Unconventional mRNA processing and degradation pathways for the polycistronic yrzI (spyTA) mRNA in Bacillus subtilis.

The ribosome-associated endoribonuclease Rae1 cleaves the Bacillus subtilis yrzI operon mRNA in a translation-dependent manner. This operon encodes up to four small peptides, S1027, YrzI, S1025, and S1024, whose functions are unknown. Here, we identified the function of YrzI and S1025 and deciphered the degradation pathways of the yrzI polycistronic mRNA. We show that YrzI is toxic at high concentrations, but co-expression with S1025 abolishes its toxicity, and that, in the absence of Rae1, S1025 is the major antidote to the YzI toxin. We show that a highly stable mRNA species containing the YrzI and S1025 open reading frames results from endoribonucleolytic cleavage upstream of yrzI followed by the arrest of 5'-exoribonucleolytic processing by ribosomes bound to its exceptionally strong Shine-Dalgarno sequence. Degradation of this mRNA requires either translation-dependent cleavage within S1025 by Rae1 or direct attack from the structured 3'-end by 3'-exoribonucleases. Neither pathway is common for a B. subtilis mRNA.