{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T06:05:29Z","timestamp":1791266729971,"version":"4.1.0"},"reference-count":38,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,4,21]],"date-time":"2020-04-21T00:00:00Z","timestamp":1587427200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2020,4,21]],"date-time":"2020-04-21T00:00:00Z","timestamp":1587427200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Parasites Vectors"],"published-print":{"date-parts":[[2020,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n<jats:title>Background<\/jats:title>\n<jats:p><jats:italic>Babesia gibsoni<\/jats:italic> is an apicomplexan parasite transmitted by ticks, which can infect canine species and cause babesiosis. The apicoplast is an organelle associated with isoprenoids metabolism, is widely present in apicomplexan parasites, except for <jats:italic>Cryptosporidium<\/jats:italic>. Available data indicate that the apicoplast is essential for the survival of apicomplexan parasites.<\/jats:p>\n<\/jats:sec><jats:sec>\n<jats:title>Methods<\/jats:title>\n<jats:p>Here, the apicoplast genome of <jats:italic>B. gibsoni<\/jats:italic> was investigated by high-throughput genome sequencing, bioinformatics analysis, and conventional PCR.<\/jats:p>\n<\/jats:sec><jats:sec>\n<jats:title>Results<\/jats:title>\n<jats:p>The apicoplast genome of <jats:italic>B. gibsoni<\/jats:italic>-Wuhan strain (<jats:italic>B. gibsoni<\/jats:italic>-WH) consists of a 28.4 kb circular molecule, with A\u2009+\u2009T content of 86.33%, similar to that of <jats:italic>B. microti<\/jats:italic>. Specifically, this genome encodes genes involved in maintenance of the apicoplast DNA, transcription, translation and maturation of organellar proteins, which contains 2 subunits of ribosomal RNAs, 17 ribosomal proteins, 1 EF-Tu elongation factor (tufA), 5 DNA-dependent RNA polymerase beta subunits, 2 Clp protease chaperones, 23 tRNA genes and 5 unknown open reading frames (hypothetical proteins). Phylogenetic analysis revealed high similarity of <jats:italic>B. gibsoni<\/jats:italic> apicoplast genome to that of <jats:italic>B. orientalis<\/jats:italic> and <jats:italic>B. bovis<\/jats:italic>.<\/jats:p>\n<\/jats:sec><jats:sec>\n<jats:title>Conclusions<\/jats:title>\n<jats:p>To our knowledge, this is the first report of annotation and characterization of <jats:italic>B. gibsoni<\/jats:italic>-WH apicoplast genome. The results will facilitate the development of new anti-<jats:italic>Babesia<\/jats:italic> drug targets.<\/jats:p>\n<\/jats:sec>","DOI":"10.1186\/s13071-020-04065-7","type":"journal-article","created":{"date-parts":[[2020,4,21]],"date-time":"2020-04-21T18:02:37Z","timestamp":1587492157000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Annotation and characterization of Babesia gibsoni apicoplast genome"],"prefix":"10.1186","volume":"13","author":[{"given":"Qin","family":"Liu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Long","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fan","family":"Jiang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Muxiao","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xueyan","family":"Zhan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuan","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sen","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoyong","family":"Du","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lan","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junlong","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,4,21]]},"reference":[{"key":"4065_CR1","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1016\/j.meegid.2016.03.025","volume":"41","author":"MN Singh","year":"2016","unstructured":"Singh MN, Raina OK, Sankar M, Rialch A, Tigga MN, Kumar GR, et al. Molecular detection and genetic diversity of Babesia gibsoni in dogs in India. Infect Genet Evol. 2016;41:100\u20136.","journal-title":"Infect Genet Evol."},{"key":"4065_CR2","doi-asserted-by":"publisher","first-page":"1501","DOI":"10.1016\/S0020-7519(00)00120-X","volume":"30","author":"AM Kjemtrup","year":"2000","unstructured":"Kjemtrup AM, Kocan AA, Whitworth L, Meinkoth J, Birkenheuer AJ, Cummings J, et al. There are at least three genetically distinct small piroplasms from dogs. Int J Parasitol. 2000;30:1501\u20135.","journal-title":"Int J Parasitol."},{"key":"4065_CR3","doi-asserted-by":"publisher","first-page":"1141","DOI":"10.1016\/j.cvsm.2010.08.001","volume":"40","author":"PJ Irwin","year":"2010","unstructured":"Irwin PJ. Canine babesiosis. Vet Clin North Am Small Anim Pract. 2010;40:1141\u201356.","journal-title":"Vet Clin North Am Small Anim Pract."