Structural signatures of thermal adaptation of bacterial ribosomal RNA, transfer RNA, and messenger RNA

Clara Jegousse; Yuedong Yang; Jian Zhan; Jihua Wang; Yaoqi Zhou

doi:10.1371/journal.pone.0184722

Structural signatures of thermal adaptation of bacterial ribosomal RNA, transfer RNA, and messenger RNA

PLoS One. 2017 Sep 14;12(9):e0184722. doi: 10.1371/journal.pone.0184722. eCollection 2017.

Authors

Clara Jegousse^{1

2}, Yuedong Yang², Jian Zhan², Jihua Wang³, Yaoqi Zhou^{2

3}

Affiliations

¹ UFR Sciences et Techniques, Université de Nantes, 2 rue de la Houssinière, Nantes, France.
² Institute for Glycomics and School of Information and Communication Technology, Griffith University, Gold Coast, QLD, Australia.
³ Shandong Provincial Key Laboratory of Biophysics, Institute of Biophysics, Dezhou University, Dezhou, China.

Abstract

Temperature adaptation of bacterial RNAs is a subject of both fundamental and practical interest because it will allow a better understanding of molecular mechanism of RNA folding with potential industrial application of functional thermophilic or psychrophilic RNAs. Here, we performed a comprehensive study of rRNA, tRNA, and mRNA of more than 200 bacterial species with optimal growth temperatures (OGT) ranging from 4°C to 95°C. We investigated temperature adaptation at primary, secondary and tertiary structure levels. We showed that unlike mRNA, tRNA and rRNA were optimized for their structures at compositional levels with significant tertiary structural features even for their corresponding randomly permutated sequences. tRNA and rRNA are more exposed to solvent but remain structured for hyperthermophiles with nearly OGT-independent fluctuation of solvent accessible surface area within a single RNA chain. mRNA in hyperthermophiles is essentially the same as random sequences without tertiary structures although many mRNA in mesophiles and psychrophiles have well-defined tertiary structures based on their low overall solvent exposure with clear separation of deeply buried from partly exposed bases as in tRNA and rRNA. These results provide new insight into temperature adaptation of different RNAs.

MeSH terms

Bacteria / genetics*
Databases, Genetic
Models, Molecular
Nucleic Acid Conformation
RNA Folding / drug effects
RNA, Bacterial / chemistry
RNA, Bacterial / drug effects
RNA, Messenger / chemistry*
RNA, Messenger / drug effects
RNA, Ribosomal / chemistry*
RNA, Ribosomal / drug effects
RNA, Transfer / chemistry*
RNA, Transfer / drug effects
Solvents / pharmacology
Temperature

Substances

RNA, Bacterial
RNA, Messenger
RNA, Ribosomal
Solvents
RNA, Transfer

Grants and funding

This work was supported in part by National Natural Science Foundation of China (61671107) to YY and JW, by the Taishan Scholars Program of Shandong province of China, National Natural Science Foundation of China (61540025), and National Health and Medical Research Council (1059775 and 1083450) of Australia to YZ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.