Inorganic carbon concentrating mechanisms in relation to the biology of algae

“The isolated diatom plastids lack the two “chloroplast endoplasmic reticulum” membranes, as is typically the case for kleptoplastids from the tribophyte Vaucheria litorea, which can photosynthesize for many months in the saccoglossan mollusk Elysia chlorotica (63, 151, 161).”

“These have evolved in many algae, including those symbiotic with invertebrates, overcoming this limitation (Raven 2003).”

“(d) Symbioses with cyanobacteria and/or algae as the partner performing photosynthesis Raven (2003) reviews the available evidence; this shows that all of the cyanobacteria and dinoflagellates investigated, and some of the green algae examined, express CCMs when they are contributing photosynthesis…”

“A minority of marine macroalgae use dissolved CO2 entering the cells by diffusion as the carbon source for photosynthesis (Maberly, 1990; Maberly et al., 1992; Beardall & Giordano, 2002; Raven et al., 2002a, b; Raven, 2003; Giordano et al., 2005).”

“This pathway also recaptures the CO2 generated from the oxygenation of Rubisco via photorespiration, thus maximizing the assimilation of CO2 [52,79].”

“…in the (stationary) chloroplasts under acid bands than under alkaline bands (Bulychev et al. 2001), despite the rapid (up to 100 lm per second) cytoplasmic streaming in these cells which would help equilibrate inorganic carbon through the cytoplasmic layer (Raven and Smith 1978; Raven 2003b).”

“Moreover, contrary to other phytoplankton groups, which generally increase cellular carbon quotas with increasing CO2 availability [Riebesell, 2004; Rost et al., 2002], C quota (as well as cellular N, P, and Chl a contents) of Trichodesmium decreases with increasing CO2.”

“Ruppia cirrhosa) (Madsen and Baattrup-Pedersen 1995; Beer and Rehnberg 1997; Hellblom and Axelsson 2003; Raven 2003). Depending on the relative proportions of HCO3/ CO2 uptake, Ruttner (1962) distinguished three basic types of C acquisition in aquatic plants:”

“…species of phytoplankton, including cyanobacteria, possess mechanisms to increase the efficiency of photosynthesis by taking up different forms of inorganic carbon (CO2, HCO3 ) and concentrating CO2 around Rubisco, the main photosynthetic (carbon fixation) enzyme (Badger et al. 2002; Raven 2003).”

“The level of CO2 available to RuBisCo is elevated by converting any bicarbonate passing the thylakoid lumen into CO2.”

“These mechanisms reduce the competition of oxygen for the enzyme by increasing the intracellular CO2:O2 ratio, thereby making it more efficient by reducing photorespiration (see Raven 1997, 2003, Raven et al. 2012 for reviews).”

“Is it possible that a drop in pCO2 level in the Cryogenian or Ediacaran Period may have forced macroalgae toward greater surface/volume ratio within their developmental possibilities to compensate for the lower pCO2 level? There is some evidence of CO2 limitation in modern macroalgae that do not use carbon concentrati…”

“…called carbon-concentrating mechanisms (CCMs) which transport HCO3 – across cell membranes using ion transporters, or catalyse the dehydration of HCO3 – to CO2 via the membrane-associated external carbonic anhydrase (Johnston, 1991; Badger and Price, 1994; Raven, 1997, 2003; Raven et al., 2002).”

“…all work to date on microalgal responses to rising CO2 has been performed using short-term studies in natural and laboratory populations (reviewed recently by Beardall et al. 1998; Colman et al. 2002; Riebesell, 2004) or by comparisons between different taxa of extant phytoplankton (Raven 2003).”

“Cyanobacteria can adapt to fluctuating Ci and O2 conditions (42) by establishing the CCM in order to minimize carbon leakage”

“In addition, some natural populations of microalgae without CCMs have been found, often in environments where it is thought that a CCM would not be needed for growth, though a straightforward link between CCM characters and algal biology is not always possible (Raven 2003).”

“Photosynthetic rate had a positive correlation between pore conductance and CO2 concentration inside cells (Raven, 2003).”

“Plant Physiology, October 2004, Vol. 136, pp. 3301–3312, www.plantphysiol.org 2004 American Society of Plant Biologists 3301 can alter the proportional availability of CO2 and HCO3 2 in the Ci pool (Shibata et al., 2002; Raven, 2003).”

“The energy costs of CCMs are still under discussion and are presumably dependent on the type of CCM used (Raven 1991; Kubler & Raven 1995; Beardall et al. 1998; Raven 2003).”

“Studies of CCMs have concentrated on cyanobacteria and freshwater green algae and almost invariably involve the active transport of the species CO2, H and HCO3 across one or more membranes in bringing about a higher steady-state concentration of CO2 available to Rubisco than presents in the bulk medium [108,115].”

“However, not all algal groups contain and utilize CCMs, as some rely upon the diffusive flux of CO2 to support photosynthetic rates (Maberly 1990; Maberly, Raven & Johnston 1992; Raven 2003).”

“Difference in photosynthesis of aquatic and land plants In algae, high rates of photosynthetic carbon assimilation occur even at CO2 concentrations as low as 5 ppm, because of an effective CO2 concentrating mechanism (CCM), based on carbonic anhydrase (Raven 2003).”

“High concentrations of CO 2 are therefore necessary to promote carbon assimilation and to meet the hosts’ energetic demand for symbiont-derived photosynthates [10–12].”

