Experimental discovery of small RNAs in Staphylococcus aureus reveals a riboregulator of central metabolism.
Using an experimental approach, we investigated the RNome of the pathogen Staphylococcus aureus to identify 30 small RNAs (sRNAs) including 14 that are newly confirmed. Among the latter, 10 are encoded in intergenic regions, three are generated by premature transcription termination associated with riboswitch activities, and one is expressed from the complementary strand of a transposase gene. The expression of four sRNAs increases during the transition from exponential to stationary phase. We focused our study on RsaE, an sRNA that is highly conserved in the bacillales order and is deleterious when over-expressed. We show that RsaE interacts in vitro with the 5' region of opp3A mRNA, encoding an ABC transporter component, to prevent formation of the ribosomal initiation complex. A previous report showed that RsaE targets opp3B which is co-transcribed with opp3A. Thus, our results identify an unusual case of riboregulation where the same sRNA controls an operon mRNA by targeting two of its cistrons. A combination of biocomputational and transcriptional analyses revealed a remarkably coordinated RsaE-dependent downregulation of numerous metabolic enzymes involved in the citrate cycle and the folate-dependent one-carbon metabolism. As we observed that RsaE accumulates transiently in late exponential growth, we propose that RsaE functions to ensure a coordinate downregulation of the central metabolism when carbon sources become scarce.
Bohn
Chantal
C
Institut de Génétique et Microbiologie, CNRS/UMR 8621, IFR115, Centre scientifique d'Orsay, Université Paris-Sud, bâtiment 400, 91405 Orsay Cedex, France.
Rigoulay
Candice
C
Chabelskaya
Svetlana
S
Sharma
Cynthia M
CM
Marchais
Antonin
A
Skorski
Patricia
P
Borezée-Durant
Elise
E
Barbet
Romain
R
Jacquet
Eric
E
Jacq
Annick
A
Gautheret
Daniel
D
Felden
Brice
B
Vogel
Jörg
J
Bouloc
Philippe
P
D018528:ATP-Binding Cassette Transporters / Q000235:genetics; D001665:Binding Sites; D002244:Carbon / Q000378:metabolism; D015536:Down-Regulation; D005492:Folic Acid / Q000378:metabolism; D015964:Gene Expression Regulation, Bacterial; D012329:RNA, Bacterial / Q000235:genetics / Q000378:metabolism; D012333:RNA, Messenger / Q000378:metabolism; D058727:RNA, Small Untranslated / Q000235:genetics / Q000378:metabolism*; D012270:Ribosomes / Q000378:metabolism; D058928:Riboswitch; D013211:Staphylococcus aureus / Q000235:genetics* / Q000378:metabolism
D018528:ATP-Binding Cassette Transporters; D012329:RNA, Bacterial; D012333:RNA, Messenger; D058727:RNA, Small Untranslated; D058928:Riboswitch; D002244:Carbon; D005492:Folic Acid