skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Evolution of context dependent regulation by expansion of feast/famine regulatory proteins

Journal Article · · BMC Systems Biology
 [1];  [2];  [1];  [2];  [2];  [1];  [1];  [1];  [3];  [4]
  1. Inst. for Systems Biology, Seattle, WA (United States)
  2. Inst. for Systems Biology, Seattle, WA (United States); Univ. of Washington, Seattle, WA (United States). Molecular and Cellular Biology Program
  3. Univ. of California, Davis, CA (United States). Dept. of Biomedical Engineering and Genome Center
  4. Inst. for Systems Biology, Seattle, WA (United States); Univ. of Washington, Seattle, WA (United States). Molecular and Cellular Biology Program, Dept. of Microbiology, and Dept. of Biology

Expansion of transcription factors is believed to have played a crucial role in evolution of all organisms by enabling them to deal with dynamic environments and colonize new environments. We investigated how the expansion of the Feast/Famine Regulatory Protein (FFRP) or Lrp-like proteins into an eight-member family in Halobacterium salinarum NRC-1 has aided in niche-adaptation of this archaeon to a complex and dynamically changing hypersaline environment. We mapped genome-wide binding locations for all eight FFRPs, investigated their preference for binding different effector molecules, and identified the contexts in which they act by analyzing transcriptional responses across 35 growth conditions that mimic different environmental and nutritional conditions this organism is likely to encounter in the wild. Integrative analysis of these data constructed an FFRP regulatory network with conditionally active states that reveal how interrelated variations in DNA-binding domains, effector-molecule preferences, and binding sites in target gene promoters have tuned the functions of each FFRP to the environments in which they act. We demonstrate how conditional regulation of similar genes by two FFRPs, AsnC (an activator) and VNG1237C (a repressor), have striking environment-specific fitness consequences for oxidative stress management and growth, respectively. This study provides a systems perspective into the evolutionary process by which gene duplication within a transcription factor family contributes to environment-specific adaptation of an organism.

Research Organization:
Institute for Systems Biology, Seattle, WA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Contributing Organization:
ENIGMA Consortium
Grant/Contract Number:
AC02-05CH11231; FG02-04ER64685; FG02-07ER64327; FG02-08ER64685; AC05-06OR23100
OSTI ID:
1212320
Journal Information:
BMC Systems Biology, Vol. 8, Issue 1; ISSN 1752-0509
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 13 works
Citation information provided by
Web of Science

References (51)

