Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review

Kunshan Gao; Douglas A. Campbell

doi:10.1071/FP13247

REVIEW (Open Access)

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Photophysiological responses of marine diatoms to elevated CO₂ and decreased pH: a review

Kunshan Gao ^A ^C and Douglas A. Campbell ^B

+ Author Affiliations

- Author Affiliations

^A State Key Laboratory of Marine Environmental Science, Xiamen University, 361005 Xiamen, China.

^B Department of Biology, Mount Allison University, Sackville, NB E4L 1G7, Canada.

^C Corresponding author. Email: ksgao@xmu.edu.cn

Functional Plant Biology 41(5) 449-459 https://doi.org/10.1071/FP13247
Submitted: 21 August 2013 Accepted: 24 December 2013 Published: 13 February 2014

Journal Compilation © CSIRO Publishing 2014 Open Access CC BY-NC-ND

Abstract

Diatoms dominate nearly half of current oceanic productivity, so their responses to ocean acidification are of general concern regarding future oceanic carbon sequestration. Community, mesocosm and laboratory studies show a range of diatom growth and photophysiological responses to increasing pCO₂. Nearly 20 studies on effects of elevated pCO₂ on diatoms have shown stimulations, no effects or inhibitions of growth rates. These differential responses could result from differences in experimental setups, cell densities, levels of light and temperature, but also from taxon-specific physiology. Generally, ocean acidification treatments of lowered pH with elevated CO₂ stimulate diatom growth under low to moderate levels of light, but lead to growth inhibition when combined with excess light. Additionally, diatom cell sizes and their co-varying metabolic rates can influence responses to increasing pCO₂ and decreasing pH, although cell size effects are confounded with taxonomic specificities in cell structures and metabolism. Here we summarise known diatom growth and photophysiological responses to increasing pCO₂ and decreasing pH, and discuss some reasons for the diverse responses observed across studies.

Additional keywords: Bacillariophyceae, CO₂, diatom, ocean acidification, photoinhibition, photosynthesis.

Introduction

Increasing atmospheric CO₂ due to anthropogenic activities affects terrestrial photosynthesis, but is also causing pCO₂ to rise and pH to drop in the surface oceans, which influence marine primary producers (Beardall et al. 2009; Riebesell and Tortell 2011; Gao et al. 2012a), in a yet more complicated way due to the concurrent changes in seawater chemistry and ocean mixing.

Diatoms are suggested to have evolved between 100 and 200 million years ago (Sims et al. 2006), when atmospheric CO₂ is thought to have been ~2000 ppmv (Veron 2008), compared with current levels of ~400 ppmv and projected end-century levels of 750–1000 ppmv. The extant diatoms now contribute ~20% of the organic carbon generated globally each year by photosynthesis (Field et al. 1998). They exist both as phytoplankton and as benthic algae. At least some diatom species operate metabolic pathways unusual among studied phytoplankton, including a urea cycle (Allen et al. 2011) and a C₄ carboxylation path (Reinfelder et al. 2004; Haimovich-Dayan et al. 2013). Diatoms run highly efficient CO₂ concentrating mechanisms (CCMs) to achieve a high ratio of carboxylation to oxygenation (Raven et al. 2011; Reinfelder 2011). They tolerate high levels of UV radiation (Guan and Gao 2008; Wu et al. 2012a), enjoy a low susceptibility to photoinactivation of PSII compared with other phytoplankters (Six et al. 2007, 2009; Key et al. 2010; Wu et al. 2011) and successfully exploit variable light (Lavaud et al. 2004, 2007). They are, as a net result, by far the most successful group of eukaryotic aquatic primary producers, not only in terms of primary production but also in their number of species and their capacities to acclimate to environmental changes with diversified metabolisms. Diatom growth rates correlate closely with their size, decreasing almost linearly with the log of increasing cell volume, which ranges across eight orders of magnitude, with cell diameters ranging from ~2 µm to a few mm (Finkel et al. 2010). Diatoms have responded to past climate change through successions of differently sized cells, with a trend towards smaller cells under higher temperatures over the past 65 million years (Falkowski and Oliver 2007; Finkel et al. 2007).

