Enhanced uptake of potassium or glycine betaine or export of cyclic-di-AMP restores osmoresistance in a high cyclic-di-AMP Lactococcus lactis mutant
The broadly conserved bacterial signalling molecule cyclic-di-adenosine monophosphate (c-di-AMP) controls osmoresistance via its regulation of potassium (K+) and compatible solute uptake. High levels of c-di-AMP resulting from inactivation of c-di-AMP phosphodiesterase activity leads to poor growth...
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Published in | PLoS genetics Vol. 14; no. 8; p. e1007574 |
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Main Authors | , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
03.08.2018
Public Library of Science (PLoS) |
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Abstract | The broadly conserved bacterial signalling molecule cyclic-di-adenosine monophosphate (c-di-AMP) controls osmoresistance via its regulation of potassium (K+) and compatible solute uptake. High levels of c-di-AMP resulting from inactivation of c-di-AMP phosphodiesterase activity leads to poor growth of bacteria under high osmotic conditions. To better understand how bacteria can adjust in response to excessive c-di-AMP levels and to identify signals that feed into the c-di-AMP network, we characterised genes identified in a screen for osmoresistant suppressor mutants of the high c-di-AMP Lactococcus ΔgdpP strain. Mutations were identified which increased the uptake of osmoprotectants, including gain-of-function mutations in a Kup family K+ importer (KupB) and inactivation of the glycine betaine transporter transcriptional repressor BusR. The KupB mutations increased the intracellular K+ level while BusR inactivation increased the glycine betaine level. In addition, BusR was found to directly bind c-di-AMP and repress expression of the glycine betaine transporter in response to elevated c-di-AMP. Interestingly, overactive KupB activity or loss of BusR triggered c-di-AMP accumulation, suggesting turgor pressure changes act as a signal for this second messenger. In another group of suppressors, overexpression of an operon encoding an EmrB family multidrug resistance protein allowed cells to lower their intracellular level of c-di-AMP through active export. Lastly evidence is provided that c-di-AMP levels in several bacteria are rapidly responsive to environmental osmolarity changes. Taken together, this work provides evidence for a model in which high c-di-AMP containing cells are dehydrated due to lower K+ and compatible solute levels and that this osmoregulation system is able to sense and respond to cellular water stress. |
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AbstractList | The broadly conserved bacterial signalling molecule cyclic-di-adenosine monophosphate (c-di-AMP) controls osmoresistance via its regulation of potassium (K.sup.+) and compatible solute uptake. High levels of c-di-AMP resulting from inactivation of c-di-AMP phosphodiesterase activity leads to poor growth of bacteria under high osmotic conditions. To better understand how bacteria can adjust in response to excessive c-di-AMP levels and to identify signals that feed into the c-di-AMP network, we characterised genes identified in a screen for osmoresistant suppressor mutants of the high c-di-AMP Lactococcus [DELTA]gdpP strain. Mutations were identified which increased the uptake of osmoprotectants, including gain-of-function mutations in a Kup family K.sup.+ importer (KupB) and inactivation of the glycine betaine transporter transcriptional repressor BusR. The KupB mutations increased the intracellular K.sup.+ level while BusR inactivation increased the glycine betaine level. In addition, BusR was found to directly bind c-di-AMP and repress expression of the glycine betaine transporter in response to elevated c-di-AMP. Interestingly, overactive KupB activity or loss of BusR triggered c-di-AMP accumulation, suggesting turgor pressure changes act as a signal for this second messenger. In another group of suppressors, overexpression of an operon encoding an EmrB family multidrug resistance protein allowed cells to lower their intracellular level of c-di-AMP through active export. Lastly evidence is provided that c-di-AMP levels in several bacteria are rapidly responsive to environmental osmolarity changes. Taken together, this work provides evidence for a model in which high c-di-AMP containing cells are dehydrated due to lower K.sup.+ and compatible solute levels and that this osmoregulation system is able to sense and respond to cellular water stress. The broadly conserved bacterial signalling molecule cyclic-di-adenosine monophosphate (c-di-AMP) controls osmoresistance via its regulation of potassium (K+) and compatible solute uptake. High levels of c-di-AMP resulting from inactivation of c-di-AMP phosphodiesterase activity leads to poor growth of bacteria under high osmotic conditions. To better understand how bacteria can adjust in response to excessive c-di-AMP levels and to identify signals that feed into the c-di-AMP network, we characterised genes identified in a screen for osmoresistant suppressor mutants of the high c-di-AMP Lactococcus ΔgdpP strain. Mutations were identified which increased the uptake of osmoprotectants, including gain-of-function mutations in a Kup family K+ importer (KupB) and inactivation of the glycine betaine transporter transcriptional repressor BusR. The KupB mutations increased the intracellular K+ level while BusR inactivation increased