Dinghui Zou

Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels

Zou D. and Gao K. 2009. Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia 48: 510–517. DOI: 10.2216/08-99.1. The red seaweed Gracilaria lemaneiformis (Bory) Weber-van Bosse (Gigartinales, Rhodophyta) from Nanao Island, Shantou, China, was cultured at 370 and 700 µl l−1 CO2 in aeration and at intermediate (160 µmol photons m−2 s−1) and low (30 µmol photons m−2 s−1) irradiance levels in order to examine the influences of the elevated atmospheric CO2 concentrations on growth, photosynthetic performance and some biochemical components in this commercially important species. Relative growth rate (RGR) was significantly higher in G. lemaneiformis thalli grown using CO2-enriched air with respect to nonenriched air when the algae were subjected to intermediate irradiance. However, RGR was similar between these two CO2 treatments when the algae were grown under the low-irradiance condition. Extra CO2 in the culture decreased phycobiliprotein (PB, including phycoerythrin, PE, and phycocyanin, PC) contents of G. lemaneiformis thalli at the higher growth irradiance. However, chlorophyll a (Chl a) and soluble protein contents were unchanged by the CO2 levels in culture. Both PB and Chl a contents were higher in G. lemaneiformis thalli grown at the lower irradiance than at the higher irradiance, regardless of the CO2 levels in culture. The parameters for photosynthetic responses to irradiance and inorganic carbon were mostly not altered with the increase of CO2 concentrations in culture. However, light-saturated photosynthetic rates (Pmax) and apparent carboxylating efficiencies (ACE), expressed per unit Chl a, were significantly higher in algae grown at the intermediate irradiance compared to the low irradiance. Photosynthetic rate was reduced by an increase in pH of seawater from 8.2 to 9.1, and it was also strongly inhibited by the external carbonic anhydrase inhibitor acetazolamide (AZ) in G. lemaneiformis thalli grown at each CO2 and irradiance condition. Moreover, pH compensation points were not affected by the growth conditions. These results suggested that G. lemaneiformis under both growth conditions had a similar capacity of the photosynthetic utilization of external pool in seawater. However, ACE decreased in G. lemaneiformis thalli grown at the low irradiance with respect to the higher irradiance implied that the transport of Ci towards Rubisco within the cell was weakened. Taken together, the data showed that an increase of CO2 was less effective on G. lemaneiformis than the irradiance levels. We concluded that CO2 affected photosynthesis and growth performance when light was not the limiting factor.

Effects of desiccation and CO2 concentrations on emersed photosynthesis in Porphyra haitanensis (Bangiales, Rhodophyta), a species farmed in China

The effects on photosynthesis of CO2 and desiccation in Porphyra haitanensis were investigated to establish the effects of increased atmospheric CO2 on this alga during emersion at low tides. With enhanced desiccation, net photosynthesis, dark respiration, photosynthetic efficiency, apparent carboxylating efficiency and light saturation point decreased, while the light compensation point and CO2 compensation point increased. Emersed net photosynthesis was not saturated by the present atmospheric CO2 level (about 350 ml m−3), and doubling the CO2 concentration (700 ml m−3) increased photosynthesis by between 31% and 89% at moderate levels of desiccation. The relative enhancement of emersed net photosynthesis at 700 ml m−3 CO2 was greater at higher temperatures and higher levels of desiccation. The photosynthetic production of Porphyra haitanensis may benefit from increasing atmospheric CO2 concentration during emersion.

Impacts of increased atmospheric CO2 concentration on photosynthesis and growth of micro- and macro-algae

Marine photosynthesis drives the oceanic biological CO2 pump to absorb CO2 from the atmosphere, which sinks more than one third of the industry-originated CO2 into the ocean. The increasing atmospheric CO2 and subsequent rise of pCO2 in seawater, which alters the carbonate system and related chemical reactions and results in lower pH and higher HCO3− concentration, affect photosynthetic CO2 fixation processes of phytoplanktonic and macroalgal species in direct and/or indirect ways. Although many unicellular and multicellular species can operate CO2-concentrating mechanisms (CCMs) to utilize the large HCO3− pool in seawater, enriched CO2 up to several times the present atmospheric level has been shown to enhance photosynthesis and growth of both phytoplanktonic and macro-species that have less capacity of CCMs. Even for species that operate active CCMs and those whose photosynthesis is not limited by CO2 in seawater, increased CO2 levels can down-regulate their CCMs and therefore enhance their growth under light-limiting conditions (at higher CO2 levels, less light energy is required to drive CCM). Altered physiological performances under high-CO2 conditions may cause genetic alteration in view of adaptation over long time scale. Marine algae may adapt to a high CO2 oceanic environment so that the evolved communities in future are likely to be genetically different from the contemporary communities. However, most of the previous studies have been carried out under indoor conditions without considering the acidifying effects on seawater by increased CO2 and other interacting environmental factors, and little has been documented so far to explain how physiology of marine primary producers performs in a high-CO2 and low-pH ocean.

