TY - JOUR
T1 - Convergent transcription confers a bistable switch in Enterococcus faecalis conjugation
AU - Chatterjee, Anushree
AU - Johnson, Christopher M.
AU - Shu, Che Chi
AU - Kaznessis, Yiannis N.
AU - Ramkrishna, Doraiswami
AU - Dunny, Gary M.
AU - Hu, Wei Shou
PY - 2011/6/7
Y1 - 2011/6/7
N2 - Convergent gene pairs with head-to-head configurations are widespread in both eukaryotic and prokaryotic genomes and are speculated to be involved in gene regulation. Here we present a unique mechanism of gene regulation due to convergent transcription from the antagonistic prgX/prgQ operon in Enterococcus faecalis controlling conjugative transfer of the antibiotic resistance plasmid pCF10 from donor cells to recipient cells. Using mathematical modeling and experimentation, we demonstrate that convergent transcription in the prgX/prgQ operon endows the system with the properties of a robust genetic switch through premature termination of elongating transcripts due to collisions between RNA polymerases (RNAPs) transcribing from opposite directions and antisense regulation between complementary counter-transcripts. Evidence is provided for the presence of truncated RNAs resulting from convergent transcription from both the promoters that are capable of sense-antisense interactions. A mathematical model predicts that both RNAP collision and antisense regulation are essential for a robust bistable switch behavior in the control of conjugation initiation by prgX/prgQ operons. Moreover, given that convergent transcription is conserved across species, the mechanism of coupling RNAP collision and antisense interaction is likely to have a significant regulatory role in gene expression.
AB - Convergent gene pairs with head-to-head configurations are widespread in both eukaryotic and prokaryotic genomes and are speculated to be involved in gene regulation. Here we present a unique mechanism of gene regulation due to convergent transcription from the antagonistic prgX/prgQ operon in Enterococcus faecalis controlling conjugative transfer of the antibiotic resistance plasmid pCF10 from donor cells to recipient cells. Using mathematical modeling and experimentation, we demonstrate that convergent transcription in the prgX/prgQ operon endows the system with the properties of a robust genetic switch through premature termination of elongating transcripts due to collisions between RNA polymerases (RNAPs) transcribing from opposite directions and antisense regulation between complementary counter-transcripts. Evidence is provided for the presence of truncated RNAs resulting from convergent transcription from both the promoters that are capable of sense-antisense interactions. A mathematical model predicts that both RNAP collision and antisense regulation are essential for a robust bistable switch behavior in the control of conjugation initiation by prgX/prgQ operons. Moreover, given that convergent transcription is conserved across species, the mechanism of coupling RNAP collision and antisense interaction is likely to have a significant regulatory role in gene expression.
KW - Gene-regulatory network
KW - Inverse expression
KW - Overlapping DNA
UR - http://www.scopus.com/inward/record.url?scp=79959349542&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=79959349542&partnerID=8YFLogxK
U2 - 10.1073/pnas.1101569108
DO - 10.1073/pnas.1101569108
M3 - Article
C2 - 21606359
AN - SCOPUS:79959349542
SN - 0027-8424
VL - 108
SP - 9721
EP - 9726
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 23
ER -