An Update on the Metabolic Roles of Carbonic Anhydrases in the Model Alga Chlamydomonas reinhardtii

Abstract

Carbonic anhydrases (CAs) are metalloenzymes that are omnipresent in nature. CAs catalyze the basic reaction of the reversible hydration of CO2 to HCO3− and H+ in all living organisms. Photosynthetic organisms contain six evolutionarily different classes of CAs, which are namely: α-CAs, β-CAs, γ-CAs, δ-CAs, ζ-CAs, and θ-CAs. Many of the photosynthetic organisms contain multiple isoforms of each CA family. The model alga Chlamydomonas reinhardtii contains 15 CAs belonging to three different CA gene families. Of these 15 CAs, three belong to the α-CA gene family; nine belong to the β-CA gene family; and three belong to the γ-CA gene family. The multiple copies of the CAs in each gene family may be due to gene duplications within the particular CA gene family. The CAs of Chlamydomonas reinhardtii are localized in different subcellular compartments of this unicellular alga. The presence of a large number of CAs and their diverse subcellular localization within a single cell suggests the importance of these enzymes in the metabolic and biochemical roles they perform in this unicellular alga. In the present review, we update the information on the molecular biology of all 15 CAs and their metabolic and biochemical roles in Chlamydomonas reinhardtii. We also present a hypothetical model showing the known functions of CAs and predicting the functions of CAs for which precise metabolic roles are yet to be discovered.

Insights on the Functions and Ecophysiological Relevance of the Diverse Carbonic Anhydrases in Microalgae

“…α-CAs are often more active than other classes of CA [10] and are typically found as monomers; however, one type, in the fungus Aspergillus oryzae, is a dimer [71] and two α-CAs in C. reinhardtii (CAH1 and CAH2) are tetramers [72]. In C. reinhardtii, 12 genes that encode CA isoforms, including three alpha, six beta, and three gamma or gamma-like CAs [73], have been reported and more recently, three more beta CAs have been described [74] (Figure 1). Another extracellular α-CA, EcaA, from cyanobacteria is also found in the periplasmic space; however, it does not have a role in the CCM [75,76].…”

“…β-CA was discovered in chloroplasts from leaves [78]. They are present in most photosynthetic organisms, and in some non-photosynthetic microorganisms, but not in animals [74]. In contrast to the α-CAs, β-CAs are more frequently found in different oligomeric states, and several trimeric and tetrameric structures have been reported [79][80][81].…”

In vitro resynthesis of lichenization reveals the genetic background of symbiosis-specific fungal-algal interaction in Usnea hakonensis.

“…Ttzw_014612 is similar to D1 reaction center protein in photosystem II (32). Ttzw_000076 showed similarities to carbonic anhydrases which catalyze the reversible hydration of carbon dioxide, known to support photosynthesis by means of CO 2 transport and/or involvement in carbon concentration mechanisms (33,34).…”

“…If analogous regulation can be supposed, the up-regulated expression of the D1 protein gene in the symbiotic states indicates increase in the number of the stock transcripts in cells, thereby enabling rapid synthesis of D1 proteins, i.e., rapid recovery from photodamage. xing root nodules (33,34). The identi cation of symbiosis-related CAs in lichen-forming algae is intriguing because it raises the possibility of symbiotic-speci c regulatory systems that may control the algal metabolism by the CO 2 condition inside a thallus.…”

In vitro resynthesis of lichenization reveals the genetic background of symbiosis-specific fungal-algal interaction in Usnea hakonensis.

“…If analogous regulation can be supposed, the up-regulated expression of the D1 protein gene in the symbiotic states indicates an increase in the number of stock transcripts in cells, thereby enabling rapid synthesis of D1 proteins, i.e., rapid recovery from photodamage. (33,34). The identi cation of symbiosis-related CAs in lichen-forming algae is intriguing because it raises the possibility of symbiotic-speci c regulatory systems that may control algal metabolism via the CO 2 condition inside a thallus.…”