybchuk-Ieremenko A., Váhala D., Maslov D.A., Votýpka J., Lukeš J., Yurchenko V.. Novel trypanosomatid - bacterium association: evolution of endosymbiosis in action. mBio. 2016; 7:e01985-15.PMC480736826980834Maslov D.A. Complete set of mitochondrial pan-edited mRNAs inLeishmania mexicana amazonensis LV78. Mol. Biochem. Parasitol. 2010; 173:107–114.PMC291360920546801Koslowsky D., Sun Y., Hindenach J., Theisen T., Lucas J.. The insect-phase gRNA transcriptome in Trypanosoma brucei. Nucleic Acids Res. 2014; 42:1873–1886.PMC391958724174546Yasuhira S., Simpson L.. Minicircle-encoded guide RNAs from Crithidia fasciculata. RNA. 1995; 1:634–643.PMC13693077489522Yurchenko V., Merzlyak E.M., Kolesnikov A.A., Martinkina L.P., Vengerov Y.Y.. Structure of Leishmania minicircle kinetoplast DNA classes. J. Clin. Microbiol. 1999; 37:1656–1657.PMC8487110328690Kostygov A.Y., Yurchenko V.. Revised classification of the subfamily Leishmaniinae (Trypanosomatidae). Folia Parasitol. 2017; 64:020.28783029Maruyama S.R., de Santana A.K.M., Takamiya N.T., Takahashi T.Y., Rogerio L.A., Oliveira C.A.B., Milanezi C.M., Trombela V.A., Cruz A.K., Jesus A.R.et al. .. Non-Leishmania parasite in fatal visceral leishmaniasis–like disease, Brazil. Emerg. Infect. Dis. 2019; 25:2088–2092.PMC681019231625841Yurchenko V., Kolesnikov A.A., Lukeš J.. Phylogenetic analysis of Trypanosomatina (Protozoa: Kinetoplastida) based on minicircle conserved regions. Folia Parasitol. 2000; 47:1–5.10833008Clement S.L., Mingler M.K., Koslowsky D.J.. An intragenic guide RNA location suggests a complex mechanism for mitochondrial gene expression in Trypanosoma brucei. Eukaryot. Cell. 2004; 3:862–869.PMC50088515302819van der Spek H., Arts G.J., Zwaal R.R., van den Burg J., Sloof P., Benne R.. Conserved genes encode guide RNAs in mitochondria of Crithidia fasciculata. EMBO J. 1991; 10:1217–1224.PMC4527761708723Sturm N.R., Maslov D.A., Blum B., Simpson L.. Generation of unexpected editing patterns inLeishmania tarentolae mitochondrial mRNAs: misediting produced by misguiding. Cell. 1992; 70:469–476.1379520Decker C.J., Sollner-Webb B.. RNA editing involves indiscriminate U changes throughout precisely defined editing domains. Cell. 1990; 61:1001–1011.1693545Ochsenreiter T., Cipriano M., Hajduk S.L.. Alternative mRNA editing in trypanosomes is extensive and may contribute to mitochondrial protein diversity. PLoS One. 2008; 3:e1566.PMC221577318270563Read L.K., Wilson K.D., Myler P.J., Stuart K.. Editing of Trypanosoma brucei maxicircle CR5 mRNA generates variable carboxy terminal predicted protein sequences. Nucleic Acids Res. 1994; 22:1489–1495.PMC3080107514788Lukeš J., Archibald J.M., Keeling P.J., Doolittle W.F., Gray M.W.. How a neutral evolutionary ratchet can build cellular complexity. IUBMB Life. 2011; 63:528–537.21698757Pollard V.W., Rohrer S.P., Michelotti E.F., Hancock K., Hajduk S.L.. Organization of minicircle genes for guide RNAs in Trypanosoma brucei. Cell. 1990; 63:783–790.2171782Suematsu T., Zhang L., Aphasizheva I., Monti S., Huang L., Wang Q., Costello C.E., Aphasizhev R.. Antisense transcripts delimit exonucleolytic activity of the mitochondrial 3′ processome to generate guide RNAs. Mol. Cell. 2016; 61:364–378.PMC474411826833087Simpson L., Thiemann O.H., Savill N.J., Alfonzo J.D., Maslov D.A.. Evolution of RNA editing in trypanosome mitochondria. Proc. Natl. Acad. Sci. USA. 2000; 97:6986–6993.PMC3437410860961Savill N.J., Higgs P.G.. A theoretical study of random segregation of minicircles in trypanosomatids. Proc. R Soc. Lond. [Biol.]. 1999; 266:611–620.PMC168981010212451