Copper-induced concomitant increases in photosynthesis, respiration, and C, N and S assimilation revealed by transcriptomic analyses in Ulva compressa (Chlorophyta)

Abstract

Background: The marine alga Ulva compressa is the dominant species in copper-polluted coastal areas in northern Chile. It has been shown that the alga tolerates micromolar concentrations of copper and accumulates copper at the intracellular level. Transcriptomic analyses were performed using total RNA of the alga cultivated with 10 μ M copper for 0, 1, 3 and 5 days using RNA-seq in order to identify processes involved in copper tolerance. Results: The levels of transcripts encoding proteins belonging to Light Harvesting Complex II (LHCII), photosystem II (PSII), cytochrome b6f, PSI, LHCI, ATP synthase and proteins involved in repair of PSII and protection of PSI were increased in the alga cultivated with copper. In addition, the level of transcripts encoding proteins of mitochondrial electron transport chain, ATP synthase, and enzymes involved in C, N and S assimilation were also enhanced. The higher percentages of increase in the level of transcripts were mainly observed at days 3 and 5. In contrast, transcripts involved protein synthesis and degradation, signal transduction, and replication and DNA repair, were decreased. In addition, net photosynthesis and respiration increased in the alga cultivated with copper, mainly at days 1 to 3. Furthermore, the activities of enzymes involved in C, N and S assimilation, rubisco, glutamine synthase and cysteine synthase, respectively, were also increased, mainly at days 1 and 3. Conclusions: The marine alga U. compressa tolerates copper excess through a concomitant increase in expression of proteins involved in photosynthesis, respiration, and C, N and S assimilation, which represents an exceptional mechanism of copper tolerance.

Copper-Induced Activation of MAPKs, CDPKs and CaMKs Triggers Activation of Hexokinase and Inhibition of Pyruvate Kinase Leading to Increased Synthesis of ASC, GSH and NADPH in Ulva compressa

“…In addition, NADPH produced by G6PDH may be consumed to increase C, N and S assimilation, which are processes requiring NADPH, in the cytoplasm (Kopriva et al, 1999;Kopriva et al, 2002). In this sense, it has been shown that C, N and S assimilation is increased in the alga exposed to copper excess since the level of transcripts and the activities of key enzymes involved in these processes are also increased (Laporte et al, 2020). The enhanced C, N and S assimilation may be required to the synthesis of new proteins and membranes that are damaged by copper-induced oxidative stress.…”

“…In addition, the constant level of NADPH that did not change with inhibitors of CaMKs, CDPKs and MAPKs indicates that the constant NADPH level is due to photosynthesis. In this sense, it was shown that net photosynthesis is increased in the alga exposed to copper excess for 0 to 5 days (Laporte et al, 2020) and the increase in NADPH level is due to activation of ferredoxin-NADPH reductase (FNR) in chloroplasts. It has been shown FNR is not regulated by phophorylation but instead by acetylation of a lysine residue located near the active site in A. thaliana (Lethimäki et al, 2014).…”

“…In addition, there was an increase in activities of rubisco, involved in C assimilation, glutamine synthase, involved in N assimilation, and O-acetyl thiol lyase, involved in S assimilation, which are reductive processes that require NADPH. Thus, photosynthesis and C, N and S assimilation are increased in the alga exposed to copper stress (Laporte et al, 2020).…”

“…This marine macroalga has been extensively studied in regard to the mechanisms involved in copper tolerance (Gonzá lez et al, 2010;Gonzá lez et al, 2012;Mellado et al, 2012;Laporte et al, 2016;Moenne et al, 2016) and copper accumulation (Ratkevicius et al, 2003;Navarrete et al, 2019;Zú ñiga et al, 2020). It has been shown that this alga presents exceptional mechanisms of copper tolerance that will be mentioned bellow (Laporte et al, 2020;Moenne et al, 2020). It was initially shown that the alga collected in copper-contaminated sites displayed and increase in intracellular copper level, AP activity and synthesis of ASC, which was accumultated as DHA (Ratkevicius et al, 2003).…”

Mechanisms of Copper Tolerance, Accumulation, and Detoxification in the Marine Macroalga Ulva compressa (Chlorophyta): 20 Years of Research

“…Transcriptomic analyses were performed with alga cultivated with 10 M of copper for short times such as 0, 3, 6, 12 and 24 h and longer times such as 0, 1, 3 and 5 d in order to find new UcMTs and probably a PCS [ 52 , 53 ]. Transcriptomic analyses performed for long times allowed the identification of two potential new UcMTs, but not a PCS.…”