},{"key":"4065_CR4","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1136\/vr.142.7.168","volume":"142","author":"R Casapulla","year":"1998","unstructured":"Casapulla R, Baldi L, Avallone V, Sannino R, Pazzanese L, Mizzoni V. Canine piroplasmosis due to Babesia gibsoni: clinical and morphological aspects. Vet Rec. 1998;142:168\u20139.","journal-title":"Vet Rec."},{"key":"4065_CR5","doi-asserted-by":"publisher","first-page":"692","DOI":"10.2307\/3284248","volume":"83","author":"EJ Wozniak","year":"1997","unstructured":"Wozniak EJ, Barr BC, Thomford JW, Yamane I, McDonough SP, Moore PF, et al. Clinical, anatomic, and immunopathologic characterization of Babesia gibsoni infection in the domestic dog (Canis familiaris). J Parasitol. 1997;83:692\u20139.","journal-title":"J Parasitol."},{"key":"4065_CR6","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1016\/S0304-4017(97)00149-0","volume":"74","author":"G Baneth","year":"1998","unstructured":"Baneth G, Breitschwerdt EB, Hegarty BC, Pappalardo B, Ryan J. A survey of tick-borne bacteria and protozoa in naturally exposed dogs from Israel. Vet Parasitol. 1998;74:133\u201342.","journal-title":"Vet Parasitol."},{"issue":"959\u201363","key":"4065_CR7","first-page":"52","volume":"222","author":"JR Stegeman","year":"2003","unstructured":"Stegeman JR, Birkenheuer AJ, Kruger JM, Breitschwerdt EB. Transfusion-associated Babesia gibsoni infection in a dog. J Am Vet Med Assoc. 2003;222(959\u201363):52.","journal-title":"J Am Vet Med Assoc."},{"key":"4065_CR8","doi-asserted-by":"publisher","first-page":"942","DOI":"10.2460\/javma.2005.227.942","volume":"227","author":"AJ Birkenheuer","year":"2005","unstructured":"Birkenheuer AJ, Correa MT, Levy MG, Breitschwerdt EB. Geographic distribution of babesiosis among dogs in the United States and association with dog bites: 150 cases (2000\u20132003). J Am Vet Med Assoc. 2005;227:942\u20137.","journal-title":"J Am Vet Med Assoc."},{"key":"4065_CR9","doi-asserted-by":"publisher","first-page":"1031","DOI":"10.1016\/j.ijpara.2005.03.018","volume":"35","author":"S Fukumoto","year":"2005","unstructured":"Fukumoto S, Suzuki H, Igarashi I, Xuan X. Fatal experimental transplacental Babesia gibsoni infections in dogs. Int J Parasitol. 2005;35:1031\u20135.","journal-title":"Int J Parasitol."},{"key":"4065_CR10","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1016\/j.parint.2014.10.005","volume":"64","author":"N Arisue","year":"2015","unstructured":"Arisue N, Hashimoto T. Phylogeny and evolution of apicoplasts and apicomplexan parasites. Parasitol Int. 2015;64:254\u20139.","journal-title":"Parasitol Int."},{"key":"4065_CR11","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1016\/S0022-5193(05)80718-0","volume":"158","author":"CJ Howe","year":"1992","unstructured":"Howe CJ. Plastid origin of an extrachromosomal DNA molecule from Plasmodium, the causative agent of malaria. J Theor Biol. 1992;158:199\u2013205.","journal-title":"J Theor Biol."},{"key":"4065_CR12","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1006\/jmbi.1996.0449","volume":"261","author":"RJ Wilson","year":"1996","unstructured":"Wilson RJ, Denny PW, Preiser PR, Rangachari K, Roberts K, Roy A, et al. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol. 1996;261:155\u201372.","journal-title":"J Mol Biol."},{"key":"4065_CR13","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/S0074-7696(05)24003-2","volume":"224","author":"BJ Foth","year":"2003","unstructured":"Foth BJ, McFadden GI. The apicoplast: a plastid in Plasmodium falciparum and other Apicomplexan parasites. Int Rev Cytol. 2003;224:57\u2013110.","journal-title":"Int Rev Cytol."},{"key":"4065_CR14","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1016\/S1360-1385(01)01921-5","volume":"6","author":"E Marechal","year":"2001","unstructured":"Marechal E, Cesbron-Delauw MF. The apicoplast: a new member of the plastid family. Trends Plant Sci. 2001;6:200\u20135.","journal-title":"Trends Plant Sci."},{"key":"4065_CR15","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1016\/0166-6851(91)90227-W","volume":"44","author":"MJ Gardner","year":"1991","unstructured":"Gardner MJ, Williamson DH, Wilson RJM. A circular DNA in malaria marasites encodes an RNA polymerase like that of prokaryotes and chloroplasts. Mol Biochem Parasitol. 1991;44:115\u201323.","journal-title":"Mol Biochem Parasitol."},{"key":"4065_CR16","doi-asserted-by":"publisher","first-page":"641","DOI":"10.1007\/s00709-010-0250-5","volume":"248","author":"GI McFadden","year":"2011","unstructured":"McFadden GI. The apicoplast. Protoplasma. 2011;248:641\u201350.","journal-title":"Protoplasma."