The ongoing ocean acidification triggered by increasing atmospheric CO₂ concentration alters seawater carbonate chemistry, the availabilities and toxicities of nutrients (Millero et al. 2009). Ocean warming will in concert tend to drive increased stratification, decreasing the thickness of the upper mixing layer and lowering transport of nutrients from interior or deeper layers to the surface ocean (Doney 2006; Steinacher et al. 2010). These changes will differentially affect differently sized diatom species (Flynn et al. 2012), and thereby alter sinking rates and organic carbon export (Finkel et al. 2010). Therefore, growth and physiological responses of diatoms to elevated CO₂ concentrations have gained attention (Riebesell et al. 1993; Burkhardt and Riebesell 1997; Burkhardt et al. 1999). Stimulative, neutral and inhibitory effects of elevated CO₂ concentrations on diatom growth have been reported in different species or even in the same species (Riebesell et al. 1993; Burkhardt et al. 1999; Chen and Gao 2003; Kim et al. 2006; Wu et al. 2010; Yang and Gao 2012; Li and Campbell 2013) (Table 1). In this review, we focus on the effects of elevated CO₂ and lower pH on diatom photophysiology, by summarising studies of their growth and photophysiological responses to elevated CO₂ under different experimental conditions, and discuss some potential mechanisms to resolve the diversity of responses observed across studies to date.

**Table 1. Effects of elevated CO₂ concentrations reported in diatoms**

Ocean acidification

The oceans are presently absorbing ~25 million tons of CO₂ from the atmosphere each day, an important role in counteracting global warming (Sabine et al. 2004). This dissolution of CO₂ from the air is, however, acidifying the oceans (Doney 2006; Gattuso and Hansson 2011).

The exchange of CO₂ between the sea and atmosphere depends on temperature, salinity, physical mixing of seawater, respiration and photosynthesis. Therefore, CO₂ fluxes change horizontally due to physical, chemical and biological properties of waters. When CO₂ dissolves in seawater, it combines with water to form carbonic acid (CO₂ + H₂O → H₂CO₃) which dissociates to bicarbonate (H₂CO₃ → H⁺ + HCO₃^–), discharging protons (H⁺) and so ultimately attaining a state of new equilibrium. However, as the H⁺ concentration increases with CO₂ dissolution, the H⁺ releases can partially reverse the secondary dissociation reaction, leading to a decrease in carbonate ions (H⁺ + CO₃^2– → HCO₃^–). Typical changes linked with ocean acidification are therefore increased concentrations of pCO₂, H⁺ and HCO₃^–, decreases in the concentration of CO₃^2– and decreases in the CaCO₃ saturation state (Gattuso et al. 2010). Since the beginning of the industrial revolution, the pH of oceanic surface seawater has already dropped by ~0.1 unit due to atmospheric CO₂ rise (Caldeira and Wickett 2003), equivalent to about a 30% increase in the H⁺ concentration. With a further increase of CO₂ concentration in the atmosphere to 800–1000 ppmv under the IPCC A1F1 scenario (Houghton et al. 2001), by the end of this century, pH of the surface oceans will decrease by another 0.3–0.4 units (Feely et al. 2004; Sabine et al. 2004; Orr et al. 2005), thus, increasing [H⁺] by 100–150%. Consequently, organisms in the euphotic zone will be exposed to a higher CO₂ and a lower pH, and their physiologies will respond to changes in seawater carbonate chemistry, as well as to secondary changes in ionic speciation and cell surface chemistry driven by decreasing pH (Millero et al. 2009; Flynn et al. 2012; Hervé et al. 2012; Sugie and Yoshimura 2013). These chemical changes can directly affect physiology of marine organisms (Pörtner and Farrell 2008), but can also indirectly influence organismal responses to other environmental factors including UV radiation (Sobrino et al. 2008; Gao et al. 2009; Chen and Gao 2011; Li et al. 2012a), light (Bartual and Galvez 2002; Sobrino et al. 2008; McCarthy et al. 2012; Li and Campbell 2013), temperature change (Pörtner and Farrell 2008; Zou et al. 2011) or nutrients (Burkhardt and Riebesell 1997; Burkhardt et al. 1999; Riebesell and Tortell 2011; Li et al. 2012b).

