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Comparative Analysis of Camelid Mitochondrial Genomes

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Comparative Analysis of Camelid Mitochondrial Genomes Journal of Genetics (2019) 98:88 © Indian Academy of Sciences https://doi.org/10.1007/s12041-019-1134-x RESEARCH ARTICLE Comparative analysis of camelid mitochondrial genomes MANEE M. MANEE1,2∗ , MANAL A. ALSHEHRI1, SARAH A. BINGHADIR1, SHAHAD H. ALDHAFER3, RIYOF M. ALSWAILEM3, ABDULMALEK T. ALGARNI1, BADR M. AL-SHOMRANI1 and MOHAMED B. AL-FAGEEH1 1National Centre for Biotechnology, King Abdulaziz City for Science and Technology, Riyadh 11442, Saudi Arabia 2Centre of Excellence for Genomics, King Abdulaziz City for Science and Technology, Riyadh 11442, Saudi Arabia 3College of Computer and Information Sciences, Imam Muhammad Ibn Saud Islamic University, Riyadh 11432, Saudi Arabia *For correspondence. E-mail: [email protected]. Received 9 April 2019; revised 26 June 2019; accepted 9 July 2019 Abstract. Camelus dromedarius has played a pivotal role in both culture and way of life in the Arabian peninsula, particularly in arid regions where other domestic animals cannot be easily domesticated. Although, the mitochondrial genomes have recently been sequenced for several camelid species, wider phylogenetic studies are yet to be performed. The features of conserved gene elements, rapid evolutionary rate, and rare recombination make the mitochondrial genome a useful molecular marker for phylogenetic studies of closely related species. Here we carried out a comparative analysis of previously sequenced mitochondrial genomes of camelids with an emphasis on C. dromedarius, revealing a number of noticeable findings. First, the arrangement of mitochondrial genes in C. dromedarius is similar to those of the other camelids. Second, multiple sequence alignment of intergenic regions shows up to 90% similarity across different kinds of camels, with dromedary camels to reach 99%. Third, we successfully identified the three domains (termination-associated sequence, conserved domain and conserved sequence block) of the control region structure. The phylogenetic tree analysis showed that C. dromedarius mitogenomes were significantly clustered in the same clade with Lama pacos mitogenome. These findings will enhance our understanding of the nucleotide composition and molecular evolution of the mitogenomes of the genus Camelus, and provide more data for comparative mitogenomics in the family Camelidae. Keywords. mitochondrial DNA; genome annotation; phylogenetic analysis; control region; intergenic regions; Camelus dromedarius. Introduction tribe characterized by thick eyelashes, a long curved neck, and a single hump as opposed to the two humps on the Camelus dromedarius, often referred as the Arabian camel, Bactrian camel and wild Bactrian camel. These unique is a member of the camelid family and by far the most physical features, among others, give Arabian camels their important domesticated herbivore desert mammal of the ability to conserve water and regulate body temperature, Arabian peninsula. The family Camelidae is divided into thereby thriving in extreme harsh environments such as the two tribes, namely Camelini (Dromedary, Bactrian and Arabian peninsula (Al-Swailem et al. 2010). For instance, wild Bactrian camel) and Lamini (alpaca, guanaco, llama the camel’s hump stores up to 35 kg of fat, which can and vicua), and they mainly inhabit southwest Asia, north- be broken down into water and energy whenever needed. ern Africa, and Australia (Wang et al. 2012; Wu et al. 2014). C. dromedarius also adapts to arid conditions by promot- C. dromedarius is an even-toed ungulate in the Camelini ing the expression of various genes such as small heat shock genes (Manee et al. 2017). Heat shock proteins play a key MMM and MBA conceived and designed the experiments; MMM, role in the protection of cells against environmental stress. MAA, SAB, SHA, RMA and ATA carried out the experiments; MMM, MAA, SAB, ATA and BMA analysed the data; MMM, MAA and SAB In addition, recent genomic studies have also revealed the wrote the manuscript. All authors reviewed the manuscript. complex characteristics related to adaptations to desert Electronic supplementary material: The online version of this article (https://doi.org/10.1007/s12041-019-1134-x) contains supplemen- tary material, which is available to authorized users. 0123456789().: V,-vol 88 Page 2 of 12 Manee. M. Manee et al. Table 1. Thirty-one mitochondrial genomes from Camelidae family members used in this study. Scientific name Common name Location Accession no. Length (bp) 1 C. dromedarius Arabian camel Middle East EU159113.1 16643 2 KU605075.1 16379 3 KU605079.1 16379 4 KU605080.1 16379 5 KU605076.1 16379 6 KU605072.1 16379 7 KU605073.1 16379 8 KU605074.1 16379 9 KU605077.1 16379 10 KU605078.1 16379 11 C. bactrianus Bactrian camel Central Asia KU666462.1 16379 12 KU666463.1 16398 13 KU666464.1 16398 14 KU666465.1 16398 15 NC_009628.2 16659 16 KU666460.1 16398 17 KU666461.1 16398 18 C. ferus Wild Bactrian camel Central Asia KU666452.1 16379 19 KU666453.1 16379 20 KU666454.1 16379 21 KU666451.1 16379 22 KU666455.1 16379 23 KU666457.1 16379 24 KU666456.1 