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Mitochondrial DNA B Resour
Mitochondrial DNA B Resour
Mitochondrial DNA. Part B, Resources
2380-2359
Taylor & Francis

10.1080/23802359.2024.2404211
2404211
Version of Record
Data Note
Mitogenome Report
The complete mitochondrial genome and phylogenetic analysis of Rattus tanezumi (Niethammer, 1975), captured from North China
H. Tian et al.
Tian Hong a
Han Weimin a
Li Luling a
Shi Xiaodong a
Han Xu b
Wei Yamei b
Cai Yanan b
Han Zhanying b
Zhang Yanbo b
Xu Yonggang b
Li Qi b
Liu Shiyou ab
a School of Public Health, Hebei Medical University, Shijiazhuang, China
b Hebei Provincial Center for Disease Control and Prevention, Shijiazhuang, China
Supplemental data for this article can be accessed online at https://doi.org/10.1080/23802359.2024.2404211.

CONTACT Shiyou Liu lsy7@outlook.com
Qi Li liqinew@126.com Hebei Provincial Center for Disease Control and Prevention, 97 Huaian East Road, Shijiazhuang, Hebei, 050021, China.
15 9 2024
2024
15 9 2024
9 9 12181222
11 5 2024
9 9 2024
KnowledgeWorks Global Ltd.14 9 2024
published online in a building issue14 9 2024
© 2024 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
2024
The Author(s)
https://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. The terms on which this article has been published allow the posting of the Accepted Manuscript in a repository by the author(s) or with their consent.

Abstract

Rattus tanezumi (Niethammer, 1975) is one of the commensal rodent species in South China. With the development of transportation and climate change, R. tanezumi has gradually migrated north and become the dominant rat species for the past few years. In this study, we assembled a complete mitochondrial genome of R. tanezumi, captured from North China. The mitogenome contains 16,307 nucleotide pairs, including 13 protein-coding genes, 2 ribosomal RNA genes, and 22 transfer RNA genes, as well as one non-coding control region. Based on whole mitogenome phylogenetical analysis showed that R. tanezumi captured from North China had a close phylogenetic relationship with that from Japan and South Korea. These findings are valuable for further studies on the evolution, genetic diversity, and taxonomy of Asian commensal rodent.

Keywords

Rattus tanezumi
complete mitochondrial genome
phylogeny
Key Research and Development Program of Hebei Province 10.13039/501100015286 D D This work was a part of the Key Research and Development Program of Hebei Province under Grant [21377727D, 20200684].
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pmcIntroduction

The commensal rodent, R. tanezumi (Figure 1) traditionally called Oriental house rat (Niethammer, 1975), native to South East Asia (Adhikari et al. 2018a). It has been introduced to East Asia and mainly distributed in the south of the Yellow River (Adhikari et al. 2018b; Guo et al. 2019). With the development of transportation and climate change, it has been found that R. tanezumi has gradually migrated north China and become the dominant rat species for the past few years (Liu et al. 2019). As one of the serious pests in farmland, R. tanezumi can cause damage to crops during harvesting and reducing crop yields (Brown et al. 2006; Htwe et al. 2019). Due to its seasonal migration and wide range of habitats, the R. tanezumi can carry various pathogens, which cause zoonotic diseases, representing a serious threat for human health (He et al. 2021; Zhang, You et al. 2021; Zhang, Li et al. 2021).

Figure 1. The morphological characteristics of R. tanezumi (HD190053). The photo of specimen was supplied by Hebei Provincial Institute for Plague Control and Prevention.

At present, there have been some studies on the gene evolution and phylogeny of the R. tanezumi, but this is little information on the whole mitochondrial genome of R. tanezumi (Teng et al. 2016; Li et al. 2023). Our study characterized the complete mitochondrial genome of R. tanezumi captured from North China, which will provide more molecular information for future research on the taxonomy and genetic evolution of asian commensal rodent.