Growth responses

Dissolved inorganic carbon (DIC) in surface seawater, at present, is ~100–200 times that of CO₂ in the atmosphere, but most seawater DIC is HCO₃^–, with CO₂ typically accounting for less than 1% in pelagic waters (Gattuso et al. 2010). In addition, CO₂ in seawater diffuses ~8000 times slower than in air, which can kinetically limit marine photosynthetic carbon fixation (Raven 1993; Riebesell et al. 1993; Morel et al. 1994). Growth of diatom species can, in turn, be limited by the availability of CO₂ (Riebesell et al. 1993), and oceanic primary production might thus be enhanced by increasing atmospheric CO₂ concentration (Hein and Sand-Jensen 1997; Schippers et al. 2004; Riebesell and Tortell 2011). However, the growth rate of diatom-dominated phytoplankton assemblages was not affected by an elevated pCO₂ concentration of 800 μatm during 2–5 days shipboard incubation under ~30% of incident sunlight (Tortell et al. 2000). Growth of Skeletonema costatum was not stimulated by an enriched CO₂ concentration (800 μatm) under laboratory conditions (Burkhardt and Riebesell 1997; Chen and Gao 2003, 2004a), but was enhanced in a mesocosm at an elevated CO₂ concentration of 750 μatm (Kim et al. 2006). Growth of the diatoms Phaeodactylum tricornutum (Schippers et al. 2004; Wu et al. 2010), Navicula pelliculosa (Low-Décarie et al. 2011) and Attheya sp. (King et al. 2011) were also enhanced under elevated CO₂ levels under laboratory conditions. However, in the diatom Chaetoceros muelleri, low-light treatments showed lower growth rates under elevated CO₂ conditions, but no CO₂ or pH effect was recorded under high light exposure (Ihnken et al. 2011). Under similar laboratory conditions, while growth of Thalassiosira pseudonana (CCMP 1335) was not stimulated at the elevated CO₂ levels of 760 (Crawfurd et al. 2011) or 1000 μatm (Yang and Gao 2012), T. pseudonana (CCMP 1014 and 1335) grew faster under low (McCarthy et al. 2012) to moderate light (Li and Campbell 2013) with pCO₂ of 750 μatm, but under higher light T. pseudonana CCMP 1335 suffered growth inhibition (Li and Campbell 2013). Growth rates of the diatoms S. costatum (CCMA110), P. tricornutum (CCMA 106) and T. pseudonana (CCMP 1335), when grown under different levels of sunlight and elevated CO₂ of 1000 μatm, were stimulated under lower light levels (5–30% surface daytime mean solar PAR), but inhibited under higher light levels, with a drop in the PAR threshold for growth saturation (Fig. 1). These results show that elevated CO₂ and light levels interact to affect diatom growth responses to ocean acidification, which may explain the different results obtained under different experimental setups, at least for the same species (Table 1). Some of these growth responses may relate to CO₂ dependent changes in the cellular susceptibility to photoinactivation of PSII (Li and Campbell 2013) (see below). Since future shoaling of upper-mixed-layer (UML) depths is expected to expose phytoplankton to increased solar irradiance, marine primary producers within UML are expected to suffer from enhanced light stress. However, both low-light CO₂ growth enhancement and high-light CO₂ growth inhibition could occur even within a single daytime solar cycle or a vertical mixing path, making the net community outcomes difficult to predict. Boelen et al. (2011) did not find any interactive effects of elevated CO₂ concentration and changing light levels nor fluctuating light on the growth and photosynthesis in the Antarctic diatom Chaetoceros brevis. Conversely, frequencies of light fluctuation that mimic different mixing regimes affect a coccolithophore’s response to ocean acidification (Jin et al. 2013a), implying an interactive effect of light fluctuation and ocean acidification, that could impose an additional layer of influence on the net species and community responses to increasing pCO₂.

**Fig. 1.** Light-dependence of diatom growth responses to elevated CO₂ (HC, 1000 μatm, pH_T 7.68) compared with ambient CO₂ level (LC, 390 μatm, pH_T 8.02). Growth rates were stimulated by elevated CO₂ under low to moderate PAR, but inhibited under higher PAR levels. The PAR thresholds for the transition from CO₂ growth stimulation, under lower light, to CO₂ growth inhibition, under higher light, were ~160 for *Phaeodactylum tricornutum* (a), 125 for *Thalassiosira pseudonana* (b) and 178 amol photons m⁻² s⁻¹, for *Skeletonema costatum* (c). These threshold light levels for the transition for CO₂ growth stimulation to CO₂ growth inhibition correspond to 22–36% of the incident surface solar PAR levels and are equivalent to PAR levels at 26–39 m depth in the South China Sea. The semi-continuous cultures were maintained under the sun and diluted every 24 h to ensure stability of cell density ranges and the seawater carbonate system (from Gao *et al*. 2012b).

