The carbon-concentrating mechanism of the extremophilic red microalga Cyanidioschyzon merolae

Abstract

Cyanidioschyzonmerolae is an extremophilic red microalga which grows in low-pH, high-temperature environments. The basis of C. merolae’s environmental resilience is not fully characterized, including whether this alga uses a carbon-concentrating mechanism (CCM). To determine if C. merolae uses a CCM, we measured CO2 uptake parameters using an open-path infra-red gas analyzer and compared them to values expected in the absence of a CCM. These measurements and analysis indicated that C. merolae had the gas-exchange characteristics of a CCM-operating organism: low CO2 compensation point, high affinity for external CO2, and minimized rubisco oxygenation. The biomass δ13C of C. merolae was also consistent with a CCM. The apparent presence of a CCM in C. merolae suggests the use of an unusual mechanism for carbon concentration, as C. merolae is thought to lack a pyrenoid and gas-exchange measurements indicated that C. merolae primarily takes up inorganic carbon as carbon dioxide, rather than bicarbonate. We use homology to known CCM components to propose a model of a pH-gradient-based CCM, and we discuss how this CCM can be further investigated.

Modeling With Uncertainty Quantification Identifies Essential Features of a Non-Canonical Algal Carbon-Concentrating Mechanism

“…These kinetics findings indicated C. merolae does operate a CCM, as C. merolae cells had higher affinity for CO2 than C. merolae rubisco (8.71 ± 1.7 µM cell KC vs. 24.9 ± 3.2 µM rubisco KC at 45 °C, p = 0.008 by two-sample t-test) (Figure 2). This result adds to the indications of the CCM in C. merolae (9)(10)(11).…”

“…C. merolae ’s CCM may be described as a “novel” or “non-canonical” CCM, as the C. merolae CCM must operate differently from the few CCMs which are well-characterized. Unlike algae and cyanobacteria with well-characterized CCMs, C. merolae is not able to take up external bicarbonate, and C. merolae lacks anatomy associated with the pyrenoid CCM organelle (10, 11, 13, 14). The absence of these CCM features in C. merolae challenges our understanding of how algal CCMs work, and presents the opportunity to define essential CCM components.…”

“…CCMs boost carbon-fixation efficiency by concentrating CO2 around rubisco, providing ample substrate for carbon-fixation and inhibiting a competing oxygen-fixation reaction of rubisco. Evidence supporting a CCM in C. merolae includes measured accumulation of carbon in the cell, d 13 C consistent with a CCM, similar growth rates under ambient and elevated CO2, transcriptional response of potential CCM genes to CO2 fluctuations, and substantial CO2 assimilation at low environmental CO2 concentrations (9)(10)(11)(12). However, many of these indications of the CCM are not definitive: in particular, it is not known how much of C. merolae's ability to assimilate CO2 efficiently could be explained by the affinity of C. merolae rubisco for CO2.…”

“…C. merolae is thought to survive in its challenging environment in part by operating a carbon-concentrating mechanism (CCM) (9)(10)(11). CCMs boost carbon-fixation efficiency by concentrating CO2 around rubisco, providing ample substrate for carbon-fixation and inhibiting a competing oxygen-fixation reaction of rubisco.…”

Biophysical carbon concentrating mechanisms in land plants: insights from reaction-diffusion modeling

“…In such systems, all DIC must first enter the cell passively as aqueous CO 2 , at which point it will interconvert primarily between CO 2 and HCO 3 , with the ratio of CO 2 :HCO 3 determined by the cytosolic pH. There is strong evidence that C. merolae has a non-pyrenoid based CCM (Steensma et al, 2023). Such a system could use HCO - pumping across the chloroplast envelope as a method of concentrating carbon, but our results suggest that this system would require maintenance of a near-neutral cytosolic pH along with the presence of carbonic anhydrases in the cytosol to be viable.…”