Rubisco Adaptation to Low Temperatures: A Comparative Study in Psychrophilic and Mesophilic Unicellular Algae

Abstract

Some properties of the ribulose‐1,5‐bisphosphate carboxylase/oxygenase (RUBISCO) from two psychrophilic Chloromonas species have been investigated in relation to their adaptation to cold environments. Contrary to the situation usually encountered with psychrophilic enzymes, the carboxylase activity of both purified “cold” RUBISCO enzymes was lower at low temperatures than that found with the enzyme of the mesophilic alga Chlamydomonas reinhardtii Dangeard. Moreover, the apparent optimal temperature for RUBISCO carboxylase activity was similar for psychrophilic and mesophilic enzymes. Psychrophilic RUBISCOs, however, showed a greater thermosensitivity than the C. reinhardtii enzyme. Genes encoding small and large subunits of RUBISCO from one psychrophilic isolate were sequenced. Comparison of the deduced amino acid sequences to those of higher plants and green algae revealed the substitution of a very highly conserved residue (cysteine247→ serine in the large subunit) that could be responsible, at least in part, for the increased thermosensitivity of the “cold” enzyme. Interestingly, the relative amount of RUBISCO subunits found in the psychrophilic isolates was about twice as high as the amount observed in C. reinhardtii and five other mesophilic algae. The high production of a key enzyme to counterbalance its poor catalytic efficiency at low temperature could constitute a novel type of adaptive mechanism to cold environments.

Adaptation and Acclimation of Photosynthetic Microorganisms to Permanently Cold Environments

“…A similar trend was observed in winter-hardened-crops species (232). Conversely, the protein was thermally sensitive to inactivation in both Antarctic algae and plants (42,236). While sequence analysis and modeling of the large subunit (rbsL) of Rubisco in the psychrophilic Chloromonas sp.…”

“…In contrast with argininosuccinate lyase, the temperature maximum for carboxylase activity of ribulose-1,5-bisphosphate carboxylase (Rubisco), one of the most critical enzymes for inorganic carbon fixation in phototrophs, was not altered in two isolates of the Antarctic Chloromonas sp., and the specific activity at low temperatures was actually lower in the psychrophilic compared with the mesophilic Rubisco (42). This was one of the few exceptions described so far of a psychrophilic enzyme not exhibiting higher catalytic activity at lower temperatures.…”

Photosynthesis, pigments and ultrastructure of the alpine snow algaChlamydomonas nivalis

“…The optimum temperature in the Antarctic species was 208C lower. However, Devos et al (1998) found that the CO 2 -fixing enzyme Rubisco was not more cold stable than in C. reinhardtii, but the relative amount of the enzyme was twice as high. This was discussed as a novel adaptation strategy.…”

Southern Ocean phytoplankton physiology in a changing climate

“…This behaviour is defined by the temperature coefficient Q 10 , which describes a rate change per change of 10 • C in temperature. An average value of 2-3 for the Q 10 of the carboxylating enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) has been measured in phytoplankton in general and recently verified for SO species (Descolas-Gros and de Billy, 1987; Devos et al, 1998;Sage, 2002;Young et al, 2015). Using this coefficient, if SST of the SO were to rise by 6 • C, it would result in an approximate doubling of physiological activity (growth).…”