Inorganic carbon acquisition mediated by elevated CO₂

Diatom Rubisco shows comparatively high CO₂ affinity and CO₂/O₂ selectivity, and is served by CO₂ concentrating mechanisms (CCMs) to supply CO₂ to Rubisco, and thereby diminish photorespiration (Roberts et al. 2007a). CCMs differ among studied diatom species. Thalassionema nitzschioides (Trimborn et al. 2009), Thalassiosira weissflogii and P. tricornutum (Burkhardt et al. 2001) actively take up both CO₂ and HCO₃^–, whereas Thalassiosira punctigera exclusively uses free CO₂ (Elzenga et al. 2000). T. pseudonana, though lacking periplasmic (known also as extracellular) carbonic anhydrase (eCA), can take up HCO₃^– directly (Nimer et al. 1997; Elzenga et al. 2000; Nakajima et al. 2013), and indeed uses HCO₃^– as the dominant substrate for photosynthesis even under increased pCO₂ (Hopkinson et al. 2013; Isensee et al. 2013). The eCA and intracellular carbonic anhydrase (iCA) facilitate Ci acquisition or utilisation by catalysing the inter-conversion of CO₂ and HCO₃^–.

The activity of eCA can be downregulated under elevated CO₂ concentrations relevant to climate change (Burkhardt et al. 2001; Chen and Gao 2003; Rost et al. 2003; Crawfurd et al. 2011). Therefore, active transport or use of HCO₃^– could be lowered under elevated CO₂. Different growth conditions can therefore bring about different efficiencies of algal CCMs or changing preferences for CO₂ or HCO₃^– (Korb et al. 1997; Nimer et al. 1997; Burkhardt et al. 2001). In microalgae and in cyanobacteria, very high CO₂ concentrations of up to 50000 µatm (or ppmv in air) turn off CCMs (Kaplan et al. 1980; Tsuzuki and Miyachi 1989; Raven 1991; Matsuda et al. 2001). CCM induction is closely related to the intracellular Ci pool, ambient CO₂ levels and oxygen availability (Woodger et al. 2005). CO₂ levels (up to 1000 µatm) relevant to future CO₂ levels projected for 2100 have been confirmed to partially downregulate CCMs in marine diatoms (Chen and Gao 2003; Trimborn et al. 2009; Wu et al. 2010, 2012a; Yang and Gao 2012) and to lower reliance upon an intracellular labile carbon pool (Isensee et al. 2013). Downregulation of CCMs can include decreased CO₂ affinity resulting in an increased requirement for pCO₂ to support photosynthesis, inhibition of carbonic anhydrase activity, depressed HCO₃^– transport, and downregulation of PEPCase and PEPCKase (Reinfelder et al. 2000; Giordano et al. 2005; Roberts et al. 2007a, 2007b; Raven 2010; Reinfelder 2011). Such CCM downregulation was found to be synchronised with diurnal photosynthetic performance in the diatom S. costatum (Chen and Gao 2004b).

CCMs in diatoms might connect to multiple metabolic pathways which differ among diatom species of differing physiology or sizes. In P. tricornutum, cAMP metabolism is involved to control CCM under elevated CO₂ levels (Harada et al. 2006). T. weissflogii appears to run a C₃–C₄-intermediate photosynthesis (Roberts et al. 2007a), which may concentrate Ci through incorporation into an organic C₄ carbon compound, before Rubisco-aided carboxylation (Reinfelder et al. 2000, 2004). However, in P. tricornutum, the C₄ path way was recently suggested to contribute to pH homeostasis or excitation dissipation, but not to a CCM function (Haimovich-Dayan et al. 2013).

