Temperature-Induced Remodeling of the Photosynthetic Machinery Tunes Photosynthesis in the Thermophilic Alga Cyanidioschyzon merolae

Abstract

The thermophilic alga thrives in extreme environments (low pH and temperature between 40°C and 56°C). In this study, we investigated the acclimation process of the alga to a colder temperature (25°C). A long-term cell growth experiment revealed an extensive remodeling of the photosynthetic apparatus in the first 250 h of acclimation, which was followed by cell growth to an even higher density than the control (grown at 42°C) cell density. Once the cells were shifted to the lower temperature, the proteins of the light-harvesting antenna were greatly down-regulated and the phycobilisome composition was altered. The amount of PSI and PSII subunits was also decreased, but the chlorophyll to photosystems ratio remained unchanged. The 25°C cells possessed a less efficient photon-to-oxygen conversion rate and require a 2.5 times higher light intensity to reach maximum photosynthetic efficiency. With respect to chlorophyll, however, the photosynthetic oxygen evolution rate of the 25°C culture was 2 times higher than the control. Quantitative proteomics revealed that acclimation requires, besides remodeling of the photosynthetic apparatus, also adjustment of the machinery for protein folding, degradation, and homeostasis. In summary, these remodeling processes tuned photosynthesis according to the demands placed on the system and revealed the capability of to grow under a broad range of temperatures.

Molecular Mechanisms of Photoadaptation of Photosystem I Supercomplex from an Evolutionary Cyanobacterial/Algal Intermediate

“…1D), from which a near atomic x-ray structure was obtained (Jordan et al, 2001). The wide temperature tolerance of isolated C. merolae PSII (Krupnik et al, 2013) and PSI-LHCI complexes (this study) is most likely the reason for the remarkable wide temperature range tolerance of this extremophilic alga, as shown in a recent study (Nikolova et al, 2017).…”

Deletion of psbQ’ gene in Cyanidioschyzon merolae reveals the function of extrinsic PsbQ’ in PSII

“…3 c, d). Similar, temperature-dependent activity of C. merolae was observed before (Nikolova et al 2017 ). The mutant cells were more susceptible to temperature than the WT and a drop of the ambient temperature to 25 °C has diminished the activity of both mutants by ~ 50% while the WT retained as much as ~ 65% of its activity from 37 °C conditions.…”

Systems Biology of Cold Adaptation in the Polyextremophilic Red Alga Galdieria sulphuraria

“…A similar increase in the growth rate was also observed in the photoautotrophic sister lineage of Cyanidioschyzon , where cultures of Cyanidioschyzon merolae 10D were grown at 25°C for a period of ∼100 days, albeit under photoautotrophic conditions. This study found that the cold-adapted cultures outgrew the control culture at the end of the experiment (Nikolova et al, 2017). While faster doubling times at 28°C can be attributed to gradual adaptation to the suboptimal growth temperatures, we may only speculate about the causes leading to slower growth in the control condition (42°C).…”

“…Variants affecting the genetic code of genes attributed to this category influence a broad variety of metabolic pathways (e.g., “cellular aromatic compound metabolic process,” GO:0006725, p = 0.0030 and “amine metabolic process,” GO:0009308, p < 0.0001) in both anabolism (e.g., “peptidoglycan biosynthetic process,” GO:0009252, p = 0.0015 and “glycerol biosynthetic process,” GO:0006114, p = 0.0086), and catabolism (e.g., “glycosaminoglycan catabolic process,” GO:0006027, p = 0.0011). In spite of pronounced changes in gene expression of metabolic enzymes during short-term cold stress in G. sulphuraria 074W (Rossoni et al, 2018) and Cyanidioschyzon merolae 10D (Nikolova et al, 2017), microevolution of genes directly involved in metabolic steps appeared to play a minor role in long-term temperature adaptation (34/234 GOs, 14.5%).…”