From economy to luxury: Copper homeostasis in Chlamydomonas and other algae

Plastocyanin and cytochrome c6, abundant proteins in photosynthesis, are readouts for cellular copper status in Chlamydomonas and other algae. Their accumulation is controlled by a transcription factor copper response regulator (CRR1). The replacement of copper-containing plastocyanin with heme-cont...

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Published in:Biochimica et biophysica acta. Molecular cell research 2020-11, Vol.1867 (11), p.118822-118822, Article 118822
Main Authors: Merchant, Sabeeha S., Schmollinger, Stefan, Strenkert, Daniela, Moseley, Jeffrey L., Blaby-Haas, Crysten E.
Format: Article
Language:English
Subjects:
BASIC BIOLOGICAL SCIENCES
Chlamydomonas
Chlamydomonas - genetics
Chlamydomonas - metabolism
Chlorophyte algae
Chloroplast
Copper - metabolism
Copper nutrition
Cytochromes c6 - genetics
Dihydrodipicolinate Reductase - genetics
Electron Transport Complex IV - genetics
Ferredoxin
Gene Expression Regulation, Plant - genetics
Homeostasis - genetics
Photosynthesis
Photosynthesis - genetics
Plastocyanin - genetics
Transcriptome - genetics
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Summary:Plastocyanin and cytochrome c6, abundant proteins in photosynthesis, are readouts for cellular copper status in Chlamydomonas and other algae. Their accumulation is controlled by a transcription factor copper response regulator (CRR1). The replacement of copper-containing plastocyanin with heme-containing cytochrome c6 spares copper and permits preferential copper (re)-allocation to cytochrome oxidase. Under copper-replete situations, the quota depends on abundance of various cuproproteins and is tightly regulated, except under zinc-deficiency where acidocalcisomes over-accumulate Cu(I). CRR1 has a transcriptional activation domain, a Zn-dependent DNA binding SBP-domain with a nuclear localization signal, and a C-terminal Cys-rich region that represses the zinc regulon. CRR1 activates >60 genes in Chlamydomonas through GTAC-containing CuREs; transcriptome differences are recapitulated in the proteome. The differentially-expressed genes encode assimilatory copper transporters of the CTR/SLC31 family including a novel soluble molecule, redox enzymes in the tetrapyrrole pathway that promote chlorophyll biosynthesis and photosystem 1 accumulation, and other oxygen-dependent enzymes, which may influence thylakoid membrane lipids, specifically polyunsaturated galactolipids and γ-tocopherol. CRR1 also down-regulates 2 proteins in Chlamydomonas: for plastocyanin, by activation of proteolysis, while for the di‑iron subunit of the cyclase in chlorophyll biosynthesis, through activation of an upstream promoter that generates a poorly-translated 5′ extended transcript containing multiple short ORFs that inhibit translation. The functions of many CRR1-target genes are unknown, and the copper protein inventory in Chlamydomonas includes several whose functions are unexplored. The comprehensive picture of cuproproteins and copper homeostasis in this system is well-suited for reverse genetic analyses of these under-investigated components in copper biology. •Plastocyanin replacement by a cytochrome is a key copper sparing response in algae.•60+ genes are up-regulated in copper-deficiency by a transcriptional activator, CRR1.•Up-regulated genes include transporters, redox proteins, and chloroplast enzymes.•CRR1 down-regulation works through 5′ extended UTRs that are poorly translated.•CYC6, CRR1, and multiple forms of CRD1/CHL27 are found in many algae.
ISSN:0167-4889
1879-2596
DOI:10.1016/j.bbamcr.2020.118822