Initiation of mRNA decay in bacteria

Soumaya Laalami,Léna Zig,Harald Putzer

doi:10.1007/s00018-013-1472-4

Abstract

The instability of messenger RNA is fundamental to the control of gene expression. In bacteria, mRNA degradation generally follows an “all-or-none” pattern. This implies that if control is to be efficient, it must occur at the initiating (and presumably rate-limiting) step of the degradation process. Studies of E. coli and B. subtilis, species separated by 3 billion years of evolution, have revealed the principal and very disparate enzymes involved in this process in the two organisms. The early view that mRNA decay in these two model organisms is radically different has given way to new models that can be resumed by “different enzymes—similar strategies”. The recent characterization of key ribonucleases sheds light on an impressive case of convergent evolution that illustrates that the surprisingly similar functions of these totally unrelated enzymes are of general importance to RNA metabolism in bacteria. We now know that the major mRNA decay pathways initiate with an endonucleolytic cleavage in E. coli and B. subtilis and probably in many of the currently known bacteria for which these organisms are considered representative. We will discuss here the different pathways of eubacterial mRNA decay, describe the major players and summarize the events that can precede and/or favor nucleolytic inactivation of a mRNA, notably the role of the 5′ end and translation initiation. Finally, we will discuss the role of subcellular compartmentalization of transcription, translation, and the RNA degradation machinery.

Highlights

The 5′ P RNA is destroyed via the 5′ tethering mechanism described above involving RNase E in E. coli, whereas in B. subtilis the Messenger RNA (mRNA) is subject to the monophosphate-dependent 5′ exonuclease activity of RNase J1 (Fig. 3b)
Bulk mRNA stability and the abundance of a majority of transcripts in E. coli appear to be much less affected by disruption of RppH than RNase E [90], but even before the discovery of RppH there was speculation that RNase E might initiate mRNA decay without being tethered to the 5′ end, in a pathway called the “internal entry” or “direct entry” model [5, 11, 60, 145, 146]
A quite different picture of the interplay translation-mRNA decay emerges when we look at organisms that do not contain RNase E like many Gram-positive Bacilli

Summary

Introduction

Inactivation of RppH affects the stability of only about 10 % of all mRNAs in E. coli [90], suggesting that the decay of a majority of transcripts is initiated via other routes, notably the direct entry pathway (see below). The 5′ P RNA is destroyed via the 5′ tethering mechanism described above involving RNase E in E. coli, whereas in B. subtilis the mRNA is subject to the monophosphate-dependent 5′ exonuclease activity of RNase J1 (Fig. 3b).

Results

Conclusion