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Title: Ni induces the CRR1-dependent regulon revealing overlap and distinction between hypoxia and Cu deficiency responses in Chlamydomonas reinhardtii

Abstract

The selectivity of metal sensors for a single metal ion is critical for cellular metal homeostasis. A suite of metal-responsive regulators is required to maintain a prescribed balance of metal ions ensuring that each apo-protein binds the correct metal. However, there are cases when non-essential metals ions disrupt proper metal sensing. Here, an analysis of the Ni-responsive transcriptome of the green alga Chlamydomonas reinhardtii reveals that Ni artificially turns on the CRR1-dependent Cu-response regulon. Since this regulon also responds to hypoxia, a combinatorial transcriptome analysis was leveraged to gain insight into the mechanisms by which Ni interferes with the homeostatic regulation of Cu and oxygen status. Based on parallels with the effect of Ni on the hypoxic response in animals, we propose that a possible link between Cu, oxygen and Ni sensing is an as yet uncharacterized prolyl hydroxylase that regulates a co-activator of CRR1. This analysis also identified transcriptional responses to the pharmacological activation of the Cu-deficiency regulon. Although the Ni-responsive CRR1 regulon is composed of 56 genes (defined as the primary response), 259 transcripts responded to Ni treatment only when a copy of the wild-type CRR1 gene was present. The genome-wide impact of CRR1 target genes on themore » transcriptome was also evident from the 210 transcripts that were at least 2-fold higher in the crr1 strain, where the abundance of many CRR1 targets was suppressed. Additionally, we identified 120 transcripts that responded to Ni independent of CRR1 function. Thus, the putative functions of the proteins encoded by these transcripts suggest that high Ni results in protein damage.« less

Authors:
 [1];  [2];  [2];  [2];  [2]
+ Show Author Affiliations
  1. Univ. of California, Los Angeles, CA (United States); Brookhaven National Lab. (BNL), Upton, NY (United States)
  2. Univ. of California, Los Angeles, CA (United States)
Publication Date:
Research Org.:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
OSTI Identifier:
1424989
Report Number(s):
BNL-113169-2016-JAAM
Journal ID: ISSN 1756-5901; METAIR
Grant/Contract Number:  
SC0012704; GM092473; GM42143; GM100753
Resource Type:
Accepted Manuscript
Journal Name:
Metallomics
Additional Journal Information:
Journal Volume: 8; Journal Issue: 7; Journal ID: ISSN 1756-5901
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Blaby-Haas, Crysten E., Castruita, Madeli, Fitz-Gibbon, Sorel T., Kropat, Janette, and Merchant, Sabeeha S. Ni induces the CRR1-dependent regulon revealing overlap and distinction between hypoxia and Cu deficiency responses in Chlamydomonas reinhardtii. United States: N. p., 2016. Web. doi:10.1039/C6MT00063K.
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Blaby-Haas, Crysten E., Castruita, Madeli, Fitz-Gibbon, Sorel T., Kropat, Janette, & Merchant, Sabeeha S. Ni induces the CRR1-dependent regulon revealing overlap and distinction between hypoxia and Cu deficiency responses in Chlamydomonas reinhardtii. United States. https://doi.org/10.1039/C6MT00063K
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Blaby-Haas, Crysten E., Castruita, Madeli, Fitz-Gibbon, Sorel T., Kropat, Janette, and Merchant, Sabeeha S. Fri . "Ni induces the CRR1-dependent regulon revealing overlap and distinction between hypoxia and Cu deficiency responses in Chlamydomonas reinhardtii". United States. https://doi.org/10.1039/C6MT00063K. https://www.osti.gov/servlets/purl/1424989.
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@article{osti_1424989,
title = {Ni induces the CRR1-dependent regulon revealing overlap and distinction between hypoxia and Cu deficiency responses in Chlamydomonas reinhardtii},
author = {Blaby-Haas, Crysten E. and Castruita, Madeli and Fitz-Gibbon, Sorel T. and Kropat, Janette and Merchant, Sabeeha S.},
abstractNote = {The selectivity of metal sensors for a single metal ion is critical for cellular metal homeostasis. A suite of metal-responsive regulators is required to maintain a prescribed balance of metal ions ensuring that each apo-protein binds the correct metal. However, there are cases when non-essential metals ions disrupt proper metal sensing. Here, an analysis of the Ni-responsive transcriptome of the green alga Chlamydomonas reinhardtii reveals that Ni artificially turns on the CRR1-dependent Cu-response regulon. Since this regulon also responds to hypoxia, a combinatorial transcriptome analysis was leveraged to gain insight into the mechanisms by which Ni interferes with the homeostatic regulation of Cu and oxygen status. Based on parallels with the effect of Ni on the hypoxic response in animals, we propose that a possible link between Cu, oxygen and Ni sensing is an as yet uncharacterized prolyl hydroxylase that regulates a co-activator of CRR1. This analysis also identified transcriptional responses to the pharmacological activation of the Cu-deficiency regulon. Although the Ni-responsive CRR1 regulon is composed of 56 genes (defined as the primary response), 259 transcripts responded to Ni treatment only when a copy of the wild-type CRR1 gene was present. The genome-wide impact of CRR1 target genes on the transcriptome was also evident from the 210 transcripts that were at least 2-fold higher in the crr1 strain, where the abundance of many CRR1 targets was suppressed. Additionally, we identified 120 transcripts that responded to Ni independent of CRR1 function. Thus, the putative functions of the proteins encoded by these transcripts suggest that high Ni results in protein damage.},
doi = {10.1039/C6MT00063K},
journal = {Metallomics},
number = 7,
volume = 8,
place = {United States},
year = {Fri May 06 00:00:00 EDT 2016},
month = {Fri May 06 00:00:00 EDT 2016}
}
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https://doi.org/10.1039/C6MT00063K
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