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A transcription network of interlocking positive feedback loops maintains intracellular iron balance in archaea
Iron is required for key metabolic processes but is toxic in excess. This circumstance forces organisms across the tree of life to tightly regulate iron homeostasis. In hypersaline lakes dominated by archaeal species, iron levels are extremely low and subject to environmental change; however, mechan...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2017
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5737653/ https://www.ncbi.nlm.nih.gov/pubmed/28973467 http://dx.doi.org/10.1093/nar/gkx662 |
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author | Martinez-Pastor, Mar Lancaster, W. Andrew Tonner, Peter D. Adams, Michael W. W. Schmid, Amy K. |
author_facet | Martinez-Pastor, Mar Lancaster, W. Andrew Tonner, Peter D. Adams, Michael W. W. Schmid, Amy K. |
author_sort | Martinez-Pastor, Mar |
collection | PubMed |
description | Iron is required for key metabolic processes but is toxic in excess. This circumstance forces organisms across the tree of life to tightly regulate iron homeostasis. In hypersaline lakes dominated by archaeal species, iron levels are extremely low and subject to environmental change; however, mechanisms regulating iron homeostasis in archaea remain unclear. In previous work, we demonstrated that two transcription factors (TFs), Idr1 and Idr2, collaboratively regulate aspects of iron homeostasis in the model species Halobacterium salinarum. Here we show that Idr1 and Idr2 are part of an extended regulatory network of four TFs of the bacterial DtxR family that maintains intracellular iron balance. We demonstrate that each TF directly regulates at least one of the other DtxR TFs at the level of transcription. Dynamical modeling revealed interlocking positive feedback loop architecture, which exhibits bistable or oscillatory network dynamics depending on iron availability. TF knockout mutant phenotypes are consistent with model predictions. Together, our results support that this network regulates iron homeostasis despite variation in extracellular iron levels, consistent with dynamical properties of interlocking feedback architecture in eukaryotes. These results suggest that archaea use bacterial-type TFs in a eukaryotic regulatory network topology to adapt to harsh environments. |
format | Online Article Text |
id | pubmed-5737653 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-57376532018-01-04 A transcription network of interlocking positive feedback loops maintains intracellular iron balance in archaea Martinez-Pastor, Mar Lancaster, W. Andrew Tonner, Peter D. Adams, Michael W. W. Schmid, Amy K. Nucleic Acids Res Gene regulation, Chromatin and Epigenetics Iron is required for key metabolic processes but is toxic in excess. This circumstance forces organisms across the tree of life to tightly regulate iron homeostasis. In hypersaline lakes dominated by archaeal species, iron levels are extremely low and subject to environmental change; however, mechanisms regulating iron homeostasis in archaea remain unclear. In previous work, we demonstrated that two transcription factors (TFs), Idr1 and Idr2, collaboratively regulate aspects of iron homeostasis in the model species Halobacterium salinarum. Here we show that Idr1 and Idr2 are part of an extended regulatory network of four TFs of the bacterial DtxR family that maintains intracellular iron balance. We demonstrate that each TF directly regulates at least one of the other DtxR TFs at the level of transcription. Dynamical modeling revealed interlocking positive feedback loop architecture, which exhibits bistable or oscillatory network dynamics depending on iron availability. TF knockout mutant phenotypes are consistent with model predictions. Together, our results support that this network regulates iron homeostasis despite variation in extracellular iron levels, consistent with dynamical properties of interlocking feedback architecture in eukaryotes. These results suggest that archaea use bacterial-type TFs in a eukaryotic regulatory network topology to adapt to harsh environments. Oxford University Press 2017-09-29 2017-08-02 /pmc/articles/PMC5737653/ /pubmed/28973467 http://dx.doi.org/10.1093/nar/gkx662 Text en © The Author(s) 2017. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
spellingShingle | Gene regulation, Chromatin and Epigenetics Martinez-Pastor, Mar Lancaster, W. Andrew Tonner, Peter D. Adams, Michael W. W. Schmid, Amy K. A transcription network of interlocking positive feedback loops maintains intracellular iron balance in archaea |
title | A transcription network of interlocking positive feedback loops maintains intracellular iron balance in archaea |
title_full | A transcription network of interlocking positive feedback loops maintains intracellular iron balance in archaea |
title_fullStr | A transcription network of interlocking positive feedback loops maintains intracellular iron balance in archaea |
title_full_unstemmed | A transcription network of interlocking positive feedback loops maintains intracellular iron balance in archaea |
title_short | A transcription network of interlocking positive feedback loops maintains intracellular iron balance in archaea |
title_sort | transcription network of interlocking positive feedback loops maintains intracellular iron balance in archaea |
topic | Gene regulation, Chromatin and Epigenetics |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5737653/ https://www.ncbi.nlm.nih.gov/pubmed/28973467 http://dx.doi.org/10.1093/nar/gkx662 |
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