the glycine betaine level. In addition, BusR was found to directly bind c-di-AMP and repress expression of the glycine betaine transporter in response to elevated c-di-AMP. Interestingly, overactive KupB activity or loss of BusR triggered c-di-AMP accumulation, suggesting turgor pressure changes act as a signal for this second messenger. In another group of suppressors, overexpression of an operon encoding an EmrB family multidrug resistance protein allowed cells to lower their intracellular level of c-di-AMP through active export. Lastly evidence is provided that c-di-AMP levels in several bacteria are rapidly responsive to environmental osmolarity changes. Taken together, this work provides evidence for a model in which high c-di-AMP containing cells are dehydrated due to lower K+ and compatible solute levels and that this osmoregulation system is able to sense and respond to cellular water stress. The broadly conserved bacterial signalling molecule cyclic-di-adenosine monophosphate (c-di-AMP) controls osmoresistance via its regulation of potassium (K + ) and compatible solute uptake. High levels of c-di-AMP resulting from inactivation of c-di-AMP phosphodiesterase activity leads to poor growth of bacteria under high osmotic conditions. To better understand how bacteria can adjust in response to excessive c-di-AMP levels and to identify signals that feed into the c-di-AMP network, we characterised genes identified in a screen for osmoresistant suppressor mutants of the high c-di-AMP Lactococcus Δ gdpP strain. Mutations were identified which increased the uptake of osmoprotectants, including gain-of-function mutations in a Kup family K + importer (KupB) and inactivation of the glycine betaine transporter transcriptional repressor BusR. The KupB mutations increased the intracellular K + level while BusR inactivation increased the glycine betaine level. In addition, BusR was found to directly bind c-di-AMP and repress expression of the glycine betaine transporter in response to elevated c-di-AMP. Interestingly, overactive KupB activity or loss of BusR triggered c-di-AMP accumulation, suggesting turgor pressure changes act as a signal for this second messenger. In another group of suppressors, overexpression of an operon encoding an EmrB family multidrug resistance protein allowed cells to lower their intracellular level of c-di-AMP through active export. Lastly evidence is provided that c-di-AMP levels in several bacteria are rapidly responsive to environmental osmolarity changes. Taken together, this work provides evidence for a model in which high c-di-AMP containing cells are dehydrated due to lower K + and compatible solute levels and that this osmoregulation system is able to sense and respond to cellular water stress. Second messengers relay signals received from the environment to intracellular targets that adjust cellular physiology. One widespread bacterial cyclic-dinucleotide signalling molecule, cyclic-di-AMP (c-di-AMP) has been shown to regulate a range of cellular processes via binding to protein and riboswitch targets, with most identified thus far being linked to osmoregulation functions. C-di-AMP levels need to be carefully tuned under different environmental conditions to allow optimal growth. Here we show that a Lactococcus lactis GdpP phosphodiesterase mutant with a high intracellular pool of c-di-AMP is able to grow under hyperosmotic conditions after acquiring mutations which increase osmolyte (potassium [K + ] or compatible solute) uptake or by actively exporting c-di-AMP. Interestingly, elevated K + or glycine betaine uptake triggered accumulation of c-di-AMP and environmental osmolarity changes were also found to significantly impact c-di-AMP levels in various bacteria. These results support a model in which c-di-AMP negatively impacts osmoresistance through inhibition of the import of osmoprotectants and this system can sense both cellular and environmental changes causing water stress. |
Audience | Academic |
Author | Liang, Zhao-Xun Pham, Huong Thi Huynh, TuAnh Ngoc Woodward, Joshua J Nhiep, Nguyen Thi Hanh Howard, Christopher B Vu, Thu Ngoc Minh Chakrabortti, Alolika Turner, Mark S Bansal, Nidhi Huynh, Anh Le Diep Zhu, Yan Marcellin, Esteban Lo, Raquel |
AuthorAffiliation | 3 Department of Microbiology, University of Washington, Seattle, WA, United States of America The University of Texas Health Science Center at Houston, UNITED STATES 4 Monash Biomedicine Discovery Institute, Monash University, Melbourne, Australia 6 Australian Institute for Bioengineering and Nanotechnology, University of Queensland, Brisbane, Queensland, Australia 5 School of Biological Sciences, Nanyang Technological University, Singapore 1 School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland, Australia 7 Queensland Alliance for Agriculture and Food Innovation, University of Queensland, Brisbane, Queensland, Australia 2 The University of Danang, University of Science and Technology, Da Nang, Vietnam |
AuthorAffiliation_xml | – name: 3 Department of Microbiology, University of Washington, Seattle, WA, United States of America – name: 2 The University of Danang, University of Science and Technology, Da Nang, Vietnam – name: 6 Australian Institute for Bioengineering and Nanotechnology, University of Queensland, Brisbane, Queensland, Australia – name: 4 Monash Biomedicine Discovery Institute, Monash University, Melbourne, Australia – name: 1 School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland, Australia – name: 7 Queensland Alliance for Agriculture and Food Innovation, University of Queensland, Brisbane, Queensland, Australia – name: 5 School of Biological Sciences, Nanyang Technological University, Singapore – name: The University of Texas Health Science Center at Houston, UNITED STATES |