MicrobesOnline: an integrated portal for comparative and functional genomics journal November 2009
Niche adaptation by expansion and reprogramming of general transcription factors journal January 2011
Sa-Lrp from Sulfolobus acidocaldarius is a versatile, glutamine-responsive, and architectural transcriptional regulator journal December 2012
Prevalence of transcription promoters within archaeal operons and coding sequences journal January 2009
A single transcription factor regulates evolutionarily diverse but functionally linked metabolic pathways in response to nutrient availability journal January 2009
General transcription factor specified global gene regulation in archaea journal March 2007
Transcription Regulation by Feast/Famine Regulatory Proteins, FFRPs, in Archaea and Eubacteria journal January 2008
A Structural Code for Discriminating between Transcription Signals Revealed by the Feast/Famine Regulatory Protein DM1 in Complex with Ligands journal October 2007
BarR, an Lrp-type transcription factor in S ulfolobus acidocaldarius , regulates an aminotransferase gene in a β-alanine responsive manner : BarR, a β-alanine responsive regulator journal April 2014
Analysis of the DNA-binding sequence specificity of the archaeal transcriptional regulator Ss-LrpB from Sulfolobus solfataricus by systematic mutagenesis and high resolution contact probing journal December 2006
Lambda placMu insertions in genes of the leucine regulon: extension of the regulon to genes not regulated by leucine. journal March 1992
Inference of Expanded Lrp-Like Feast/Famine Transcription Factor Targets in a Non-Model Organism Using Protein Structure-Based Prediction journal September 2014
Genome sequence of Halobacterium species NRC-1 journal October 2000
A Novel Ligand-binding Domain Involved in Regulation of Amino Acid Metabolism in Prokaryotes journal July 2002
Metallochaperones Regulate Intracellular Copper Levels journal January 2013
A systems view of haloarchaeal strategies to withstand stress from transition metals journal July 2006
Quantifying similarity between motifs journal January 2007
Partitioning RNAs by length improves transcriptome reconstruction from short-read RNA-seq data journal January 2022
The anatomy of microbial cell state transitions in response to oxygen journal September 2007
Transcriptional control by two leucine-responsive regulatory proteins in Halobacterium salinarum R1 journal January 2010
Unexpected Coregulator Range for the Global Regulator Lrp of Escherichia coli and Proteus mirabilis journal December 2010
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0 journal October 2013
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
The ilvIH operon of Escherichia coli is positively regulated. journal August 1990
An integrated systems approach for understanding cellular responses to gamma radiation journal January 2006
A thermostable platform for transcriptional regulation: the DNA-binding properties of two Lrp homologs from the hyperthermophilic archaeon Methanococcus jannaschii journal January 2001
The genome-wide binding profile of the Sulfolobus solfataricus transcription factor Ss-LrpB shows binding events beyond direct transcription regulation journal January 2013
A Predictive Model for Transcriptional Control of Physiology in a Free Living Cell journal December 2007
Comprehensive Genome-wide Protein-DNA Interactions Detected at Single-Nucleotide Resolution journal December 2011
Feast/famine regulatory proteins (FFRPs): Escherichia coli Lrp, AsnC and related archaeal transcription factors journal January 2006
Two transcription factors are necessary for iron homeostasis in a salt-dwelling archaeon journal November 2010
Systems Level Insights Into the Stress Response to UV Radiation in the Halophilic Archaeon Halobacterium NRC-1 journal May 2004
Coordination of frontline defense mechanisms under severe oxidative stress journal January 2010
The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. journal January 1994
Feast/Famine Regulation by Transcription Factor FL11 for the Survival of the Hyperthermophilic Archaeon Pyrococcus OT3 journal December 2007
Expanded target and cofactor repertoire for the transcriptional activator LysM from Sulfolobus journal January 2013
An Update of DIVERGE Software for Functional Divergence Analysis of Protein Family journal April 2013
The DNA-recognition mode shared by archaeal feast/famine-regulatory proteins revealed by the DNA-binding specificities of TvFL3, FL10, FL11 and Ss-LrpB journal May 2009
Crystal structure of the Lrp-like transcriptional regulator from the archaeon Pyrococcus furiosus journal March 2001
Improved scoring of functional groups from gene expression data by decorrelating GO graph structure journal April 2006
Model-based deconvolution of genome-wide DNA binding journal December 2007
METREE: a program package for inferring and testing minimum-evolution trees journal January 1994
Functional Diversification of Paralogous Transcription Factors via Divergence in DNA Binding Site Motif and in Expression journal June 2008
Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains11Edited by F. Cohen journal April 2001
The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. journal January 1994
Coding limits on the number of transcription factors journal September 2006
An expanding family of archaeal transcriptional activators journal October 2005
SBEAMS-Microarray: database software supporting genomic expression analyses for systems biology journal June 2006
Identification and Genomic Analysis of Transcription Factors in Archaeal Genomes Exemplifies Their Functional Architecture and Evolutionary Origin journal February 2010
Adaptation of cells to new environments: Adaptation of cells to new environments
  • Brooks, Aaron N.; Turkarslan, Serdar; Beer, Karlyn D.
  • Wiley Interdisciplinary Reviews: Systems Biology and Medicine, Vol. 3, Issue 5 https://doi.org/10.1002/wsbm.136
journal December 2010
Correlated changes between regulatory cis elements and condition-specific expression in paralogous gene families journal November 2009

Cited By (6)