CCMs consume energy (Raven 1991; Bouma et al. 1994; Crawfurd et al. 2011; Hopkinson et al. 2011). Active uptake of HCO₃^– and CO₂ is supported by cyclic and linear electron transport in cyanobacteria (Li and Canvin 1998). Pseudocyclic electron flow through the Mehler reaction can also contribute (Sültemeyer et al. 1993). The energisation mechanisms of diatom CCMs are as yet unclear. It addition to the initial uptake, it takes further energy to maintain high intracellular Ci levels by counteracting CO₂ efflux (Sukenik et al. 1997; Tchernov et al. 1997) although in diatoms tested to date efflux rates appear small (Burkhardt et al. 2001; Trimborn et al. 2009). The major energy expenditure by the CCMs in diatoms is active Ci transport, and a doubling of ambient [CO₂] could save ~20% of the CCM-related energy expenditure in several diatom species (Hopkinson et al. 2011). Under elevated CO₂ concentrations, the growth enhancement under limiting light levels could be partially due to downregulation of CCMs, thereby lowering energy costs (Raven and Johnston 1991; Gao et al. 2012b). Alternatively, since CCMs can also be downregulated under low light, elevated pCO₂ could have stimulated the low light growth of diatoms due to both increased availability of CO₂ and savings on the energy cost of CCM operation.

Photosynthetic responses

Light energy captured and delivered via photochemical processes powers the active transport of CO₂ and HCO₃ in cyanobacteria and microalgae (Sültemeyer et al. 1993; Sukenik et al. 1997; Li and Canvin 1998), and then assimilatory carboxylation. Elevated CO₂ concentration had no significant effect upon pigment contents nor upon the effective absorbance cross-section serving photosystem II photochemistry (σ_PSII) in S. costatum, P. tricornutum or T. pseudonana (Chen and Gao 2004a; Wu et al. 2010; Crawfurd et al. 2011; McCarthy et al. 2012; Li and Campbell 2013). Furthermore, elevated pCO₂ had only limited effects on levels of the major protein complexes mediating photosynthesis across multiple species of centric diatoms, grown under low to saturating light (McCarthy et al. 2012; Li and Campbell 2013).

The photochemical quantum yield of S. costatum, P. tricornutum and T. pseudonana decreases faster with increasing levels of PAR under elevated, than under ambient CO₂ levels (Gao et al. 2012b). Non-photochemical quenching (NPQ), however, increases faster in the high-CO₂ grown cells with increasing light levels compared with the ambient CO₂ grown cells (Gao et al. 2012b). Modulating NPQ helps diatoms, like other photoautoauphs, to withstand high or fluctuating levels of PAR (Niyogi et al. 2005; Lavaud et al. 2007; Zhu and Green 2010; Wu et al. 2012b). T. pseudonana employs NPQ to cope with light stress, even under elevated CO₂ levels, more effectively than does a strain of P. tricornutum (Yang and Gao 2012), so that photoinhibition of electron transport was observed in P. tricornutum, but not T. pseudonana, when grown under elevated CO₂ of 1000 µatm (Wu et al. 2010). These differential responses between two model diatoms show taxon-specific mechanisms in coping with the combined impacts of ocean acidification and light stress.

At a functional level, the diatoms P. tricornutum and T. pseudonana grown under elevated CO₂ of 1000 µatm, at subsaturating photosynthetically active radiation, showed an increase in photosynthetic carbon fixation rate per cell of more than 20% (Wu et al. 2010; Yang and Gao 2012). Their growth rate was, however, only enhanced by ~5% in P. tricornutum and was unaffected in T. pseudonana. Enhanced respiratory and photorespiratory carbon losses under elevated CO₂ are likely responsible for this discrepancy (Wu et al. 2010; Gao et al. 2012b; Yang and Gao 2012). In the toxic diatom Pseudo-nitzschia multiseries, maximum carbon fixation rates per cell also increased with elevated CO₂ levels, although the apparent light use efficiency was not affected (Sun et al. 2011). In Cylindrotheca closterium f. minutissima, when grown at 1000 µatm CO₂ under sunlight, rates of electron transport and O₂ evolution dropped compared with the cells grown at the ambient CO₂ concentration (Wu et al. 2012a).

