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In reef-building corals (order Scleractinia) and giant clams (phylum Molluca), V-type H + -ATPase (VHA) in host cells is part of a carbon concentrating mechanism (CCM) that regulates photosynthetic rates of their symbiotic algae. Here, we show that VHA plays a similar role in the sea anemone Anemonia majano , a member of the order Actinaria and sister group to the Scleractinia, which in contrast to their colonial calcifying coral relatives is a solitary, soft-bodied taxa. Western blotting and immunofluorescence revealed that VHA was abundantly present in the host-derived symbiosome membrane surrounding the photosymbionts. Pharmacological inhibition of VHA activity in individual anemones resulted in an approximately 80% decrease of photosynthetic O 2 production. These results extend the presence of a host-controlled VHA-dependent CCM to non-calcifying cnidarians of the order Actiniaria, suggesting it is widespread among photosymbiosis between aquatic invertebrates and Symbiodiniaceae algae.

In reef-building corals (order Scleractinia) and giant clams (phylum Molluca), V-type H+-ATPase (VHA) in host cells is part of a carbon concentrating mechanism (CCM) that regulates photosynthetic rates of their symbiotic algae. Here, we show that VHA plays a similar role in the sea anemone Anemonia majano, a member of the order Actinaria and sister group to the Scleractinia, which in contrast to their colonial calcifying coral relatives is a solitary, soft-bodied taxa. Western blotting and immunofluorescence revealed that VHA was abundantly present in the host-derived symbiosome membrane surrounding the photosymbionts. Pharmacological inhibition of VHA activity in individual anemones resulted in an approximately 80% decrease of photosynthetic O2 production. These results extend the presence of a host-controlled VHA-dependent CCM to non-calcifying cnidarians of the order Actiniaria, suggesting it is widespread among photosymbiosis between aquatic invertebrates and Symbiodiniaceae algae.

In reef-building corals (order Scleractinia) and giant clams (phylum Molluca), V-type H+-ATPase (VHA) in host cells is part of a carbon concentrating mechanism (CCM) that regulates photosynthetic rates of their symbiotic algae. Here, we show that VHA plays a similar role in the sea anemone Anemonia majano, a member of the order Actinaria and sister group to the Scleractinia, which in contrast to their colonial calcifying coral relatives is a solitary, soft-bodied taxa. Western blotting and immunofluorescence revealed that VHA was abundantly present in the host-derived symbiosome membrane surrounding the photosymbionts. Pharmacological inhibition of VHA activity in individual anemones resulted in an approximately 80% decrease of photosynthetic O2 production. These results extend the presence of a host-controlled VHA-dependent CCM to non-calcifying cnidarians of the order Actiniaria, suggesting it is widespread among photosymbiosis between aquatic invertebrates and Symbiodiniaceae algae.

Hygrophila polysperma is a heterophyllous amphibious plant. The growth of H. polysperma in submerged conditions is challenging due to the low CO2 environment, increased resistance to gas diffusion, and bicarbonate ion (HCO3–) being the dominant dissolved inorganic carbon source. The submerged leaves of H. polysperma have significantly higher rates of underwater photosynthesis compared with the terrestrial leaves. 4,4′-Diisothiocyanatostilbene-2,2′-disulfonate (DIDS), an anion exchanger protein inhibitor, and ethoxyzolamide (EZ), an inhibitor of internal carbonic anhydrase, repressed underwater photosynthesis by the submerged leaves. These results suggested that H. polysperma acclimates to the submerged condition by using HCO3– for photosynthesis. H. polysperma transports HCO3– into the leaf by a DIDS-sensitive HCO3– transporter and converted to CO2 by carbonic anhydrase. Additionally, proteome analysis revealed that submerged leaves accumulated fewer proteins associated with C4 photosynthesis compared with terrestrial leaves. This finding suggested that H. polysperma is capable of C4 and C3 photosynthesis in the terrestrial and submerged leaves, respectively. The ratio of phosphoenol pyruvate carboxylase to ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) in the submerged leaves was less than that in the terrestrial leaves. Upon anatomical observation, the terrestrial leaves exhibited a phenotype similar to the Kranz anatomy found among C4 plants; however, chloroplasts in the bundle sheath cells were not located adjacent to the vascular bundles, and the typical Kranz anatomy was absent in submerged leaves. These results suggest that H. polysperma performs proto-Kranz type photosynthesis in a terrestrial environment and shifts from a proto-Kranz type in terrestrial leaves to a HCO3– use photosynthesis in the submerged environments.

