Cyclic nucleotides in archaea: Cyclic di‐AMP in the archaeon Haloferax volcanii and its putative role

Abstract The role of cyclic nucleotides as second messengers for intracellular signal transduction has been well described in bacteria. One recently discovered bacterial second messenger is cyclic di‐adenylate monophosphate (c‐di‐AMP), which has been demonstrated to be essential in bacteria. Compare...

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Main Authors: Frank Braun, Laura Thomalla, Chris van derDoes, Tessa E. F. Quax, Thorsten Allers, Volkhard Kaever, Sonja‐Verena Albers
Format: Article
Language:English
Published: Wiley 2019-09-01
Series:MicrobiologyOpen
Subjects:
Online Access:https://doi.org/10.1002/mbo3.829
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author Frank Braun
Laura Thomalla
Chris van derDoes
Tessa E. F. Quax
Thorsten Allers
Volkhard Kaever
Sonja‐Verena Albers
author_facet Frank Braun
Laura Thomalla
Chris van derDoes
Tessa E. F. Quax
Thorsten Allers
Volkhard Kaever
Sonja‐Verena Albers
author_sort Frank Braun
collection DOAJ
description Abstract The role of cyclic nucleotides as second messengers for intracellular signal transduction has been well described in bacteria. One recently discovered bacterial second messenger is cyclic di‐adenylate monophosphate (c‐di‐AMP), which has been demonstrated to be essential in bacteria. Compared to bacteria, significantly less is known about second messengers in archaea. This study presents the first evidence of in vivo presence of c‐di‐AMP in an archaeon. The model organism Haloferax volcanii was demonstrated to produce c‐di‐AMP. Its genome encodes one diadenylate cyclase (DacZ) which was shown to produce c‐di‐AMP in vitro. Similar to bacteria, the dacZ gene is essential and homologous overexpression of DacZ leads to cell death, suggesting the need for tight regulation of c‐di‐AMP levels. Such tight regulation often indicates the control of important regulatory processes. A central target of c‐di‐AMP signaling in bacteria is cellular osmohomeostasis. The results presented here suggest a comparable function in H. volcanii. A strain with decreased c‐di‐AMP levels exhibited an increased cell area in hypo‐salt medium, implying impaired osmoregulation. In summary, this study expands the field of research on c‐di‐AMP and its physiological function to archaea and indicates that osmoregulation is likely to be a common function of c‐di‐AMP in bacteria and archaea.
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spelling doaj.art-d2c3afdeac1145f196428d284a8b9a2b2022-12-21T20:06:34ZengWileyMicrobiologyOpen2045-88272019-09-0189n/an/a10.1002/mbo3.829Cyclic nucleotides in archaea: Cyclic di‐AMP in the archaeon Haloferax volcanii and its putative roleFrank Braun0Laura Thomalla1Chris van derDoes2Tessa E. F. Quax3Thorsten Allers4Volkhard Kaever5Sonja‐Verena Albers6Molecular Biology of Archaea Institute of Biology, University of Freiburg Freiburg GermanyMolecular Biology of Archaea Institute of Biology, University of Freiburg Freiburg GermanyMolecular Biology of Archaea Institute of Biology, University of Freiburg Freiburg GermanyMolecular Biology of Archaea Institute of Biology, University of Freiburg Freiburg GermanySchool of Life Sciences, Queen's Medical Centre University of Nottingham Nottingham UKResearch Core Unit Metabolomics, Hannover Medical School Hannover GermanyMolecular Biology of Archaea Institute of Biology, University of Freiburg Freiburg GermanyAbstract The role of cyclic nucleotides as second messengers for intracellular signal transduction has been well described in bacteria. One recently discovered bacterial second messenger is cyclic di‐adenylate monophosphate (c‐di‐AMP), which has been demonstrated to be essential in bacteria. Compared to bacteria, significantly less is known about second messengers in archaea. This study presents the first evidence of in vivo presence of c‐di‐AMP in an archaeon. The model organism Haloferax volcanii was demonstrated to produce c‐di‐AMP. Its genome encodes one diadenylate cyclase (DacZ) which was shown to produce c‐di‐AMP in vitro. Similar to bacteria, the dacZ gene is essential and homologous overexpression of DacZ leads to cell death, suggesting the need for tight regulation of c‐di‐AMP levels. Such tight regulation often indicates the control of important regulatory processes. A central target of c‐di‐AMP signaling in bacteria is cellular osmohomeostasis. The results presented here suggest a comparable function in H. volcanii. A strain with decreased c‐di‐AMP levels exhibited an increased cell area in hypo‐salt medium, implying impaired osmoregulation. In summary, this study expands the field of research on c‐di‐AMP and its physiological function to archaea and indicates that osmoregulation is likely to be a common function of c‐di‐AMP in bacteria and archaea.https://doi.org/10.1002/mbo3.829archaeacyclic di‐AMPdiadenylate cyclaseHaloferax volcaniiosmoregulationsecond messenger
spellingShingle Frank Braun
Laura Thomalla
Chris van derDoes
Tessa E. F. Quax
Thorsten Allers
Volkhard Kaever
Sonja‐Verena Albers
Cyclic nucleotides in archaea: Cyclic di‐AMP in the archaeon Haloferax volcanii and its putative role
MicrobiologyOpen
archaea
cyclic di‐AMP
diadenylate cyclase
Haloferax volcanii
osmoregulation
second messenger
title Cyclic nucleotides in archaea: Cyclic di‐AMP in the archaeon Haloferax volcanii and its putative role
title_full Cyclic nucleotides in archaea: Cyclic di‐AMP in the archaeon Haloferax volcanii and its putative role
title_fullStr Cyclic nucleotides in archaea: Cyclic di‐AMP in the archaeon Haloferax volcanii and its putative role
title_full_unstemmed Cyclic nucleotides in archaea: Cyclic di‐AMP in the archaeon Haloferax volcanii and its putative role
title_short Cyclic nucleotides in archaea: Cyclic di‐AMP in the archaeon Haloferax volcanii and its putative role
title_sort cyclic nucleotides in archaea cyclic di amp in the archaeon haloferax volcanii and its putative role
topic archaea
cyclic di‐AMP
diadenylate cyclase
Haloferax volcanii
osmoregulation
second messenger
url https://doi.org/10.1002/mbo3.829
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