16379 25 KU666458.1 16379 26 KU666459.1 16379 27 NC_009629.2 16379 28 L. glama Llama South America AP003426.1 16597 29 L. guanicoe Guanaco South America NC_011822.1 16649 30 L. pacos Alpaca South America Y19184.1 16652 31 V. vicugna Vicuña South America NC_013558.1 16084 harsh environments, including heat stress responses, fat particular, we annotated and characterized the mitochon- and water metabolism, dehydration, and choking dust drial genome of C. dromedarius from the United Arab (Wu et al. 2014). Genome data, particularly mitochondrial Emirates and described its gene structure, arrangement DNA (mtDNA), can be used to investigate evolutionary and base composition, as well as its noncoding regions. relationships among species and to infer the evolutionary Further, C. dromedarius mitogenome was compared with and demographic history of the species (Robinson et al. those from other camels to identify similarities and dif- 2010; Gonzalez-Freire et al. 2015). ferences between these animals. We also constructed a The mitochondria is a vital organelle responsible for phylogenetic tree for the purpose of analysing evolutionary oxidative phosphorylation to produce adenosine triphos- relationships among family Camelidae. phate (ATP), as well as having various other roles in metabolism, cell signalling, cell cycle regulation, initiation Materials and methods of cell differentiation, cell proliferation, ageing and apop- tosis (Mandal et al. 2011). The mitochondria possess its Annotation and analysis of the mitochondrial genome own DNA (mitogenome), which is considered a power- ful material for phylogenetic studies because of its small The C. dromedarius reference mitogenome was included size, lack of recombination, and lack of repair mechanisms as a sample due to the geographical location of the collec- (Chen 2013; Zinovkina 2018). Mitogenome is typically tion site (United Arab Emirates, the Arabian Peninsula). circular double-stranded DNA molecule, 16-kb long and This was the first C. dromedarius mitogenome deposited in encodes 37 genes in humans (Boore 1999). It also has a GenBank with accession number EU159113.1. We anno- massive copy rate compared to the nuclear genome, and tated this mitogenome and identified protein-coding genes its maternal inheritance pattern precludes recombination, (PCG), transfer RNA (tRNA) genes, and ribosomal RNA with the result that to the sequence of the mitogenome is (rRNA) genes using the free web server MITOS (http:// usually stable through generations (Gupta et al. 2015). mitos.bioinf.uni-leipzig.de/index.py) with default settings This study is the first report on mitogenome annotation and the genetic code set to ‘05 – Invertebrate/Mito’ and characterization of C. dromedarius.In(Bernt et al. 2013). All tRNA genes were confirmed Camelid Mitochondrial Genomes Page 3 of 12 88 Figure 1. The organization of the C. dromedarius mitogenome (16.643 bp). The circular genome depicted protein coding genes (green), ribosomal RNAs (red), tRNAs (pink), and repeat region (brown). The origin and direction of L-strand (OL) replication are indicated by bent blue arrows. using tRNAScan-SE (v2.0) with default parameters and numbers are given in table 1. Base composition, AT-skew sequence source set to vertebrate mitochondrial (Lowe and GC-skew were determined for these mitogenomes. and Chan 2016). The positions of rRNA genes and of We calculated base composition using Geneious soft- the control region were confirmed using the boundaries ware (Kearse et al. 2012). AT-skew and GC-skew were of the tRNA genes. All detected C. dromedarius genes, calculated according to the formulas: AT-skew = (A% including PCG, and the control region were later refined – T%)/(A% + T%) and GC-skew = (G% – C%)/(G% through multiple sequence alignment to the mitochondrial + C%). The relative synonymous codon usage of all DNA and amino acid sequences of 30 other Camelidae PCG for C. dromedarius (accession no. EU159113.1) and species (table 1) using the webserver MAFFT (v7.130) C. bactrianus (accession no. KU666462.1) was calculated (https://mafft.cbrc.jp/alignment/server/)(Katoh and Stan- using MEGA software (v7) (Kumar et al. 2016). The sec- dley 2013). Intergenic spacers and overlapping regions ondary structures of tRNA genes of the 14 selected camelid between genes were also identified using an in-house script. mitogenomes were also determined using MITOS web- Classification of the domains and elements of the control server (Bernt et al. 2013). region was based on previously published sequence data from several mammals (Gemmell et al. 1996). Short tan- dem repeats were identified using PERF (v0.2.5) (Avvaru Phylogenetic analysis et al. 2017). We generated two phylogenetic trees for the 31 camelid Comparative analysis of the mitochondrial genomes mitogenomes (table 1), one based on whole mitogenomes, and the other based on the extracted intergenic regions. Wecompared the mitochondrial genomes of 31 individuals Multiple sequence alignments were conducted using Clu- from seven species, including C. dromedarius; all accession stalW integrated with MEGA (v7) (Kumar et al. 2016). 88 Page 4 of 12 Manee. M. Manee et al. Table 2. Annotation of the C.
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