Hygrophila polysperma is a heterophyllous amphibious plant. The growth of H. polysperma in submerged conditions is challenging due to the low CO2 environment, increased resistance to gas diffusion, and bicarbonate ion (HCO3–) being the dominant dissolved inorganic carbon source. The submerged leaves of H. polysperma have significantly higher rates of underwater photosynthesis compared with the terrestrial leaves. 4,4′-Diisothiocyanatostilbene-2,2′-disulfonate (DIDS), an anion exchanger protein inhibitor, and ethoxyzolamide (EZ), an inhibitor of internal carbonic anhydrase, repressed underwater photosynthesis by the submerged leaves. These results suggested that H. polysperma acclimates to the submerged condition by using HCO3– for photosynthesis. H. polysperma transports HCO3– into the leaf by a DIDS-sensitive HCO3– transporter and converted to CO2 by carbonic anhydrase. Additionally, proteome analysis revealed that submerged leaves accumulated fewer proteins associated with C4 photosynthesis compared with terrestrial leaves. This finding suggested that H. polysperma is capable of C4 and C3 photosynthesis in the terrestrial and submerged leaves, respectively. The ratio of phosphoenol pyruvate carboxylase to ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) in the submerged leaves was less than that in the terrestrial leaves. Upon anatomical observation, the terrestrial leaves exhibited a phenotype similar to the Kranz anatomy found among C4 plants; however, chloroplasts in the bundle sheath cells were not located adjacent to the vascular bundles, and the typical Kranz anatomy was absent in submerged leaves. These results suggest that H. polysperma performs proto-Kranz type photosynthesis in a terrestrial environment and shifts from a proto-Kranz type in terrestrial leaves to a HCO3– use photosynthesis in the submerged environments.

A field dataset detailing the abundance and carbon use strategies (obtained with C13 isotopes) of marine macroalgae within 3 wave-exposed and 4 wave-sheltered coastal kelp forests in Otago, New Zealand, along with site information such as temperature, light, nutrients of each site. Additionally, a dataset of the results from a laboratory experiment measuring the photosynthetic response of Xiphophora gladiata and Hymenena palmata to increasing DIC concentrations and under high or low water motion and high (8.1) or low (7.6) pH.

Photoautotrophic organisms globally fix 111-117x1015 grams of carbon per year and around half of this global net primary production is aquatic (Behrenfeld et al., 2001; Field et al., 1998), with green algae a major contributor to this global carbon fixation. However, aquatic environments have some limitations The concentration of CO2 is often 2,200 times lower in water than in air, and diffusion is also 8,000 times slower. In addition, Rubisco, which catalyses the first major step of carbon fixation, converting atmospheric CO2 into precursors of energy-rich molecules, exhibits slow catalytic rates, low affinity for CO2 and competition from O2 for the active sites. Therefore, most green algae have developed a Carbon Concentrating Mechanism (CCM). In eukaryotic micro-algae, the Rubisco micro-compartment is called the pyrenoid and together with active inorganic carbon transporters and strategically located carbonic anhydrases, elevated CO2 within the pyrenoid improves photosynthetic efficiency. Most photosynthetic organisms have an hexadecameric Rubisco holoenzyme (L8S8), composed of eight ~55-kDa large subunit (LSU), encoded by a chloroplast gene (rbcL) and eight ~15-kDa small subunit (SSU), encoded by a nuclear gene family (RbcS) in Form I Rubisco. The CCM has been particularly well-defined in the model unicellular chlorophyte Chlamydomonas reinhardtii and recent studies showed that for full CCM induction, a key protein linker EPYC1 and its interaction with Rubisco SSU were necessary. The overall goal of this study was to use a phylogenetic approach, firstly to investigate SSU structure across the green algal phylogeny, and also to explore CCM diversity in two specific groups of species. This study used a variety of methodologies combining physiological experiments, biochemistry, imaging and bioinformatic analyses. The results firstly showed the presence of two different Rubisco SSU structures within the green algae. Secondly, the Rubisco catalytic properties found in streptophyte algae closely related to land plants (streptophytes) reflect the strength of any CCM and pyrenoid leakiness, whereas Rubisco in extant land plants reflects more recent selective pressures associated with the terrestrial atmospheric environment. This research also provides evidence for diversity of CCM expression in two closely related genera (Chlamydomonas and Chloromonas), ranging from species expressing a CCM and pyrenoid, or a CCM without a pyrenoid, to neither pyrenoid or CCM. This study provides the first preliminary analyses of five different genomes confirming multiple independent origins of the pyrenoid in green algae but has also allowed an initial comparison of the molecular components essential for pyrenoid formation across these species., Natural Environment Research Council (grant number NE/L002507/1 to Howard Griffiths) and resources associated with BBSRC-BB/M007693/1, BB/I024518/1 as part of the Combining Algal and Plant Photosynthesis (CAPP), supported by BBSRC and NSF. We are grateful for a Cambridge Trust Vice Chancellor’s award and Lucy Cavendish College, Cambridge, for supporting the PhD scholarship of Myriam Goudet. Doug Orr and Elizabete Carmo-Silva acknowledge support from the UK Biotechnology and Biological Sciences Research Council (BBSRC; grant number BB/I024488/1).