PSII photoinactivation and UV responses

Diatoms, like all photoautotrophs, suffer light- and UV-dependent photoinactivation of their PSII centres (Kok 1956). To maintain their photosynthesis in the face of light-dependent photoinactivation, diatoms must use a metabolically expensive PSII repair cycle (Aro et al. 1993) to proteolytically remove photoinactivated protein subunits (Nixon et al. 2010; Nagao et al. 2012; Campbell et al. 2013) and replace them with newly synthesised subunits (Edelman and Mattoo 2008). In comparison with other phytoplankton groups, diatoms enjoy a relatively low susceptibility to photoinactivation of their PSII (Key et al. 2010; Wu et al. 2011, 2012b). In T. pseudonana CCMP 1335, however, the primary susceptibility to photoinactivation of PSII changes under elevated pCO₂ (Sobrino et al. 2008; McCarthy et al. 2012; Li and Campbell 2013). As a net result, cells under high pCO₂ and high light incur an increased metabolic expense to accelerate PSII protein cycling, to counter increased photoinactivation (G Li, DA Campbell, unpubl. data). This increased metabolic cost to maintain PSII function is a possible explanation for the pattern of growth stimulation under elevated pCO₂ under low to moderate light, but growth inhibition under excess light (Gao et al. 2012b; McCarthy et al. 2012; Li and Campbell 2013). We are as yet unsure as to the mechanism(s) for the changes in susceptibility to primary photoinactivation under elevated pCO₂. Decreased silification under elevated pCO₂ (Mejía et al. 2013) might alter cellular optics. Or, a drop in excitation dissipation capacity, as reported in cyanobacteria (Tchernov et al. 1997) and now suggested in diatoms (Haimovich-Dayan et al. 2013) could result if the CCM is partly downregulated. Evidence in this direction is that the content of the reactive-oxygen toxicity indicator malondialdehyde increases in T. pseudonana CCMP 1335 growing under elevated pCO₂ (Li and Campbell 2013), consistent with a downregulation of paths with photoprotective roles under elevated pCO₂.

Solar UV radiation (UVR, 280–400 nm) affects phytoplankton physiology and primary productivity (Häder 2011; and literatures cited therein). In T. pseudonana, acclimation to UVR, partially relieved the increased susceptibility to photoinhibition under elevated pCO₂ (Sobrino et al. 2008), consistent with a hormetic protective induction of reactive oxygen species (ROS) detoxification by UV acclimation. The effect of UV-B irradiance (280–320 nm) on P. tricornutum was counteracted under ocean acidification conditions (Li et al. 2012a). Cylindrotheca closterium f. minutissima did not show any significant growth response to solar UVR after acclimation to solar radiation, though a combination of UVR and elevated CO₂ concentration led to significant drop in maximal electron transport (Wu et al. 2012a).

Respiratory responses

Altered seawater carbonate chemistry due to ocean acidification could perturb energy requirements for the diatom cells, leading to changes in respiration. Mitochondrial respiration indeed increases under ocean acidification conditions of 1000 µatm pCO₂ (pH 7.8) by ~34% in P. tricornutum (Wu et al. 2010) and by 35% in T. pseudonana (Yang and Gao 2012). Increased acidity of seawater associated with increased pCO₂ could disturb cell surface (Flynn et al. 2012) or even intracellular pH stability, so that phytoplankton cells may need to allocate additional energy to transport ions against the acid–base perturbation. Cell surface effects of increasing pCO₂ and decreasing pH will vary with cell size and with the co-varying cellular metabolic rate (Flynn et al. 2012). Thus, increasing pCO₂ is likely to increase the influences of cell size on phytoplankton responses to environmental forcings (Finkel et al. 2010; Flynn et al. 2012).

Photorespiration and electron flows to oxygen can be important in photoprotection and short-term responses to excess light in diatoms (Wingler et al. 2000; Waring et al. 2010). Both P. tricornutum and T. pseudonana showed enhanced photorespiration by up to 23–27% under elevated CO₂ or ocean acidification conditions (Gao et al. 2012b). Cells of T. pseudonana grown under the elevated CO₂ level of 1000 µatm showed higher carbon fixation rates but a lower net O₂ evolution rate compared with cells grown under the ambient CO₂, although the cells exhibited equivalent electron transfer rates from PSII (Yang and Gao 2012), providing evidence for enhanced photorespiratory or pseudocyclic re-consumption of O₂ released from PSII, under ocean acidification. Enhanced excretion of organic compounds due to photorespiration can connect to production of transparent exopolymers in phytoplankton communities that include diatoms (Engel 2002). These metabolic pathways could result in discrepant effects of ocean acidification on different species or under different light levels.