Author_xml | – sequence: 1 givenname: Huong Thi orcidid: 0000-0003-1769-6713 surname: Pham fullname: Pham, Huong Thi organization: The University of Danang, University of Science and Technology, Da Nang, Vietnam – sequence: 2 givenname: Nguyen Thi Hanh orcidid: 0000-0001-7973-3386 surname: Nhiep fullname: Nhiep, Nguyen Thi Hanh organization: School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland, Australia – sequence: 3 givenname: Thu Ngoc Minh orcidid: 0000-0002-2344-1234 surname: Vu fullname: Vu, Thu Ngoc Minh organization: School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland, Australia – sequence: 4 givenname: TuAnh Ngoc surname: Huynh fullname: Huynh, TuAnh Ngoc organization: Department of Microbiology, University of Washington, Seattle, WA, United States of America – sequence: 5 givenname: Yan orcidid: 0000-0001-7342-3782 surname: Zhu fullname: Zhu, Yan organization: Monash Biomedicine Discovery Institute, Monash University, Melbourne, Australia – sequence: 6 givenname: Anh Le Diep surname: Huynh fullname: Huynh, Anh Le Diep organization: School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland, Australia – sequence: 7 givenname: Alolika surname: Chakrabortti fullname: Chakrabortti, Alolika organization: School of Biological Sciences, Nanyang Technological University, Singapore – sequence: 8 givenname: Esteban surname: Marcellin fullname: Marcellin, Esteban organization: Australian Institute for Bioengineering and Nanotechnology, University of Queensland, Brisbane, Queensland, Australia – sequence: 9 givenname: Raquel surname: Lo fullname: Lo, Raquel organization: School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland, Australia – sequence: 10 givenname: Christopher B orcidid: 0000-0001-9797-8686 surname: Howard fullname: Howard, Christopher B organization: Australian Institute for Bioengineering and Nanotechnology, University of Queensland, Brisbane, Queensland, Australia – sequence: 11 givenname: Nidhi surname: Bansal fullname: Bansal, Nidhi organization: School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland, Australia – sequence: 12 givenname: Joshua J orcidid: 0000-0002-4630-403X surname: Woodward fullname: Woodward, Joshua J organization: Department of Microbiology, University of Washington, Seattle, WA, United States of America – sequence: 13 givenname: Zhao-Xun surname: Liang fullname: Liang, Zhao-Xun organization: School of Biological Sciences, Nanyang Technological University, Singapore – sequence: 14 givenname: Mark S orcidid: 0000-0003-2770-852X surname: Turner fullname: Turner, Mark S organization: Queensland Alliance for Agriculture and Food Innovation, University of Queensland, Brisbane, Queensland, Australia |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30074984$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | COPYRIGHT 2018 Public Library of Science 2018 Pham et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2018 Pham et al 2018 Pham et al |
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Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The authors have declared that no competing interests exist. Current address: Food Science Department, University of Wisconsin–Madison, Madison, Wisconsin, United States of America. |
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Snippet | The broadly conserved bacterial signalling molecule cyclic-di-adenosine monophosphate (c-di-AMP) controls osmoresistance via its regulation of potassium (K+)... The broadly conserved bacterial signalling molecule cyclic-di-adenosine monophosphate (c-di-AMP) controls osmoresistance via its regulation of potassium... The broadly conserved bacterial signalling molecule cyclic-di-adenosine monophosphate (c-di-AMP) controls osmoresistance via its regulation of potassium (K + )... |
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SubjectTerms | ABC transporters Adenosine Monophosphate AMP Bacteria Bacterial Proteins - genetics Bacterial Proteins - physiology Betaine - metabolism Bioengineering Biology and Life Sciences Cell division Cyclic AMP - metabolism E coli Enzymes Food Funding Gene Expression Regulation, Bacterial Glycine Glycine betaine Gram-positive bacteria Intracellular Lactococcus Lactococcus lactis - genetics Lactococcus lactis - physiology Medicine and Health Sciences Multidrug resistance Mutation Nanotechnology Operon Osmolar Concentration Osmolarity Osmoprotectants Osmoregulation Phosphodiesterase Physical Sciences Physiological aspects Potassium Potassium (Nutrient) Potassium - metabolism Proteins Research and Analysis Methods Second Messenger Systems Sensors Streptococcus infections Supervision Transcription Turgor Water stress |
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Title | Enhanced uptake of potassium or glycine betaine or export of cyclic-di-AMP restores osmoresistance in a high cyclic-di-AMP Lactococcus lactis mutant |
URI | https://www.ncbi.nlm.nih.gov/pubmed/30074984 https://www.proquest.com/docview/2250664202 https://search.proquest.com/docview/2083713315 https://pubmed.ncbi.nlm.nih.gov/PMC6108528 https://doaj.org/article/b18b53e2941a40ed99bddeff8d3a0c37 http://dx.doi.org/10.1371/journal.pgen.1007574 |
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