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Annotation and Characterization of Babesia Gibsoni Apicoplast Genome

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Annotation and Characterization of Babesia Gibsoni Apicoplast Genome Liu et al. Parasites Vectors (2020) 13:209 https://doi.org/10.1186/s13071-020-04065-7 Parasites & Vectors RESEARCH Open Access Annotation and characterization of Babesia gibsoni apicoplast genome Qin Liu1,2, Long Yu1,2, Fan Jiang3, Muxiao Li1,2, Xueyan Zhan1,2, Yuan Huang1,2, Sen Wang1,2, Xiaoyong Du3, Lan He1,2,4* and Junlong Zhao1,2,4 Abstract Background: Babesia gibsoni 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 apicom- plexan parasites, except for Cryptosporidium. Available data indicate that the apicoplast is essential for the survival of apicomplexan parasites. Methods: Here, the apicoplast genome of B. gibsoni was investigated by high-throughput genome sequencing, bioinformatics analysis, and conventional PCR. Results: The apicoplast genome of B. gibsoni-Wuhan strain (B. gibsoni-WH) consists of a 28.4 kb circular molecule, with A T content of 86.33%, similar to that of B. microti. Specifcally, this genome encodes genes involved in mainte- nance of+ the apicoplast DNA, transcription, translation and maturation of organellar proteins, which contains 2 subu- nits 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 pro- teins). Phylogenetic analysis revealed high similarity of B. gibsoni apicoplast genome to that of B. orientalis and B. bovis. Conclusions: To our knowledge, this is the frst report of annotation and characterization of B. gibsoni-WH apicoplast genome. The results will facilitate the development of new anti-Babesia drug targets. Keywords: Babesia gibsoni, Apicoplast genome, Sequencing, Annotation, Comparative analysis Background research eforts have been devoted to pathogenicity, Babesia gibsoni, an obligate intraerythrocytic para- gene diversity and identifcation of new targets against sitic protozoan that can cause canine babesiosis [1–3], the disease. spreads widely around the world. Canine babesiosis Apicomplexan parasites, except for Cryptosporidium, caused by B. gibsoni may cause hyperacute, acute and contain an apicoplast, which is a unique, essential orga- more commonly chronic infection [3], with the clinical nelle for the survival of these parasites [10]. Te apico- symptoms of fever, hemolytic anemia and even death [4, plast has been reported to contain four membranes in 5]. Babesia gibsoni is mainly transmitted by ticks but can apicomplexan parasites [11, 12] and results from a sec- also be transmitted by blood transfusion, dog bites and ondary endosymbiosis of eukaryotic algae, and that the even transplacental route [6–9]. In an efort to improve red algae origin hypothesis is more likely than the green the diagnosis and treatment of canine babesiosis, many algae origin hypothesis [13, 14]. After the evolution from chloroplast into apicoplast, the genes encoding a variety of proteins, transfer RNAs (tRNAs) and ribosomal RNA *Correspondence: [email protected] (rRNA) are still present in apicomplexan parasites [15]. 1 State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan 430070, Hubei, China Tis endowed the apicoplast with a series of bacteria-like Full list of author information is available at the end of the article pathways to replicate and express its genome coupled © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Liu et al. Parasites Vectors (2020) 13:209 Page 2 of 10 with an anabolic capacity for producing fatty acids, Apicoplast genome sequencing iron-sulphur cluster, haem and isoprenoid precursors Te raw apicoplast sequence and the whole genome [16–20]. A previous study has shown that interfering the sequence (unpublished data) of B. gibsoni obtained from apicoplast in laboratory conditions (such as interference PacBio sequencing (Wuhan, China) were assembled using with isoprenoid synthesis pathways) could cause parasite the CAP3 assembly program to obtain the raw sequence death, but the addition of relevant substitutes after inter- [25], which was used as reference to obtain highly con- ference does not afect parasite growth [21]. Tis con- served genes through BLAST alignment. Based on the frms the importance of apicoplast for parasite survival, conserved genes, primers were designed for conventional making it a hotspot in anti-parasitic drug design. PCR amplifcation, followed by amplifying the sequence Te apicoplast genomes of Babesia bovis, Babesia between two conserved