Thousands of eukaryotes transcriptomes have been generated, mainly to investigate nuclear genes expression, and the amount of available data is constantly increasing. A neglected but promising use of this large amount of data is to assemble organelle genomes. To assess the reliability of this approach, we attempted to reconstruct complete mitochondrial genomes from RNA-Seq experiments of Reticulitermes termite species, for which transcriptomes and conspecific mitogenomes are available. We successfully assembled complete molecules, although a few gaps corresponding to tRNAs had to be filled manually. We also reconstructed, for the first time, the mitogenome of Reticulitermes banyulensis. The accuracy and completeness of mitogenomes reconstruction appeared independent from transcriptome size, read length and sequencing design (single/paired end), and using reference genomes from congeneric or intra-familial taxa did not significantly affect the assembly. Transcriptome-derived mitogenomes were found highly similar to the conspecific ones obtained from genome sequencing (nucleotide divergence ranging from 0% to 3.5%) and yielded a congruent phylogenetic tree. Reads from contaminants and nuclear transcripts, although slowing down the process, did not result in chimeric sequence reconstruction. We suggest that the described approach has the potential to increase the number of available mitogenomes by exploiting the rapidly increasing number of transcriptomes.

Agrarian Entomology Research and Innovation Centre Fondazione Edmund Mach Via E Mach 1 38010 San Michele all'Adige TN Italy

Department of Biological Geological and Environmental Sciences University of Bologna via Selmi 3 40126 Bologna Italy

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Czech Republic

Okinawa Institute of Science and Technology Graduate University 1919 1 Tancha Onna son Okinawa 904 0495 Japan

School of Animal Biology University of Western Australia Perth WA 6009 Australia

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Cameron SL. Insect mitochondrial genomics: implications for evolution and phylogeny. Ann. Rev. Entomol. 2014;59:95–117. doi: 10.1146/annurev-ento-011613-162007. PubMed DOI

Song N, Li H, Song F, Cai W. Molecular phylogeny of Polyneoptera (Insecta) inferred from expanded mitogenomic data. Sci. Rep. 2016;6:36175. doi: 10.1038/srep36175. PubMed DOI PMC

Bourguignon T, et al. The evolutionary history of termites as inferred from 66 mitochondrial genomes. Mol. Biol. Evol. 2015;32:406–421. doi: 10.1093/molbev/msu308. PubMed DOI

Ometto L, et al. Linking genomics and ecology to investigate the complex evolution of an invasive Drosophila pest. Genome Biol. Evol. 2013;5:745–757. doi: 10.1093/gbe/evt034. PubMed DOI PMC

Bourguignon T, et al. Mitochondrial phylogenomics resolves the global spread of higher termites, ecosystem engineers of the tropics. Mol. Biol. Evol. 2017;34:589–597. PubMed

Ma C, et al. Mitochondrial genomes reveal the global phylogeography and dispersal routes of the migratory locust. Mol. Ecol. 2012;21:4344–4358. doi: 10.1111/j.1365-294X.2012.05684.x. PubMed DOI

Mikheyev AS, et al. Museum genomics confirms that the Lord Howe Island stick insect survived extinction. Curr. Biol. 2017;27:3157–3161. doi: 10.1016/j.cub.2017.08.058. PubMed DOI

Cameron SL. How to sequence and annotate insect mitochondrial genomes for systematic and comparative genomics research. Syst. Entomol. 2014;39:400–411. doi: 10.1111/syen.12071. DOI

Sullivan KAM, Platt RN, II, Bradley RD, Ray DA. Whole mitochondrial genomes provide increased resolution and indicate paraphyly in deer mice. BMC Zool. 2017;2:11. doi: 10.1186/s40850-017-0020-3. DOI

Smith DR. RNA-Seq data: a goldmine for organelle research. Brief. Funct. Genomics. 2013;12:454–456. doi: 10.1093/bfgp/els066. PubMed DOI

Smith DR. The past, present and future of mitochondrial genomics: have we sequenced enough mtDNAs? Brief. Funct. Genomics. 2016;15:47–54. PubMed PMC

Sanitá Lima M, Smith DR. Pervasive transcription of mitochondrial, plastid, and nucleomorph genomes across diverse plastid-bearing species. Genome Biol. Evol. 2017;9:2650–2657. doi: 10.1093/gbe/evx207. PubMed DOI PMC

Williams ST, et al. Curius bivalves: systematic utility and unusual properties of anomalodesmatan mitochondrial genomes. Mol. Phylogenet. Evol. 2017;110:60–72. doi: 10.1016/j.ympev.2017.03.004. PubMed DOI

Wang HL, et al. The characteristics and expression profiles of the mitochondrial genome for the Mediterranean species of the Bemisia tabaci complex. BMC Genomics. 2013;14:401. doi: 10.1186/1471-2164-14-401. PubMed DOI PMC

Tian Y, Smith DR. Recovering complete mitochondrial genome sequences from RNA-Seq: A case study of Polytomella non-photosynthetic green algae. Mol. Phylogenet. Evol. 2016;98:57–62. doi: 10.1016/j.ympev.2016.01.017. PubMed DOI

Moreira DA, Furtado C, Parente TE. The use of transcriptomic next-generation sequencing data to assembly mitochondrial genomes of Ancistrus spp. (Loricariidae) Gene. 2015;573(1):171–175. doi: 10.1016/j.gene.2015.08.059. PubMed DOI

Song N, An S, Yin X, Cai W, Li H. Application of RNA-seq for mitogenome reconstruction, and reconsideration of long-branch artifacts in Hemiptera phylogeny. Sci. Rep. 2016;6:33465. doi: 10.1038/srep33465. PubMed DOI PMC