Effects of elevated CO2 and phosphorus supply on growth, photosynthesis and nutrient uptake in the marine macroalga Gracilaria lemaneiformis (Rhodophyta)

Chinese 973 Projects [2009CB421207]; National Natural Science Foundation of China [30970450, 30670396]; Chinese 863 Projects [2006AA10A416]

SHORT- AND LONG-TERM EFFECTS OF ELEVATED CO2 ON PHOTOSYNTHESIS AND RESPIRATION IN THE MARINE MACROALGA HIZIKIA FUSIFORMIS (SARGASSACEAE, PHAEOPHYTA) GROWN AT LOW AND HIGH N SUPPLIES

The short‐term and long‐term effects of elevated CO2 on photosynthesis and respiration were examined in cultures of the marine brown macroalga Hizikia fusiformis (Harv.) Okamura grown under ambient (375 μL · L−1) and elevated (700 μL · L−1) CO2 concentrations and at low and high N availability. Short‐term exposure to CO2 enrichment stimulated photosynthesis, and this stimulation was maintained with prolonged growth at elevated CO2, regardless of the N levels in culture, indicating no down‐regulation of photosynthesis with prolonged growth at elevated CO2. However, the photosynthetic rate of low‐N‐grown H. fusiformis was more responsive to CO2 enrichment than that of high‐N‐grown algae. Elevation of CO2 concentration increased the value of K1/2(Ci) (the half‐saturation constant) for photosynthesis, whereas high N supply lowered it. Neither short‐term nor long‐term CO2 enrichment had inhibitory effects on respiration rate, irrespective of the N supply, under which the algae were grown. Under high‐N growth, the Q10 value of respiration was higher in the elevated‐CO2‐grown algae than the ambient‐CO2‐grown algae. Either short‐ or long‐term exposure to CO2 enrichment decreased respiration as a proportion of gross photosynthesis (Pg) in low‐N‐grown H. fusiformis. It was proposed that in a future world of higher atmospheric CO2 concentration and simultaneous coastal eutrophication, the respiratory carbon flux would be more sensitive to changing temperature.

Photosynthetic utilization of inorganic carbon in the economic brown alga, Hizikia Fusiforme (Sargassaceae) from the South China Sea

The mechanism of inorganic carbon (Ci) acquisition by the economic brown macroalga, Hizikia fusiforme (Harv.) Okamura (Sargassaceae), was investigated to characterize its photosynthetic physiology. Both intracellular and extracellular carbonic anhydrase (CA) were detected, with the external CA activity accounting for about 5% of the total. Hizikia fusiforme showed higher rates of photosynthetic oxygen evolution at alkaline pH than those theoretically derived from the rates of uncatalyzed CO2 production from bicarbonate and exhibited a high pH compensation point (pH 9.66). The external CA inhibitor, acetazolamide, significantly depressed the photosynthetic oxygen evolution, whereas the anion‐exchanger inhibitor 4,4′‐diisothiocyano‐stilbene‐2,2′‐disulfonate had no inhibitory effect on it, implying the alga was capable of using HCO3− as a source of Ci for its photosynthesis via the mediation of the external CA. CO2 concentrations in the culture media affected its photosynthetic properties. A high level of CO2 (10,000 ppmv) resulted in a decrease in the external CA activity; however, a low CO2 level (20 ppmv) led to no changes in the external CA activity but raised the intracellular CA activity. Parallel to the reduction in the external CA activity at the high CO2 was a reduction in the photosynthetic CO2 affinity. Decreased activity of the external CA in the high CO2 grown samples led to reduced sensitiveness of photosynthesis to the addition of acetazolamide at alkaline pH. It was clearly indicated that H. fusiforme, which showed CO2‐limited photosynthesis with the half‐saturating concentration of Ci exceeding that of seawater, did not operate active HCO3− uptake but used it via the extracellular CA for its photosynthetic carbon fixation.

