Regulating cellular trace metal economy in algae

Abstract

As indispensable protein cofactors, Fe, Mn, Cu and Zn are at the center of multifaceted acclimation mechanisms that have evolved to ensure extracellular supply meets intracellular demand. Starting with selective transport at the plasma membrane and ending in protein metalation, metal homeostasis in algae involves regulated trafficking of metal ions across membranes, intracellular compartmentalization by proteins and organelles, and metal-sparing/recycling mechanisms to optimize metal-use efficiency. Overlaid on these processes are additional circuits that respond to the metabolic state as well as to the prior metal status of the cell. In this review, we focus on recent progress made toward understanding the pathways by which the single-celled, green alga Chlamydomonas reinhardtii controls its cellular trace metal economy. We also compare these mechanisms to characterized and putative processes in other algal lineages. Photosynthetic microbes continue to provide insight into cellular regulation and handling of Cu, Fe, Zn and Mn as a function of the nutritional supply and cellular demand for metal cofactors. New experimental tools such as RNA-Seq and subcellular metal imaging are bringing us closer to a molecular understanding of acclimation to supply dynamics in algae and beyond.

A Series of Fortunate Events: Introducing Chlamydomonas as a Reference Organism

“…Cellular and physiological responses to various essential metal concentrations can also be investigated; iron deficiency is the easiest, as the chloroplast constitutes the major iron sink in the cell and requires a high iron quota to sustain photosynthesis. Deficiencies in other metals (zinc, copper, and manganese) are more difficult to observe and require the use of ultra-pure water and acid-washed glassware to remove any trace contamination from glass surfaces (Blaby-Haas and Merchant, 2017). Trace element solutions can be purchased from CRC (therefore alleviating the significant effort of preparing them); alternatively, cells grow very well when using a revised mineral nutrient supplement that more than covers cellular requirements and is easy to prepare (Kropat et al, 2011).…”

Nitric Oxide Remodels the Photosynthetic Apparatus upon S-Starvation in Chlamydomonas reinhardtii

“…We have shown previously that NO is produced when C. reinhardtii is starved of nitrogen (Wei et al, 2014). NO is produced in response to a series of abiotic stresses during which it is suspected to act as a signaling molecule that modulates enzymatic activities, protein localization, and proteolytic susceptibility (Wendehenne and Hancock, 2011;Zaffagnini et al, 2016;Blaby-Haas and Merchant, 2017). Although NO production in C. reinhardtii under sulfur starvation has recently been documented (Minaeva et al, 2017), the kinetics of synthesis and the source(s) of this molecule are still to be elucidated.…”

“…The signaling pathway could therefore be a multistep cascade, with increased specificity at each step, starting from the highly reactive and poorly specific NO to end up with highly specific nitrosylases. In photosynthetic organisms, NO, besides its involvement in physiological responses (Beligni and Lamattina, 2000;Neill et al, 2002;Pagnussat et al, 2002;He et al, 2004;Prado et al, 2004;Mishina et al, 2007;Tada et al, 2008;Lindermayr et al, 2010;Gibbs et al, 2014), is also implicated in many stress responses with increased oxidative load (Delledonne et al, 1998;García-Mata and Lamattina, 2001;Graziano et al, 2002;Feechan et al, 2005;Baudouin et al, 2006;Zhao et al, 2007;Lee et al, 2008aLee et al, , 2008bBesson-Bard et al, 2009;Blaby-Haas and Merchant, 2017), including nitrogen starvation (Wei et al, 2014).…”

Arabidopsis Pollen Fertility Requires the Transcription Factors CITF1 and SPL7 That Regulate Copper Delivery to Anthers and Jasmonic Acid Synthesis

“…An uptake-based Cu homeostatic mechanism involves the upregulated expression of Cu acquisition and transport genes under Cu deficiency (Burkhead et al, 2009). The Cu economy or "metal switch" mechanism, originally discovered in the green alga Chlamydomonas reinhardtii, includes the downregulation of the expression of potentially redundant Cu proteins for the metabolic reutilization of cellular Cu reserves (Burkhead et al, 2009;Blaby-Haas and Merchant, 2017;Kropat et al, 2015;Ravet et al, 2011;Shahbaz et al, 2015). In Arabidopsis thaliana, both processes are controlled by a conserved transcription factor, SPL7 (SQUAMOSA PROMOTER BINDING PROTEIN LIKE7), a homolog of the algal Cu sensor, CRR1 (COPPER RESPONSE REGULATOR1) (Yamasaki et al, 2009;Bernal et al, 2012;GarciaMolina et al, 2014;Sommer et al, 2010;Kropat et al, 2005).…”