},{"key":"4065_CR17","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1038\/nature01097","volume":"419","author":"MJ Gardner","year":"2002","unstructured":"Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature. 2002;419:498\u2013511.","journal-title":"Nature."},{"key":"4065_CR18","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1098\/rstb.2001.1047","volume":"357","author":"DS Roos","year":"2002","unstructured":"Roos DS, Crawford MJ, Donald RGK, Fraunholz M, Harb OS, He CY, et al. Mining the Plasmodium genome database to define organellar function: what does the apicoplast do? Philos Trans R Soc Lond B Biol Sci. 2002;357:35\u201346.","journal-title":"Philos Trans R Soc Lond B Biol Sci."},{"key":"4065_CR19","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1078\/1434461000169","volume":"155","author":"S Sato","year":"2004","unstructured":"Sato S, Clough B, Coates L, Wilson RJM. Enzymes for heme biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum. Protist. 2004;155:117\u201325.","journal-title":"Protist."},{"key":"4065_CR20","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/j.1365-2958.2004.04314.x","volume":"55","author":"SA Ralph","year":"2005","unstructured":"Ralph SA. Strange organelles - Plasmodium mitochondria lack a pyruvate dehydrogenase complex. Mol Microbiol. 2005;55:1\u20134.","journal-title":"Mol Microbiol."},{"key":"4065_CR21","doi-asserted-by":"publisher","first-page":"e1001138","DOI":"10.1371\/journal.pbio.1001138","volume":"9","author":"E Yeh","year":"2011","unstructured":"Yeh E, DeRisi JL. Chemical rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum. PLoS Biol. 2011;9:e1001138.","journal-title":"PLoS Biol."},{"key":"4065_CR22","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1186\/s13071-015-1158-x","volume":"8","author":"Y Huang","year":"2015","unstructured":"Huang Y, He L, Hu J, He P, He J, Yu L, et al. Characterization and annotation of Babesia orientalis apicoplast genome. Parasit Vectors. 2015;8:543.","journal-title":"Parasit Vectors."},{"key":"4065_CR23","doi-asserted-by":"publisher","first-page":"e107939","DOI":"10.1371\/journal.pone.0107939","volume":"9","author":"A Garg","year":"2014","unstructured":"Garg A, Stein A, Zhao W, Dwivedi A, Frutos R, Cornillot E, et al. Sequence and annotation of the apicoplast genome of the human pathogen Babesia microti. PLoS One. 2014;9:e107939.","journal-title":"PLoS One."},{"key":"4065_CR24","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1016\/j.exppara.2009.07.007","volume":"123","author":"AO Lau","year":"2009","unstructured":"Lau AO, McElwain TF, Brayton KA, Knowles DP, Roalson EH. Babesia bovis: a comprehensive phylogenetic analysis of plastid-encoded genes supports green algal origin of apicoplasts. Exp Parasitol. 2009;123:236\u201343.","journal-title":"Exp Parasitol."},{"key":"4065_CR25","doi-asserted-by":"publisher","first-page":"868","DOI":"10.1101\/gr.9.9.868","volume":"9","author":"X Huang","year":"1999","unstructured":"Huang X, Madan A. CAP3: a DNA sequence assembly program. Genome Res. 1999;9:868\u201377.","journal-title":"Genome Res."},{"key":"4065_CR26","doi-asserted-by":"publisher","first-page":"D427","DOI":"10.1093\/nar\/gky995","volume":"47","author":"S El-Gebali","year":"2019","unstructured":"El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2019;47:D427\u201332.","journal-title":"Nucleic Acids Res."},{"key":"4065_CR27","doi-asserted-by":"publisher","first-page":"312","DOI":"10.1186\/s13071-019-3581-x","volume":"12","author":"X Wang","year":"2019","unstructured":"Wang X, Wang J, Liu J, Liu A, He X, Xu J, et al. Comparative analysis of apicoplast genomes of Babesia infective to small ruminants in China. Parasit Vectors. 2019;12:312.","journal-title":"Parasit Vectors."},{"key":"4065_CR28","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1016\/j.vetpar.2016.11.004","volume":"233","author":"T Wang","year":"2017","unstructured":"Wang T, Guan G, Korhonen PK, Koehler AV, Hall RS, Young ND, et al. The apicoplast genomes of two taxonomic units of Babesia from sheep. Vet Parasitol. 2017;233:123\u20138.","journal-title":"Vet Parasitol."},{"key":"4065_CR29","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1016\/j.ijpara.2018.05.008","volume":"49","author":"AZ Virji","year":"2019","unstructured":"Virji AZ, Thekkiniath J, Ma W, Lawres L, Knight J, Swei A, et al. Insights into the evolution and drug susceptibility of Babesia duncani from the sequence of its mitochondrial and apicoplast genomes. Int J Parasitol. 2019;49:105\u201313.","journal-title":"Int J Parasitol."},{"key":"4065_CR30","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1104\/pp.118.1.9","volume":"118","author":"W Martin","year":"1998","unstructured":"Martin W, Herrmann RG. Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol. 1998;118:9\u201317.","journal-title":"Plant Physiol."},{"key":"4065_CR31","doi-asserted-by":"publisher","first-page":"705","DOI":"10.1126\/science.1078599","volume":"299","author":"BJ Foth","year":"2003","unstructured":"Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, Roos DS, et al. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science. 2003;299:705\u20138.","journal-title":"Science."},{"key":"4065_CR32","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1016\/j.lfs.2016.06.030","volume":"158","author":"A Chakraborty","year":"2016","unstructured":"Chakraborty A. Understanding the biology of the Plasmodium falciparum apicoplast; an excellent target for antimalarial drug development. Life Sci. 2016;158:104\u201310.","journal-title":"Life Sci."},{"key":"4065_CR33","doi-asserted-by":"publisher","first-page":"2095","DOI":"10.1093\/molbev\/mss082","volume":"29","author":"N Arisue","year":"2012","unstructured":"Arisue N, Hashimoto T, Mitsui H, Palacpac NM, Kaneko A, Kawai S, et al. The Plasmodium apicoplast genome: conserved structure and close relationship of P. ovale to rodent malaria parasites. Mol Biol Evol. 2012;29:2095\u20139.","journal-title":"Mol Biol Evol."},{"key":"4065_CR34","doi-asserted-by":"publisher","first-page":"2375","DOI":"10.1091\/mbc.9.9.2375","volume":"9","author":"PJ Magalhaes","year":"1998","unstructured":"Magalhaes PJ, Andreu AL, Schon EA. Evidence for the presence of 5S rRNA in mammalian mitochondria. Mol Biol Cell. 1998;9:2375\u201382.","journal-title":"Mol Biol Cell."},{"key":"4065_CR35","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/0014-5793(94)80351-X","volume":"338","author":"S Yoshionari","year":"1994","unstructured":"Yoshionari S, Koike T, Yokogawa T, Nishikawa K, Ueda T, Miura K, et al. Existence of nuclear-encoded 5S-rRNA in bovine mitochondria. FEBS Lett. 1994;338:137\u201342.","journal-title":"FEBS Lett."},{"key":"4065_CR36","doi-asserted-by":"publisher","first-page":"10949","DOI":"10.1073\/pnas.1003335107","volume":"107","author":"J Janouskovec","year":"2010","unstructured":"Janouskovec J, Horak A, Obornik M, Lukes J, Keeling PJ. A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA. 2010;107:10949\u201354.","journal-title":"Proc Natl Acad Sci USA"},{"key":"4065_CR37","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/j.ijpara.2016.08.005","volume":"47","author":"GI McFadden","year":"2017","unstructured":"McFadden GI, Yeh E. The apicoplast: now you see it, now you don\u02bct. Int J Parasitol. 2017;47:137\u201344.","journal-title":"Int J Parasitol."},{"key":"4065_CR38","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1038\/s41564-018-0162-2","volume":"3","author":"TD Otto","year":"2018","unstructured":"Otto TD, Gilabert A, Crellen T, Bohme U, Arnathau C, Sanders M, et al. Genomes of all known members of a Plasmodium subgenus reveal paths to virulent human malaria. Nat Microbiol. 2018;3:687\u201397.","journal-title":"Nat Microbiol."}],"container-title":["Parasites &amp; Vectors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13071-020-04065-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13071-020-04065-7\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13071-020-04065-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,4,21]],"date-time":"2021-04-21T00:39:14Z","timestamp":1618965554000},"score":1,"resource":{"primary":{"URL":"https:\/\/parasitesandvectors.biomedcentral.com\/articles\/10.1186\/s13071-020-04065-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,4,21]]},"references-count":38,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2020,12]]}},"alternative-id":["4065"],"URL":"https:\/\/doi.org\/10.1186\/s13071-020-04065-7","relation":{},"ISSN":["1756-3305"],"issn-type":[{"value":"1756-3305","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,4,21]]},"assertion":[{"value":"31 October 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"9 April 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 April 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The feeding conditions and environment of all experimental animals comply with and strictly per the stipulated rules for the Regulation of the Administration of Affairs Concerning Experimental Animals of PR China, Laboratory Animals Research Centre of Hubei Province and the Ethics Committee of Huazhong Agricultural University (license number: HZAUDO-2017-005). Each experimental animal was carefully treated during the experiment so that the damage to the experimental animals could be minimized.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"209"}}