Inorganic carbon concentrating mechanisms in free‐living and symbiotic dinoflagellates and chromerids

Abstract

Photosynthetic dinoflagellates are ecologically and biogeochemically important in marine and freshwater environments. However, surprisingly little is known of how this group acquires inorganic carbon or how these diverse processes evolved. Consequently, how CO2 availability ultimately influences the success of dinoflagellates over space and time remains poorly resolved compared to other microalgal groups. Here we review the evidence. Photosynthetic core dinoflagellates have a Form II RuBisCO (replaced by Form IB or Form ID in derived dinoflagellates). The in vitro kinetics of the Form II RuBisCO from dinoflagellates are largely unknown, but dinoflagellates with Form II (and other) RuBisCOs have inorganic carbon concentrating mechanisms (CCMs), as indicated by in vivo internal inorganic C accumulation and affinity for external inorganic C. However, the location of the membrane(s) at which the essential active transport component(s) of the CCM occur(s) is (are) unresolved; isolation and characterization of functionally competent chloroplasts would help in this respect. Endosymbiotic Symbiodiniaceae (in Foraminifera, Acantharia, Radiolaria, Ciliata, Porifera, Acoela, Cnidaria, and Mollusca) obtain inorganic C by transport from seawater through host tissue. In corals this transport apparently provides an inorganic C concentration around the photobiont that obviates the need for photobiont CCM. This is not the case for tridacnid bivalves, medusae, or, possibly, Foraminifera. Overcoming these long‐standing knowledge gaps relies on technical advances (e.g., the in vitro kinetics of Form II RuBisCO) that can functionally track the fate of inorganic C forms.

In vivo assessment of mitochondrial respiratory alternative oxidase activity and cyclic electron flow around photosystem I on small coral fragments

“…For this reason, light-induced absorption changes of P700 were directly measured at 705 nm 45 by applying μs detecting flashes during short intervals of dark pulses (as described in 46 ). Continuous actinic light at different intensities (25,85,210,380, 670 and 1400 μmol photons m −2 s −1 ) was provided during 5 s (3 min for field coral specimens) by a LED array (640 nm). When coral fragments were exposed to continuous light, a stable negative change in absorbance at 705 nm (due to the formation of oxidized P700) 47 was obtained and recorded as Ps (Fig.…”

“…Carbon fixation is carried out by a type II Rubisco which is characterized by a low CO 2 -O 2 selectivity factor, and requires the presence of an efficient CO 2 concentrating mechanism 24 , 25 largely controlled by the host 26 , 27 that limits the occurrence of the photorespiratory pathway 24 . After accomplishing carbohydrate synthesis, an important amount of photosynthetic products is transported to the host 28 thanks to the expression of membrane transporters 29 .…”

Evolution of Phytoplankton in Relation to Their Physiological Traits

“…Others are planktonic in the ocean, or benthic or planktonic in inland waters [31]. There have been multiple losses of photosynthesis in dinoflagellates, and replacement over varying timespans with kleptoplastids retained after phagotrophy, with varying extents of retention of quantities of extra-plastidial genetic material from the ingested phototroph [32]. The upper extremes of genome retention, other than retention of entire cells, potentially capable of free-living growth and survival, are the diatom endosymbionts as 'dinotoms'; there are also cyanobacterial symbionts [32].…”

“…This greater limitation to diffusion results in a larger CO 2 depletion and O 2 enrichment in the light in cyanobacterial hypersaline mats and marine diatom mats [136][137][138] than is the case for planktonic photosynthetic organisms [139,140]. The widespread occurrence of inorganic carbon concentrating mechanisms (CCMs), in planktonic eukaryotic algae, and the universal occurrence of CCMs in photosynthetically competent cyanobacteria [32,140] and basal, peridinin-containing dinoflagellates [23], shows that the greater perceived need for CCMs in benthic microbial oxygenic photosynthetic organisms does not distinguish phytoplankton from microphytobenthos with respect to the occurrence of CCMs. The CCMs are almost all based on active transport of bicarbonate, some on active transport of protons, and with little evidence of a role for C 4 -like metabolism [32,140].…”

“…The widespread occurrence of inorganic carbon concentrating mechanisms (CCMs), in planktonic eukaryotic algae, and the universal occurrence of CCMs in photosynthetically competent cyanobacteria [32,140] and basal, peridinin-containing dinoflagellates [23], shows that the greater perceived need for CCMs in benthic microbial oxygenic photosynthetic organisms does not distinguish phytoplankton from microphytobenthos with respect to the occurrence of CCMs. The CCMs are almost all based on active transport of bicarbonate, some on active transport of protons, and with little evidence of a role for C 4 -like metabolism [32,140]. The limited data do not permit differentiation of inorganic carbon acquisition mechanisms in planktonic and benthic microalgae [32,140,141].…”