genes (Additional fle 1: Table S1). microti, Babesia orientalis and Toxoplasma gondii have After several calibrations, the entire apicoplast genome been sequenced and characterized [12, 22–24]. How- was completely covered. Te sequences were assembled ever, little information is available about the apicoplast again to obtain the fnal apicoplast genome sequence. genome of B. gibsoni. Terefore, this study focused on the annotation and characterization of Babesia gibsoni- Analysis and annotation Wuhan strain (Babesia gibsoni-WH) apicoplast genome. Te apicoplast genome of B. gibsoni was annotated by Artemis (https ://www.sange r.ac.uk/resou rces/softw are/ Methods artem is/) in combination with BLAST in NCBI (http:// Parasites and animal experiments blast .ncbi.nlm.nih.gov/Blast .cgi). Te data was screened Babesia gibsoni-WH was stored in liquid nitrogen in by Open Reading Frame Finder (ORFs) (https ://www. the State Key Laboratory of Agricultural Microbiology, ncbi.nlm.nih.gov/orf nder/) and GenMark (http://opal. Huazhong Agricultural University, China. biolo gy.gatec h.edu/GeneM ark/index .html). Published Two one-year-old beagles with health certifcates were protozoan apicoplast genomes were used as references purchased from Anlu Laboratory Animal Center and to conceptually translate and annotate the putative confrmed to be Babesia-free by microscopic examina- code areas. Te tRNA genes were predicted by tRNAs- tion and PCR. After injection with 5 ml of blood infected canSE 2.0 (http://lowel ab.ucsc.edu/tRNAs can-SE/) with with B. gibsoni, the body temperature of the experimen- the following parameters: source ‘‘Mito/Chloroplast’’ tal beagles was observed daily and blood smears were and search mode ‘‘default’’. Te rDNA sequences (SSU prepared every second days to monitor the parasitemia. and LSU) were separately obtained by comparing the When parasitemia reached 20%, blood was collected from counterparts of B. bovis, B. microti and B. orientalis. the experimentally infected dogs for further research as Mis-annotations in the published apicoplast genomes described below. were re-annotated. Te maps of the B. gibsoni apico- plast genome were produced using online CGView soft- Purifcation of parasites ware (http://stoth ard.afns.ualbe rta.ca/cgvie w_serve r/). Te blood was collected from infected dogs into tubes Te repeatability of rRNA genes was verifed using the containing EDTA-K2 solution, followed by storage at repeatmasker server (http://www.repea tmask er.org/cgi- 4 °C for 2 h and centrifugation at 2000× rpm at 4 °C for bin/WEBRe peatM asker ). Te multiple genome align- 10 min. After removing the supernatant, a fve-fold vol- ments were generated by the software Mauve (http:// ume of hypotonic RBC lysis bufer (Na3PO4/EDTA, PH darli nglab .org/mauve /mauve .html). All of the above 7.6) was added to the pellets, followed by incubation at analysis results were corrected manually on a gene-by- 37 °C for 30 min. Next, the lysate was fltered through a gene basis as needed. Te reference genomes used in 2 μm membrane (Whatman, Florham Park, USA) and the this study included NC_011395 (B. bovis), KT428643.1 collected bufer was centrifuged at 12,000×g at 4 °C for (B. orientalis), KX881914.1 (Babesia sp. Xinjiang), 10 min. Finally, the pellets were collected and stored at LK028575 (B. microti), NC_007758 (T. parva), X95275 − 80 °C until further use. (IRA) and X95276 (IRB) (P. falciparum), U87145 (T. gon- dii), NC_014345.1 (Alveolata sp. CCMP3155). Te phy- DNA extraction logenetic tree of the rRNA genes was constructed using Genomic DNA was extracted from purifed parasites MEGA 7.0 with the Maximum Likelihood method (https using the QIAamp DNA Mini Kit (Qiagen, Shanghai, ://www.megas oftwa re.net/). Te functional domains China) according to the manufacturer’s instructions. and transmembrane domain were separately predicted After passing the quality test, the genomic DNA was used by using the software Pfam (http://pfam.sange r.ac.uk/) for further analysis. [26] and TMpred (http://www.ch.embne t.org/softw are/ TMPRE D_form.html). Liu et al. Parasites Vectors (2020) 13:209 Page 3 of 10 Results and discussion of B. gibsoni was shown to be a circular DNA of 28.4 kb Characteristics of apicoplast genome sequence of B. with A + T content of 86.33%, which is similar to that of gibsoni B. microti (28.7 kb, A + T% = 86%) (Table 1) [23]. Te available literature has shown limited genetic infor- Te Babesia gibsoni apicoplast genome contains mation of B.
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