Seasonal pattern of reproduction of Hizikia fusiformis (Sargassaceae, Phaeophyta) from Nanao Island, Shantou, China

The maturation pattern of sexual reproduction in Hizikiafusiformis (Harvey) Okamura (Sargassaceae, Phaeaophyta) was examined in 2003 at Yunao Bay, Nanao Island, Shantou, China. Maturation began in mid-April (seawater temperature 19–21 ∘C), reached the peak in mid-May (maturation rate ca. 70%, and seawater temperature 23.5–25 ∘C) and finished in late-June (seawater temperature 27.5–30 ∘C). The Hizikia plants continued to gain the length from the beginning of maturation season to reach a maximum mean length of 34.8 cm in mid-May, after which the mean length was reduced drastically due to the senescence and rupture of the larger plants in size. The major portion of the mature plants belonged to the larger plants between April and May, but to the smaller ones in June. It is suggested that the plant must achieve a critical size before reproductive maturation occurred. There was a positive relationship between the number of receptacles (NR), as well as the reproductive allocation (RA), and the plant size of Hizikia population, with the recorded maximum values of NR and RA being 1220 and 64.3% respectively, for a single plant.

Photosynthetic bicarbonate utilization by a terrestrial cyanobacterium, Nostoc flagelliforme (Cyanophyceae)

The photosynthetic characteristics of the terrestrial cyanobacterium, Nostoc flagelliforme, after complete recovery by rewetting, was investigated to see whether it could use bicarbonate as the external inorganic carbon source when submerged. The photosynthesis–pH relationship and high pH compensation point suggested that the terrestrial alga could use bicarbonate to photosynthesize when submerged. The photosynthetic oxygen evolution rates were significantly inhibited in Na+‐free and Na++ Li+ media but were not affected by the absence of Cl−, implying that the bicarbonate uptake was associated with Na+/ HCO3− symport rather than Cl−/HCO3− exchange system.

Thermal acclimation of respiration and photosynthesis in the marine macroalga Gracilaria lemaneiformis (Gracilariales, Rhodophyta)

The responses of respiration and photosynthesis to temperature fluctuations in marine macroalgae have the potential to significantly affect coastal carbon fluxes and sequestration. In this study, the marine red macroalga Gracilaria lemaneiformis was cultured at three different temperatures (12, 19, and 26°C) and at high‐ and low‐nitrogen (N) availability, to investigate the acclimation potential of respiration and photosynthesis to temperature change. Measurements of respiratory and photosynthetic rates were made at five temperatures (7°C–33°C). An instantaneous change in temperature resulted in a change in the rates of respiration and photosynthesis, and the temperature sensitivities (i.e., the Q10 value) for both the metabolic processes were lower in 26°C‐grown algae than 12°C‐ or 19°C‐grown algae. Both respiration and photosynthesis acclimated to long‐term changes in temperature, irrespective of the N availability under which the algae were grown; respiration displayed strong acclimation, whereas photosynthesis only exhibited a partial acclimation response to changing growth temperatures. The ratio of respiration to gross photosynthesis was higher in 12°C‐grown algae, but displayed little difference between the algae grown at 19°C and 26°C. We propose that it is unlikely that respiration in G. lemaneiformis would increase significantly with global warming, although photosynthesis would increase at moderately elevated temperatures.

Ecophysiological responses of marine macroalgae to climate change factors

Marine macroalgae are ecologically and economically important primary producers, being adjacent to human living areas and playing key roles in coastal carbon cycles. They are subject to both regional and global environmental changes in coastal waters, where environmental factors fluctuate dramatically due to high biological production and land runoff. Since global ocean changes can influence coastal environments, global warming-induced ocean warming, ocean acidification (OA) caused by atmospheric CO2 rise and increasing ultraviolet B (UVB) irradiance at the earth’s surface are affecting physiology, life cycles, and community structures of macroalgae. Here, we examine recent progress towards understanding the effects of these climate change factors on ecophysiology of macroalgae. Some species tested show enhanced growth and/or photosynthesis under elevated CO2 levels or ocean acidification conditions, possibly due to increased availability of CO2 in seawater with neglected influence of pH drop. Nevertheless, OA can harm some macroalgae due to their high sensitivity to the acidic perturbation to intracellular acid–base stability. Mild ocean warming has been shown to benefit most macroalgae examined. Respiration quotient increased due to combined effects of ocean warming and acidification. UVB almost always harms the physiological functions of macroalgae, which develop protective strategies, such as accumulation of UV-absorbing compounds; UVA can drive photosynthesis under moderate levels of solar radiation or when solely exposed to it. However, little has been documented on the interactions of these multiple stressors. Future work requires further investigations to examine the effects of OA under complex environments or under multiple stressors to advance knowledge on macroalgal global change biology.