Arm-less mitochondrial tRNAs conserved for over 30 millions of years in spiders

Joan Pons,Miquel A Arnedo,Pere Bover,Leticia Bidegaray-Batista

doi:10.1186/s12864-019-6026-1

Abstract

BackgroundIn recent years, Next Generation Sequencing (NGS) has accelerated the generation of full mitogenomes, providing abundant material for studying different aspects of molecular evolution. Some mitogenomes have been observed to harbor atypical sequences with bizarre secondary structures, which origins and significance could only be fully understood in an evolutionary framework.ResultsHere we report and analyze the mitochondrial sequences and gene arrangements of six closely related spiders in the sister genera Parachtes and Harpactocrates, which belong to the nocturnal, ground dwelling family Dysderidae. Species of both genera have compacted mitogenomes with many overlapping genes and strikingly reduced tRNAs that are among the shortest described within metazoans. Thanks to the conservation of the gene order and the nucleotide identity across close relatives, we were able to predict the secondary structures even on arm-less tRNAs, which would be otherwise unattainable for a single species. They exhibit aberrant secondary structures with the lack of either DHU or TΨC arms and many miss-pairings in the acceptor arm but this degeneracy trend goes even further since at least four tRNAs are arm-less in the six spider species studied.ConclusionsThe conservation of at least four arm-less tRNA genes in two sister spider genera for about 30 myr suggest that these genes are still encoding fully functional tRNAs though they may be post-transcriptionally edited to be fully functional as previously described in other species. We suggest that the presence of overlapping and truncated tRNA genes may be related and explains why spider mitogenomes are smaller than those of other invertebrates.

Highlights

In recent years, Generation Sequencing (NGS) has accelerated the generation of full mitogenomes, providing abundant material for studying different aspects of molecular evolution
The gene order found in Parachtes and Harpactocrates is a new discovery in spiders and it seems to arise from a translocation involving trnI and a large gene block
Our study reveals that Parachtes and Harpactocrates spiders have taken Transfer RNA (tRNA) reduction to an extreme, since none of the 22 tRNAs had a cloverleaf structure and at least four of them lack both DHU and TΨC arms

Summary

Introduction

Generation Sequencing (NGS) has accelerated the generation of full mitogenomes, providing abundant material for studying different aspects of molecular evolution. Mitogenomes share some distinctive features such as A + T richness, at third codon sites and control region [7], and conservation of secondary structures of tRNAs and rRNAs, despite primary sequences may vary greatly across taxonomic groups and even between close relatives [5, 6]. Some other mitogenomic studies have payed attention to the evolution of this reduced genome itself, addressing questions about the frequencies of nucleotide and amino acid sequences, codon usage, secondary structures of RNA genes and compensatory substitutions, and control regions and origin of replication across genes and species, e.g. We interrogate on aspects of the secondary structure of mitochondrial tRNAs in spiders, by sequencing the mitogenomes of several representatives of the family Dysderidae, which belongs to the Synspermiata [17,18,19], one of the main evolutionary lineages within spiders (Fig. 1). Synspermiata includes 17 families, only one mitogenome is currently available in public organelle databases, that of the common cellar spider Pholcus phalangioides (Pholcidae)

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Conclusion