Bourguignon T, et al. Oceanic dispersal, vicariance and human introduction shaped the modern distribution of the termites Reticulitermes, Heterotermes and Coptotermes. Proc. R. Soc. B. 2016;283:20160179. doi: 10.1098/rspb.2016.0179. PubMed DOI PMC

Dedeine F, et al. Historical biogeography of Reticulitermes termites (Isoptera: Rhinotermitidae) inferred from analyses of mitochondrial and nuclear loci. Mol. Phylogenet. Evol. 2016;94:778–790. doi: 10.1016/j.ympev.2015.10.020. PubMed DOI

Perera PO, Walsh TK, Luttrell LG. Complete mitochondrial genome of Helicoverpa zea (Lepidoptera: Noctuidae) and expression profiles of mitochondrial-encoded genes in early and late embryos. J. Insect Sci. 2016;16:1–10. doi: 10.1093/jisesa/iew023. PubMed DOI PMC

Sun Y, Kurisaki M, Hashiguchi Y, Kumazawa Y. Variation and evolution of polyadenylation profiles in sauropsid mitochondrial mRNAs as deduced from the high-throughput RNA sequencing. BMC Genomics. 2017;18:665. doi: 10.1186/s12864-017-4080-0. PubMed DOI PMC

Ghiselli F, et al. The complete mitochondrial genome of the grooved carpet shell, Ruditapes decussatus (Bivalvia, Veneridae) PeerJ. 2017;5:e3692. doi: 10.7717/peerj.3692. PubMed DOI PMC

Konrad A, et al. Mitochondrial mutation rate, spectrum and heteroplasmy in Caenorhabditis elegans spontaneous mutation accumulation lines of differing population size. Mol. Biol. Evol. 2017;34:1319–1334. PubMed PMC

Timbó RV, Togawa RC, Costa MMC, Andow AD, Paula DP. Mitogenome sequence accuracy using different elucidation methods. PLoS One. 2017;12:e0179971. doi: 10.1371/journal.pone.0179971. PubMed DOI PMC

Mercer TR, et al. The human mitochondrial transcriptome. Cell. 2011;146(4):645–658. doi: 10.1016/j.cell.2011.06.051. PubMed DOI PMC

Boore JL, Brown WM. Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Curr. Biol. 1998;8:668–674. PubMed

Cameron SL, Lo N, Bourguignon T, Svenson GJ, Evans TA. A mitochondrial genome phylogeny of termites (Blattodea: Termitoidae): robust support for interfamilial relationships and molecular synapomorphies define major clades. Mol. Phylogenet. Evol. 2012;65:163–173. doi: 10.1016/j.ympev.2012.05.034. PubMed DOI

Zhang D, et al. Mitochondrial architecture rearrangements produce asymmetrical nonadaptive mutational pressures that subvert the phylogenetic reconstruction in Isopoda. Genome Biol. Evol. 2019;11:1797–1812. doi: 10.1093/gbe/evz121. PubMed DOI PMC

Romiguier J, et al. Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature. 2014;515:261–263. doi: 10.1038/nature13685. PubMed DOI

Mitaka Y, Kobayashi K, Matsuura K. Caste-, sex-, and age-dependent expression of immune-related genes in a Japanese subterranean termite, Reticulitermes speratus. PLoS One. 2017;12:e0175417–22. doi: 10.1371/journal.pone.0175417. PubMed DOI PMC

Sanitá Lima M, Woods LC, Cartwright MW, Smith DR. The (in)complete organelle genome: exploring the use and nonuse of available technologies for characterizing mitochondrial and plastid chromosomes. Mol. Ecol. Res. 2016;16:1279–1286. doi: 10.1111/1755-0998.12585. PubMed DOI

Castandet B, Hotto AM, Strickler SR, Stern DB. ChloroSeq, an optimized chloroplast RNA-Seq bioinformatic pipeline, reveals remodeling of the organellar transcriptome under heat stress. G3-Genes Genom Genet. G3-GENES GENOM. GENET. 2016;6:2817–2827. PubMed PMC

Andrews, S. Fast QC, A Quality Control tool for High Throughput Sequence Data. Available from: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/, last accessed January 2019 (2014).

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie2. Nat. Methods. 2012;9:357–359. doi: 10.1038/nmeth.1923. PubMed DOI PMC

Haas BJ, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 2013;8:1494–1512. doi: 10.1038/nprot.2013.084. PubMed DOI PMC

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Larsson A. AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics. 2014;30:3276–3278. doi: 10.1093/bioinformatics/btu531. PubMed DOI PMC

Huang X, Madan A. CAP3: A DNA sequence assembly program. Genome Res. 1999;9:868–877. doi: 10.1101/gr.9.9.868. PubMed DOI PMC

Katoh K, Kuma KI, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005;33(2):511–518. doi: 10.1093/nar/gki198. PubMed DOI PMC

Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat. Methods. 2015;12:59–60. doi: 10.1038/nmeth.3176. PubMed DOI

Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. 2011;27:2987–2993. doi: 10.1093/bioinformatics/btr509. PubMed DOI PMC

Bernt M, et al. MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet. Evol. 2013;69:313–319. doi: 10.1016/j.ympev.2012.08.023. PubMed DOI

Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010. New Orleans, LA. pp 1–8 (2010).

Kalyaanamoorthy S, et al. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC

Nguyen L-T, Schmidt HA, Haeseler, von A, Minh BQ. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Mol Biol Evol. 2014;32:268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC

Ronquist F, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

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