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Stem Region of tRNA Genes Favors Transition Substitution Towards Keto Bases in Bacteria

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Abstract

Transversion and transition mutations have variable effects on the stability of RNA secondary structure considering that the former destabilizes the double helix geometry to a greater extent by introducing purine:purine (R:R) or pyrimidine:pyrimidine (Y:Y) base pairs. Therefore, transversion frequency is likely to be lower than that of transition in the secondary structure regions of RNA genes. Here, we performed an analysis of transition and transversion frequencies in tRNA genes defined well with secondary structure and compared with the intergenic regions in five bacterial species namely Escherichia coli, Klebsiella pneumoniae, Salmonella enterica, Staphylococcus aureus and Streptococcus pneumoniae using a large genome sequence data set. In general, the transversion frequency was observed to be lower than that of transition in both tRNA genes and intergenic regions. The transition to transversion ratio was observed to be greater in tRNA genes than that in the intergenic regions in all the five bacteria that we studied. Interestingly, the intraspecies base substitution analysis in tRNA genes revealed that non-compensatory substitutions were more frequent than compensatory substitutions in the stem region. Further, transition to transversion ratio in the loop region was observed to be significantly lesser than that among the non-compensatory substitutions in the stem region. This indicated that the transversion is more deleterious than transition in the stem regions. In addition, substitutions from amino bases (A/C) to keto bases (G/T) were also observed to be more than the reverse substitutions in the stem region. Substitution from amino bases to keto bases are likely to facilitate the stable G:U pairing unlike the reverse substitution that facilitates the unstable A:C pairing in the stem region of tRNA. This work provides additional support that the secondary structure of tRNA molecule is what drives the different substitutions in its gene sequence.

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Data Availability

The data underlying this article will be shared on request to the corresponding author S. S. Satapathy.

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Not applicable.

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Acknowledgements

We are highly grateful to anonymous reviewers and Prof. Paul Higgs for their kind suggestions that improved the quality of the manuscript significantly. We thank Dr. Harry Thrope for providing the sequence data. PS is thankful to UGC, GoI New Delhi for the JRF. SSS and SKR are thankful to DBT, GoI for the twinning Grant (BT/PR16361/NER/95/192/2015 date 18-10-2016) to them. SKR and RCD are thankful to DBT, GoI for the twinning Grant BT/PR16182/NER/95/92/2015. SSS is thankful to DBT for the NE Overseas Associateship, which helped him to work in University of Bath. EF, SSS, RCD and SKR are thankful to the society for Molecular Biology and Evolution (SMBE) for holding the satellite meeting at Kaziranga, Assam, India on Dec 14th–6th, 2017, which helped the authors to have collaboration on this work.

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Authors and Affiliations

  1. Department of Computer Science and Engineering, Tezpur University, Napaam, Tezpur, Assam, 784028, India

    Piyali Sen & Siddhartha Sankar Satapathy

  2. Molecular Biology and Biotechnology, Tezpur University, Napaam, Tezpur, Assam, 784028, India

    Ruksana Aziz & Suvendra Kumar Ray

  3. Chemical Sciences, Tezpur University, Napaam, Tezpur, Assam, 784028, India

    Ramesh C. Deka

  4. Department of Biology and Biochemistry, The Milner Centre for Evolution, University of Bath, Bath, BA2 7AY, UK

    Edward J. Feil

  5. Center for Multidisciplinary Research, Tezpur University, Napaam, Tezpur, Assam, 784028, India

    Ramesh C. Deka, Suvendra Kumar Ray & Siddhartha Sankar Satapathy

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  1. Piyali Sen
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  2. Ruksana Aziz
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  3. Ramesh C. Deka
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  4. Edward J. Feil
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Contributions

PS performed the work, analyzed data; PS wrote the computer programs; RCD performed energy calculation of different base pairs; SSS and SKR designed the experiment; PS, RA, SSS, EF and SKR critically analyzed the data; PS, RA, RCD, EF, SKR and SSS wrote the manuscript. All authors have read and approved the manuscript.

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Correspondence to Edward J. Feil, Suvendra Kumar Ray or Siddhartha Sankar Satapathy.

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Handling editor: Arturo Becerra.

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Sen, P., Aziz, R., Deka, R.C. et al. Stem Region of tRNA Genes Favors Transition Substitution Towards Keto Bases in Bacteria. J Mol Evol 90, 114–123 (2022). https://doi.org/10.1007/s00239-021-10045-x

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  • DOI: https://doi.org/10.1007/s00239-021-10045-x

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