Background Pyropia yezoensis (Rhodophyta) is widely cultivated in East Asia and plays important economic, ecological and research roles. Although inorganic carbon utilization of P. yezoensis has been investigated from a physiological aspect, the carbon concentration mechanism (CCM) of P. yezoensis remains unclear. To explore the CCM of P. yezoensis, especially during its different life stages, we tracked changes in the transcriptome, photosynthetic efficiency and in key enzyme activities under different inorganic carbon concentrations. Results Photosynthetic efficiency demonstrated that sporophytes were more sensitive to low carbon (LC) than gametophytes, with increased photosynthesis rate during both life stages under high carbon (HC) compared to normal carbon (NC) conditions. The amount of starch and number of plastoglobuli in cells corresponded with the growth reaction to different inorganic carbon (Ci) concentrations. We constructed 18 cDNA libraries from 18 samples (three biological replicates per Ci treatment at two life cycles stages) and sequenced these using the Illumina platform. De novo assembly generated 182,564 unigenes, including approximately 275 unigenes related to CCM. Most genes encoding internal carbonic anhydrase (CA) and bicarbonate transporters involved in the biophysical CCM pathway were induced under LC in comparison with NC, with transcript abundance of some PyCAs in gametophytes typically higher than that in sporophytes. We identified all key genes participating in the C4 pathway and showed that their RNA abundances changed with varying Ci conditions. High decarboxylating activity of PEPCKase and low PEPCase activity were observed in P. yezoensis. Activities of other key enzymes involved in the C4-like pathway were higher under HC than under the other two conditions. Pyruvate carboxylase (PYC) showed higher carboxylation activity than PEPC under these Ci conditions. Isocitrate lyase (ICL) showed high activity, but the activity of malate synthase (MS) was very low. Conclusion We elucidated the CCM of P. yezoensis from transcriptome and enzyme activity levels. All results indicated at least two types of CCM in P. yezoensis, one involving CA and an anion exchanger (transporter), and a second, C4-like pathway belonging to the PEPCK subtype. PYC may play the main carboxylation role in this C4-like pathway, which functions in both the sporophyte and gametophyte life cycles.

Symbiotic dinoflagellate algae residing inside coral tissues supply the host with the majority of their energy requirements through the translocation of photosynthetically fixed carbon. The algae, in turn, rely on the host for the supply of inorganic carbon. Carbon must be concentrated as CO2 in order for photosynthesis to proceed, and here we show that the coral host plays an active role in this process. The host-derived symbiosome membrane surrounding the algae abundantly expresses vacuolar H(+)-ATPase (VHA), which acidifies the symbiosome space down to pH ∼ 4. Inhibition of VHA results in a significant decrease in average H(+) activity in the symbiosome of up to 75% and a significant reduction in O2 production rate, a measure of photosynthetic activity. These results suggest that host VHA is part of a previously unidentified carbon concentrating mechanism for algal photosynthesis and provide mechanistic evidence that coral host cells can actively modulate the physiology of their symbionts.

The fluxes of CO 2 and oxygen during photosynthesis by cell suspensions of Tessellaria volvocina and Mallomonas papillosa were monitored mass spectrometrically. There was no rapid uptake of CO 2, only a slow drawdown to compensation concentrations of 26 lM for T. volvocina and 18 lM for M. papillosa, when O 2 evolution ceased, indicating a lack of active bicarbonate uptake by the cells. Darkening of the cells after a period of photosynthesis did not cause rapid release of CO 2, indicating the absence of an intracellular inorganic carbon pool. However, upon darkening a brief burst of CO 2 was observed similar to the post-illumination burst characteristic of C3 higher plants. Treatment of the cells of both species with the membrane-permeable carbonic anhydrase inhibitor ethoxyzolamide had no adverse effect on photosynthetic rate, but stimulated the dark CO 2 burst indicating the dark oxidation of a compound formed in the light. In the absence of any active accumulation of inorganic carbon photosynthesis in these species should be inhibited by O 2. This was investigated in four synurophyte species T. volvocina, M. papillosa, Synura petersenii, and Synura uvella: Photosynthetic O 2 evolution rates in all four algae, measured by O 2 electrode, were significantly higher (40-50%) in media at low O 2 (4%) than in airequilibrated (21% O 2) media, indicating an O 2 inhibition of photosynthesis (Warburg effect) and thus the occurrence of photorespiration in these species. © Springer Science+Business Media B.V. 2011.