A transcription network of interlocking positive feedback loops maintains intracellular iron balance in archaea

Nucleic Acids Res. 2017 Sep 29;45(17):9990-10001. doi: 10.1093/nar/gkx662.

Abstract

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.

MeSH terms

  • Archaeal Proteins / genetics*
  • Archaeal Proteins / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Feedback, Physiological*
  • Gene Expression Regulation, Archaeal*
  • Gene Regulatory Networks*
  • Halobacterium salinarum / genetics*
  • Halobacterium salinarum / metabolism
  • Homeostasis / genetics
  • Iron / metabolism*
  • Mutation
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Transcription, Genetic

Substances

  • Archaeal Proteins
  • DNA-Binding Proteins
  • Repressor Proteins
  • Iron