Materials and methods

The R. tanezumi specimen was collected in autumn 2019 from Handan (36°34′60.0″N, 114°28′60.0″E), Hebei Province, China. The tissue (hearts, lungs, livers, spleens and kidneys) was acquired after morphological analysis (Figure 1) on site, and stored at −80 °C in Hebei Provincial Center for Disease Control and Prevention (Shiyou Liu, lsy7@outlook.com) under the voucher number HD190053. Total genomic DNA was isolated from the liver tissue using the Tissue Genomic DNA kit (Biogerm, Shanghai, China). The extractive genome was sent to Personalbio (Shanghai, China) for sequencing use shotgun technology. DNA library with an insert size of approximately 400 bp was constructed and sequenced on the Illumina Miseq platform, with 250 bp paired-end reads. After filtering out of raw sequencing reads containing adapters and reads of low quality, the resultant sequences were assembled using SPAdesv3.9.0 (Bankevich et al. 2012) and correcting the results with Pilon v1.18 (Walker et al. 2014). The functional annotations were performed using the MITOS (http://mitos.bioinf.uni-leipzig.de/) (Bernt et al. 2013), and mitochondrial whole genome circles were mapped using the cgview. Phylogenetic analysis was performed using the MEGA 11, the complete mitochondrial genomes of 23 species were obtained from Genbank, the best nucleotide substitution model GTR + G + I was selected and the No. of bootstrap replications was 1000.

Results

Mitogenome organization

The whole mitogenome of R. tanezumi is 16,307 bp in length and has been deposited in GenBank (Accession number: OK054583.1). The nucleotide composition of the R. tanezumi mitochondrial genome was as follows: A = 34.08%, T = 28%, G = 12.6%, and C = 25.33%. It consists of 13 protein-coding genes (PCGs), 2 ribosomal RNA genes (rRNAs), 22 transfer RNA genes (tRNAs), and a control region. Among these, 12 PCGs, 14 tRNA genes, and 2 rRNA genes were encoded in the heavy strand, whereas 1 PCG (NADH dehydrogenase subunit 6) and 8 tRNA genes were encoded in the light strand. Among the protein-coding genes, except for nad3 and nad5, which had ATA as the start codon, the other 11 genes had ATG as the start codon. In addition, two protein-coding genes (cox3, nad4) ended with incomplete stop codons, while the remaining 11 protein-coding genes ended with complete stop codons TAA or TAG (Figure 2, Table S2). The genome coverage across the reference figure is detailed in the supplementary material (Figure S1).

Figure 2. Complete mitochondrial genome map of R. tanezumi. The diagram displays the scale, GC skew, GC content, and arrangement of protein coding genes, tRNA genes, and rRNA genes on the genome. The first circle represents the scale, followed by the GC skew in the second circle, the GC content in the third circle, and the arrangement of genes in the fourth and fifth circles.

Phylogenetic analysis

To investigate the phylogenetic relationship between R. tanezumi from China and other regions, we constructed the phylogenetic tree using the complete mitochondrial genome sequence of R. tanezumi and the sequences from the other 23 species (supplementary material Table S1). Bunomys penitus and Sundamys muelleri were set as the outer groups and the sequences were obtained from GenBank. The phylogenetic tree indicates that R. tanezumi captured from North China was closely clustered with that from Japan and South Korea and completely separated from other species (Figure 3). This newly sequenced complete mitochondrial genome provides valuable information for exploring the genetic diversity and phylogenetic relationships of the Rodent family.

Figure 3. Phylogenetic tree of R. tanezumi and other related species based on mitochondrial genome sequences. Phylogenetic analysis was performed using MEGA 11 software. GenBank accession numbers of each mitochondrial genome sequences are given after the species name, and the bootstrap value based on 1,000 replicates is represented on each node. Bunomys penitus and Sundamys muelleri were used as outgroups to root the tree. The name of reported species was noted with a red dot. The following sequences were used: KF011916 (Adhikari et al. 2018), MN126566 (Camacho-Sanchez and Leonard 2020), NC_011638 (Robins et al. 2008), DQ673917 (Robins et al. 2010), NC_040919 (Zhu et al. 2016), MK558274 (Robins et al. 2008), EU273710 (Robins et al. 2010), EU273707 (Robins et al. 2010), EU273708 (Robins et al. 2010), NC_023347 (Adhikari et al. 2018b), NC_035621 (Camacho-Sanchez and Leonard 2020), MN126561 (Cai et al. 2021), MN126563 (Camacho-Sanchez and Leonard 2020), MN126567 (Camacho-Sanchez and Leonard 2020), NC_0148,55 (Robins et al. 2010), NC_014858 (Robins et al. 2010), NC_014861 (Robins et al. 2010), NC_014864 (Robins et al. 2010), NC_014867 (Robins et al. 2010), NC_014871 (Robins et al. 2010), NC_005089.1 (Zhang et al. 2021), KT029807 (Wang et al. 2016), KY464167 (Camacho-Sanchez et al. 2017), KY464172 (Camacho-Sanchez et al. 2017).

