An epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element

Horizontal transfer of the integrative and conjugative element ICEMlSymR7A converts non-symbiotic Mesorhizobium spp. into nitrogen-fixing legume symbionts. Here, we discover subpopulations of Mesorhizobium japonicum R7A become epigenetically primed for quorum-sensing (QS) and QS-activated horizontal...

Full description

Bibliographic Details
Main Authors: Ramsay, Josh, Bastholm, T.R., Verdonk, Callum J., Tambalo, D.D., Sullivan, J.T., Harold, L.K., Panganiban, Beatrice A., Colombi, Elena, Perry, B.J., Jowsey, W., Morris, C., Hynes, M.F., Bond, C.S., Cameron, A.D.S., Yost, C.K., Ronson, C.W.
Format: Journal Article
Language:English
Published: OXFORD UNIV PRESS 2022
Subjects:
Online Access:http://purl.org/au-research/grants/arc/FT170100235
http://hdl.handle.net/20.500.11937/89033
_version_ 1848765143724326912
author Ramsay, Josh
Bastholm, T.R.
Verdonk, Callum J.
Tambalo, D.D.
Sullivan, J.T.
Harold, L.K.
Panganiban, Beatrice A.
Colombi, Elena
Perry, B.J.
Jowsey, W.
Morris, C.
Hynes, M.F.
Bond, C.S.
Cameron, A.D.S.
Yost, C.K.
Ronson, C.W.
author_facet Ramsay, Josh
Bastholm, T.R.
Verdonk, Callum J.
Tambalo, D.D.
Sullivan, J.T.
Harold, L.K.
Panganiban, Beatrice A.
Colombi, Elena
Perry, B.J.
Jowsey, W.
Morris, C.
Hynes, M.F.
Bond, C.S.
Cameron, A.D.S.
Yost, C.K.
Ronson, C.W.
author_sort Ramsay, Josh
building Curtin Institutional Repository
collection Online Access
description Horizontal transfer of the integrative and conjugative element ICEMlSymR7A converts non-symbiotic Mesorhizobium spp. into nitrogen-fixing legume symbionts. Here, we discover subpopulations of Mesorhizobium japonicum R7A become epigenetically primed for quorum-sensing (QS) and QS-activated horizontal transfer. Isolated populations in this state termed R7A* maintained these phenotypes in laboratory culture but did not transfer the R7A* state to recipients of ICEMlSymR7A following conjugation. We previously demonstrated ICEMlSymR7A transfer and QS are repressed by the antiactivator QseM in R7A populations and that the adjacently-coded DNA-binding protein QseC represses qseM transcription. Here RNA-sequencing revealed qseM expression was repressed in R7A* cells and that RNA antisense to qseC was abundant in R7A but not R7A*. Deletion of the antisense-qseC promoter converted cells into an R7A*-like state. An adjacently coded QseC2 protein bound two operator sites and repressed antisense-qseC transcription. Plasmid overexpression of QseC2 stimulated the R7A* state, which persisted following curing of this plasmid. The epigenetic maintenance of the R7A* state required ICEMlSymR7A-encoded copies of both qseC and qseC2. Therefore, QseC and QseC2, together with their DNA-binding sites and overlapping promoters, form a stable epigenetic switch that establishes binary control over qseM transcription and primes a subpopulation of R7A cells for QS and horizontal transfer.
first_indexed 2025-11-14T11:30:34Z
format Journal Article
id curtin-20.500.11937-89033
institution Curtin University Malaysia
institution_category Local University
language English
last_indexed 2025-11-14T11:30:34Z
publishDate 2022
publisher OXFORD UNIV PRESS
recordtype eprints
repository_type Digital Repository
spelling curtin-20.500.11937-890332022-08-19T06:38:20Z An epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element Ramsay, Josh Bastholm, T.R. Verdonk, Callum J. Tambalo, D.D. Sullivan, J.T. Harold, L.K. Panganiban, Beatrice A. Colombi, Elena Perry, B.J. Jowsey, W. Morris, C. Hynes, M.F. Bond, C.S. Cameron, A.D.S. Yost, C.K. Ronson, C.W. Science & Technology Life Sciences & Biomedicine Biochemistry & Molecular Biology SYMBIOSIS ISLAND MESORHIZOBIUM-LOTI TRANSCRIPTION REGULATION BACILLUS-SUBTILIS GENE PLASMID BISTABILITY EXPRESSION EVOLUTION PROTEIN Horizontal transfer of the integrative and conjugative element ICEMlSymR7A converts non-symbiotic Mesorhizobium spp. into nitrogen-fixing legume symbionts. Here, we discover subpopulations of Mesorhizobium japonicum R7A become epigenetically primed for quorum-sensing (QS) and QS-activated horizontal transfer. Isolated populations in this state termed R7A* maintained these phenotypes in laboratory culture but did not transfer the R7A* state to recipients of ICEMlSymR7A following conjugation. We previously demonstrated ICEMlSymR7A transfer and QS are repressed by the antiactivator QseM in R7A populations and that the adjacently-coded DNA-binding protein QseC represses qseM transcription. Here RNA-sequencing revealed qseM expression was repressed in R7A* cells and that RNA antisense to qseC was abundant in R7A but not R7A*. Deletion of the antisense-qseC promoter converted cells into an R7A*-like state. An adjacently coded QseC2 protein bound two operator sites and repressed antisense-qseC transcription. Plasmid overexpression of QseC2 stimulated the R7A* state, which persisted following curing of this plasmid. The epigenetic maintenance of the R7A* state required ICEMlSymR7A-encoded copies of both qseC and qseC2. Therefore, QseC and QseC2, together with their DNA-binding sites and overlapping promoters, form a stable epigenetic switch that establishes binary control over qseM transcription and primes a subpopulation of R7A cells for QS and horizontal transfer. 2022 Journal Article http://hdl.handle.net/20.500.11937/89033 10.1093/nar/gkab1217 English http://purl.org/au-research/grants/arc/FT170100235 http://creativecommons.org/licenses/by-nc/4.0/ OXFORD UNIV PRESS fulltext
spellingShingle Science & Technology
Life Sciences & Biomedicine
Biochemistry & Molecular Biology
SYMBIOSIS ISLAND
MESORHIZOBIUM-LOTI
TRANSCRIPTION REGULATION
BACILLUS-SUBTILIS
GENE
PLASMID
BISTABILITY
EXPRESSION
EVOLUTION
PROTEIN
Ramsay, Josh
Bastholm, T.R.
Verdonk, Callum J.
Tambalo, D.D.
Sullivan, J.T.
Harold, L.K.
Panganiban, Beatrice A.
Colombi, Elena
Perry, B.J.
Jowsey, W.
Morris, C.
Hynes, M.F.
Bond, C.S.
Cameron, A.D.S.
Yost, C.K.
Ronson, C.W.
An epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element
title An epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element
title_full An epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element
title_fullStr An epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element
title_full_unstemmed An epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element
title_short An epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element
title_sort epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element
topic Science & Technology
Life Sciences & Biomedicine
Biochemistry & Molecular Biology
SYMBIOSIS ISLAND
MESORHIZOBIUM-LOTI
TRANSCRIPTION REGULATION
BACILLUS-SUBTILIS
GENE
PLASMID
BISTABILITY
EXPRESSION
EVOLUTION
PROTEIN
url http://purl.org/au-research/grants/arc/FT170100235
http://hdl.handle.net/20.500.11937/89033