“…have hypothesized that photoautotrophs relying on carbon-concentrating mechanisms (CCM) to concentrate CO2 at the active site of the RuBisCO enzyme may benefit from increases in pCO2 through reduction in energetic demands of the CCM components [Kaplan et al., 1991; Price et al., 2008; Raven, 2003].”

“Furthermore, decreased ambient dissolved CO2 concentration may trigger active CO2 transport or taking up HCO3 by phytoplankton which subsequently in the cell is dehydrated to CO2 by carbonic anhydrase immediately (carbon concentration mechanism, CCM) (Takahashi et al., 1990; Fogel et al., 1992; Raven, 2003).”

“For example, carbon acquisition patterns in relation with morphophysiological processes, biomass allocation, reproduction, and development of adult and early stages of seaweeds have been hitherto overlooked (Raven 2003).”

“In the last 20 years, increasing attention has been dedicated to characterizing the CCM in model organisms, and significant contributions have been made on physiological, molecular, and ecological aspects of the inorganic carbon (Ci) acquisition processes (Colman et al. 2002; Badger and Price 2003; Raven 2003).”

“A possible size dependency of pH tolerances could be explained by the difference in the surface:volume ratio, in the same way that smaller cells have a more efficient nutrient uptake due to their larger surface:volume ratio (Raven 2003).”

“…Microalgae: Ecological Role and Possible Biotechnological Application Our present understanding of the CCM in aquatic photosynthetic microorganisms (Raven, 1991, 1997, 2003; Johnston et al., 1992; Kaplan and Reinhold, 1999; Badger and Spalding, 2000; Colman et al., 2002; Ogawa and Kaplan, 2003;…”

“…both CO2-sensitive and CO2insensitive growth have been reported in natural populations of phytoplankton (Hein and Sand-Jensen 1998; Tortell and Morel 2002), as have different CCM regulation strategies, even among phytoplankton with similar biology (Raven et al. 2002; Raven 2003; Rost et al. 2003).”

“Marine epilithic algae use two main sources of carbon: inorganic carbon as CO2 and HCO3 ¡ dissolved in seawater (Raven 2003) and, to a minor extent, (1–6% of total carbon assimilation) DOM (Titlyanov et al.”

“[37–38]), since the energy saved by a down-regulated CCM operation could be reallocated to carbon fixation and growth.”

“CCM are well described in many phototrophs to increase the concentration of CO 2 in the proximity of Rubisco ( Raven 1990, 2003; Giordano et al. 2005).”

“When the algae uses inorganic carbon, dissolved CO2 was firstly utilized (Raven 2003) and then the HCO3 - (Hellblom and Axelsson 2003) was used as a photosynthetic carbon source (Dong et al.”

“Further on, CO2/O2 specificity values of Rubisco in some dinoflagellates are so low that photosynthesis in airequilibrated solutions appears impossible on the basis of diffusive CO2 entry, except aided by some mechanisms to concentrate carbon (Raven 2003).”

“The HCO3 2 that is transported into the cell can be transformed to CO2 in the proximity of Rubisco (Raven, 2003).”

“Freshwater b-cyanobacteria, including S. elongatus (PCC 7942), can induce CCMs, a system of protein complexes that use energy from reorganized photosynthetic electron transport to concentrate dilute Ci from the environment to high levels within the cell (Kaplan et al. 1980, Raven 2003).”

“Many of these microalgae genetically control their CCM activity in response to environmental conditions including DIC, nitrogen, and phosphorous (Badger et al. 1980; Palmqvist et al. 1994; Fukuzawa et al. 2001; Beardall and Giordano 2002; Raven 2003; Beardall et al. 2005; Vance and Spalding 2005; Yamano et al. 2008).”

“Since all strains, with the exception of Chlorella minutissima L32, had increased growth rates in both the bicarbonate and carbonate treatments, these algae probably could utilize both carbon forms (Colman et al. 2002, Espie et Colman 2005, Raven 1997, Raven 2003, Raven et al. 2005).”

“Very fewmacroalgal species rely on passive CO2 diffusion alone for DIC uptake (Raven, 2003; Giordano et al., 2005; Raven and Hurd, 2012; Stepien et al., 2016).”

“Cyanobacteria could survive in a low CO2 environment in water due to their CCMs, which can increase the CO2 concentration around the active site of Rubisco, the key enzyme of photosynthetic carbon assimilation, and overcome their low affinity for CO2, thereby effectively assimilating CO2 (Price et al., 1998; Kaplan an…”

“Rapid phytoplankton growth can, under such conditions, place local limitations upon the delivery of DIC into cells for assimilation.”

“Some macroalgae also have HCO3 transporters or co-transporters, which allow them to transport HCO3 directly into their cells (see Raven 2003 for review).”

“Conceivably, extended periods of light in aerated cultures depleted the medium in CO2, which would then reequilibrate during the dark phase [40, 41].”

“However, not all algal groups contain and utilize CCMs, as some rely upon the diffusive flux of CO2 to support photosynthetic rates [34-36].”

“This implies that the green algae are more enriched in 13C than the red algae, which is also consistent with the literature data (Raven 2003; Raven et al. 2002, 2005; Wang and Yeh 2003; Giordano et al. 2005).”

“This is because algae pho-tosynthesize under light and release organic matter, which supports methanogens activity (Raven, 2003; Li et al., 2024; Hall et al., 2022).”