Discussion and conclusion

The sequence we assembled is 16307 bp in length and the other three are 16306 bp. We analyzed the mitochondrial sequences of four different species of R. tanezumi, and discovered that while the overall length of each sequence was slightly different, it was composed of 13 PCGs, 2 rRNAs, 22 tRNAs, and a control region. However, they distributed and been formed stable local communities in different countries (China, Japan, Malaysia, South Korea) and captured in different years. So these four R. tanezumi should have been evolved into different evolutionary branches.

In the 1950s, R. tanezumi in China was mainly distributed in the Yellow River basin, eastern and southern regions (Robins et al. 2008), however R. tanezumi has recently expanded its range to north of the Yellow River in the south of Hebei Province and partially replaced the native R. norvegicus subspecies (Li et al. 2023). Invasive species have an advantage in interspecific competition, and invasive species are often more aggressive than native species, and closely related species are more competitive than distantly related, encouraging invasive R. tanezumi to replace native species (Amarasekare 2002).

There was study suggest that R. tanezumi and R. norvegicus may chronically interact, and that such interactions may contribute to the invasive success and northward expansion of R. tanezumi and the decline of native R. norvegicus populations in natural habitats (Guo et al. 2017). Several factors, including global warming and higher resistance to common rodenticides compared with R. norvegicus, are believed to likely contribute to the invasive success of R. tanezumi (Guo et al. 2017). Rats as typical zoonotic hosts, harbor ectoparasites such as ticks, lice and mites, and a variety of internal parasites (Puckett et al. 2020). The change in population structure of native rat species will certainly have some impact on the original ecosystem and the prevalence of rat-borne diseases. The wider public health implications of the R. tanezumi invasion deserve our attention and further research.

The genus Rattus is highly speciose, the taxonomy is complex, and individuals are often difficult to identify to the species level (Robins et al. 2014). R. rattus and R. tanezumi were well known to be difficult to be morphologically differentiated from one another (Aplin et al. 2011; Huang et al. 2022). This suggests that the accuracy of traditional morphological identification is difficult to ensure and that molecular biology methods can be used as a complementary tool (Camacho-Sanchez and Leonard 2020). The sequencing of mitochondrial genomes can better identify rat species at the molecular level and help us understand the composition of rat species in North China.

In conclusion, we identified the complete mitochondrial genome of R. tanezumi and elucidated the phylogenetic relationship with other Rattus by constructing a phylogenetic tree. These data provide important information for future taxonomic, systematic, and genetic studies on R. tanezumi and commensal rodent species in North China.

Supplementary Material

model selection.xlsx

supplemental material.docx

Acknowledgments

We express our gratitude to Handan Municipal Center for Disease Control and Prevention, China, for facilitating and supporting this research project.

Authors’ contributions

SL, QL designed the study. SL and HT wrote the original manuscript, LL, XS, XH, YW, XH and YC performed sample collection, ZH, YZ, YX collected the data, SL, HT and WH supported the bioinformatics analyses. All the authors approved the manuscript.

Disclosure statement

The authors report there are no competing interests to declare.

Ethical approval

The sample used in this study was Rattus tanezumi, which is not involve endangered or protected animals, and the sampling did not violate any laws or regulations in China. The collection of field samples was approved by the Hebei Provincial Center for Disease Control and Prevention (HeBCDCIRB(S)2021-017), and the study strictly complied with the relevant regulations of China’s animal welfare management.

Data availability statement

The genome sequence data that support the findings of this study are openly available in GenBank of NCBI at (https://www.ncbi.nlm.nih.gov/) under the accession no. OK054583.1. The associated ‘BioProject’, ‘SRA’ and ‘Bio-Sample’ numbers are PRJNA1104746, SRR28818859, and SAMN41085771 respectively.
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