Photosynthesis in marine macroalgae: evidence for carbon limitation

Holbrook, Gabriel P.; Beer, Sven; Spencer, William E.; Reiskind, Julia B.; Davis, Joseph S.; Bowes, George

doi:10.1139/b88-083

Cited by 69 publications

(31 citation statements)

References 18 publications

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“…The responses for Udotea are reminiscent of terrestrial C4 plants or the low-photorespiration state of freshwater angiosperms (6), while those of Codium appear more akin to C3 systems. It is apparent that a number of marine macroalgae do not exhibit a Warburg effect (4,6,19,22). Taxonomic consistency is obscure, as species with and without 02 inhibition occur in each division of marine macroalgae (6).…”

Section: Resultsmentioning

confidence: 99%

“…This has led to the general conclusion that marine macroalgae are C3 (5), not C4 plants (24). However, recent observations that many marine macroalgae have low r values and no Warburg effect at seawater DIC levels (4,6,19) 2Abbreviations: RuBPCO, ribulose-1,5-bisP carboxylase-oxygenase; CA, carbonic anhydrase; DIC, dissolved inorganic carbon (CO2 + HCO3); EZ, ethoxyzolamide; r, C02 compensation point; IRGA, infrared gas analysis; OAA, oxaloacetate; PCR, photosynthetic carbon reduction; PCO, photorespiratory carbon oxidation; PEP, P-enolpyruvate; PEPC, P-enolpyruvate carboxylase; PEPCK, P-enolpyruvate carboxykinase; TCA, tricarboxylic acid.…”

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confidence: 99%

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Alternative Methods of Photosynthetic Carbon Assimilation in Marine Macroalgae

Reiskind¹,

Seamon²,

Bowes³

1988

Plant Physiol.

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Two green macroalgae, Codium decorticatum and Udotea flabellum, differ photosynthetically. Codium had high O2-sensitive, and Udotea low 02-insensitive, CO2 compensation points; Codium showed a Warburg effect at seawater dissolved inorganic carbon levels and had photorespiratory C02 release, whereas Udotea did not. Seawater dissolved inorganic carbon levels did not saturate photosynthesis. For Codium, but not Udotea, the Warburg effect was increased by ethoxyzolamide, a carbonic anhydrase inhibitor, at high but not low pH. Isolated chloroplasts from both macroalgae showed a Warburg effect that was ethoxyzolamideinsensitive. In both macroalgae, chloroplastic and extrachloroplastic carbonic anhydrase activity was present. P-enolpyruvate carboxykinase (PEPCK) carboxylating activity in Udotea extracts was equivalent to that of ribulose bisphosphate carboxylase, and enzyme activities for C4 acid metabolism and P-enolpyruvate regeneration were sufficient to operate a limited C4-like system. In Udotea, malate and aspartate were earlylabeled photosynthetic products that turned over within 60 seconds. Photorespiratory compounds were much less labeled in Udotea. Low dark fixation rates ruled out Crassulacean acid metabolism. A limited C4-like system, based on PEPCK, is hypothesized to be the mechanism reducing photorespiration in Udotea. Codium showed no evidence of photosynthetic C4 acid metabolism. Marine macroalgae, like terrestrial angiosperms, seem to have diverse photosynthetic modes.In the three divisions of marine macroalgae, Rhodophyta (reds), Phaeophyta (browns), and Chlorophyta (greens), Ru-BPCO2 has been reported to be a major carboxylase, and labeling studies point to a functional PCR cycle (6,22,24). Photorespiration measurements and labeling of glycine and serine suggest that the PCO cycle also operates, and, furthermore, all three divisions contain species which exhibit 02 inhibition of photosynthesis or the Warburg effect and high r values (5-7, 22, 24, 28). This has led to the general conclusion that marine macroalgae are C3 (5) There is evidence that many, but not all, marine macroalgae use HCO3 ions for photosynthesis (4,6,10,22,24) and that CA is required (4, 10, 22). Thus, the possibility that they concentrate C02, in a manner comparable to unicellular organisms, has been broached (4, 6, 10); though there are no direct measurements of internal DIC levels to substantiate this hypothesis.Enzymes of C4 acid metabolism and C4 acid labeling during photosynthesis occur in some macroalgae (6,(22)(23)(24). In the case of brown macroalgae and marine diatoms, substantial ,8-carboxylation of PEP in the light and dark has been reported (20,24). The enzyme responsible is PEPCK acting in a carboxylating mode, not PEPC which occurs in terrestrial C4 plants (6,20,22,24). Dark fixation and diel titratable acidity changes associated with the PEPCK activity (22,24) are small, and a CAM-like system in brown macroalgae has been discounted (21). The operation of C4-like photosynthesis in marine macroalgae (23) is ...

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Alternative Methods of Photosynthetic Carbon Assimilation in Marine Macroalgae

Reiskind¹,

Seamon²,

Bowes³

1988

Plant Physiol.

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“…Beer & Koch 1996;Israel & Hophy 2002), others demonstrating increased photosynthetic production with increasing CO 2 (e.g. Holbrook et al 1988), and yet others switching the source of carbon with greater CO 2 availability (e.g. Johnston & Raven 1990;Schmid et al 1992).…”

Section: Discussionmentioning

confidence: 99%

The direct effects of increasing CO ₂ and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests

2010

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Predictions about the ecological consequences of oceanic uptake of CO 2 have been preoccupied with the effects of ocean acidification on calcifying organisms, particularly those critical to the formation of habitats (e.g. coral reefs) or their maintenance (e.g. grazing echinoderms). This focus overlooks the direct effects of CO 2 on non-calcareous taxa, particularly those that play critical roles in ecosystem shifts. We used two experiments to investigate whether increased CO 2 could exacerbate kelp loss by facilitating non-calcareous algae that, we hypothesized, (i) inhibit the recovery of kelp forests on an urbanized coast, and (ii) form more extensive covers and greater biomass under moderate future CO 2 and associated temperature increases. Our experimental removal of turfs from a phase-shifted system (i.e. kelp-to turf-dominated) revealed that the number of kelp recruits increased, thereby indicating that turfs can inhibit kelp recruitment. Future CO 2 and temperature interacted synergistically to have a positive effect on the abundance of algal turfs, whereby they had twice the biomass and occupied over four times more available space than under current conditions. We suggest that the current preoccupation with the negative effects of ocean acidification on marine calcifiers overlooks potentially profound effects of increasing CO 2 and temperature on non-calcifying organisms.

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“…Such CO2 fixation should be competitively inhibited by 02, with the oxygenase activity of Rubisco initiating the photorespiratory carbon oxidation cycle. However, many marine algae show no 02 inhibition of photosynthesis (1)(2)(3) (6), while cytosolic and mitochondrial isozymes, acting as GTPrequiring decarboxylases, regulate mammalian gluconeogenesis (7,8). In the algal protist Euglena, two forms operate: one as a gluconeogenic decarboxylase and one in CO2 fixation for the methylmalonyl CoA pathway (9).…”

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confidence: 99%