Future CO2-induced ocean acidification mediates the physiological performance of a green tide alga.

The oceans take up more than 1 million tons of CO2 from the air per hour, about one-quarter of the anthropogenically released amount, leading to disrupted seawater chemistry due to increasing CO2 emissions. Based on the fossil fuel-intensive CO2 emission scenario (A1F1; Houghton et al., 2001), the H concentration or acidity of surface seawater will increase by about 150% (pH drop by 0.4) by the end of this century, the process known as ocean acidification (OA; Sabine et al., 2004; Doney et al., 2009; Gruber et al., 2012). Seawater pH is suggested to decrease faster in the coastal waters than in the pelagic oceans due to the interactions of hypoxia, respiration, and OA (Cai et al., 2011). Therefore, responses of coastal algae to OA are of general concern, considering the economic and social services provided by the coastal ecosystem that is adjacent to human living areas and that is dependent on coastal primary productivity. On the other hand, dynamic environmental changes in the coastal waters can interact with OA (Beardall et al., 2009). Macroalgae have diversified strategies in terms of inorganic carbon (Ci) acquisition, with different carboxylation efficiencies associated with different photosynthetic affinities for Ci (Johnston and Raven, 1990; Giordano et al., 2005; Zou and Gao, 2010). Most macroalgae can actively use bicarbonate or directly take up CO2 to provide a CO2 source for Rubisco, a mechanism known as the carbon-concentrating mechanism (CCM), while a few red and green macroalgae, known as “non bicarbonate users,” acquire Ci solely by diffusion of dissolved CO2 (Raven et al., 1995; Kübler et al., 1999). Therefore, macroalgae may respond differentially to increasing pCO2 (for partial pressure of CO2 in seawater) and the changing chemistry of seawater. Increasing atmospheric CO2 concentrations have been demonstrated to enhance the photosynthesis of intertidal macroalgae at low tide during emersion (Gao et al., 1999; Zou and Gao, 2005) and enhance the growth of the red algae Porphyra yezoensis, Gracilaria spp., and Lomentaria articulata (Gao et al., 1991, 1993; Kübler et al., 1999) and the brown alga Hizikia fusiforme (Zou, 2005). However, decreased growth rates under elevated CO2 concentrations are observed in Gracilaria tenuistipitata (Garcŕa-Sánchez et al., 1994), Porphyra leucostica (Mercado et al., 1999), and Porphyra linearis (Israel et al., 1999). Neutral effects of elevated CO2 levels (750 matm) on the growth of several macroalgae are also reported (Israel and Hophy, 2002). Recent research shows that meiospore germination in the brown macroalga Macrocystis pyrifera benefits from the increased availability of CO2 (820 matm; Roleda et al., 2012). Despite these differential responses, OA is notorious for reducing calcification of the red coralline algae (Gao et al., 1993; Gao and Zheng, 2010), green Halimeda spp. (Sinutok et al., 2011), and brown Padina spp. (Johnson et al., 2012). Furthermore, elevated CO2 has the potential to influence competition between noncalcareous macroalgae and coralline species (Hepburn et al., 2011). Marine green algae represent a large paraphyletic group of green plants from which the higher plants (the embryophytes) developed (Douglas et al., 2004). They share the same photosynthetic pigments with, but live in a quite different environment from, terrestrial higher plants. These plants, mostly distributed in coastal waters, where biological production is high, experience dynamic environmental changes associated with reciprocal tides and human activities. In most coastal waters, because of the photosynthetic carbon removal from and respiratory carbon release to the ambient environment, fluctuation of pH usually shows a day-night (high to low) reversion pattern. Therefore, marine green algae are usually tolerant to acid-base perturbations (Larsson et al., 1997), although the mechanisms involved are not understood yet. From a physiological point of view, marine green algae may show fairly different responses from terrestrial plants to increasing CO2 concentration, if acidity change acts to affect their physiology. However, to our knowledge, little has been documented on this aspect. Increased availability of ambient CO2 to about 1,000 matm based on the projected future atmospheric CO2 rise may not be large enough to affect the influx of CO2 1 This work was supported by the National Basic Research Program of China (grant no. 2009CB421207 to K.G.), the National Natural Science Foundation (grant nos. 41120164007 to KG., 41106093 to J.X., and 40930846 to K.G.), the Natural Science Foundation of Jiangsu Province (grant no. BK2011400 to J.X.), the Program for Changjiang Scholars and Innovative Research Team (grant no. IRT0941), and a China-Japan collaboration project from the Ministry of Science and Technology of China (grant no. S2012GR0290 to K.G). * Corresponding author; e-mail [email protected]. www.plantphysiol.org/cgi/doi/10.1104/pp.112.206961