Effects on diatom communities across diverse habitats

Although photosynthesis of diatoms is likely to be stimulated by increased availability of CO₂, lower pH might increase their respiration (Wu et al. 2010; Yang and Gao 2012) and their costs for photoprotection, therefore, the net effect of ocean acidification on diatoms will depend on multiple environmental forcings and possibly species-specific metabolic pathways.

Community level responses to rising pCO₂ and temperature vary across oceanic regions. In the north-east Atlantic and North Sea a 50 year (1960–2009) time series survey revealed a decline of dinoflagellate abundance, whereas diatoms showed relatively constant richness (Hinder et al. 2012). The transition over the half century was attributed to ocean warming and windy conditions. In contrast, elevated temperatures lowered the short-term abundance of diatoms in a North Atlantic Bloom incubation study (Feng et al. 2009), although CO₂ changes had no apparent effect. A shipboard incubation study that examined rising temperature and CO₂ in two natural Bering Sea assemblages also found large community shifts away from diatoms towards nanoflagellates in the ‘greenhouse’ treatment (Hare et al. 2007), though diatom-dominated phytoplankton growth increased in the Ross Sea under elevated CO₂ levels (Tortell et al. 2008).

Across a CO₂ and pH gradient off the volcanic island of Vulcano (Mediterranean, NE Sicily), periphyton communities altered significantly as CO₂ concentrations increased, with significant increases in chlorophyll a concentrations and in diatom abundance (Johnson et al. 2013).

Feng et al. (2010) found no interactive effects of light and CO₂ on community photosynthesis during an experiment using a Ross Sea diatom/Phaeocystis assemblage, but the diatom community structure shifted away from small pennate diatoms towards much larger centric diatoms. In the very different conditions of the South China Sea a shipboard incubation combining elevated CO₂ concentration and near surface solar irradiances, showed decreased photosynthesis while diatom abundance declined (Gao et al. (2012b).

In hypoxic seawaters, algae may experience large changes in the ratio of pO₂ to pCO₂ or respiration index (RI = log₁₀ (pO₂/pCO₂)), which is predicted to decline in future oceans (Brewer and Peltzer 2009). Together with lower pH, hypoxic areas represent a future situation of combined ocean acidification and deoxygenation. There has been little documented on the interactive effects of these two climate-change factors on diatoms nor upon other marine primary producers. However, changes in RI could affect net photosynthesis (Fig. 2) (Gao et al. 2012b; Xu and Gao 2012). For diatoms grown under either elevated or ambient levels of CO₂, net photosynthetic O₂ evolution decreases with increased RI (Fig. 2a, b).

**Fig. 2.** Decreased net photosynthetic O₂ evolution rates of algae with increased external partial pressure ratio of O₂ to CO₂ or respiration index (log₁₀(pO₂/pCO₂): (a) diatoms *Thalassiosira pseudonana* and (b) *Phaeodactylum tricornutum* and (c) green alga, *Ulva prolifera*, grown under elevated (HC, 1000 μatm) or ambient (LC, 390 μatm) CO₂ levels (re-constructed from Gao *et al*. 2012b; Xu and Gao 2012).

Future efforts

Based on the work summarised here, priorities for future study on diatoms include the following.

Response of frustule mineralisation to elevated CO₂ concentrations. Biogenic silicate content of some diatoms decreases under ocean acidification conditions (Hervé et al. 2012; Tatters et al. 2012; Mejía et al. 2013). However, we do not know the mechanisms involved, nor the interactive effects of multiple factors, such as warming, UV radiation, nutrient limitation, deoxygenation and cell surface pH (Flynn et al. 2012; Milligan and Morel 2002) upon silicate mineralisation.
Higher CO₂ concentrations appear to favour growth enhancement of larger rather than smaller diatoms (Feng et al. 2010) (Y Wu, AJ Irwin, D Suggett, D Campbell, ZV Finkel, unpubl. data). Mechanistic studies are needed to examine responses of differently sized diatoms to ocean acidification, to discriminate among direct size effects (Barton et al. 2013) and effects of taxonomic distinctions in cell structures (Mitchell et al. 2013) or metabolisms.
Coastal and pelagic water diatoms may react differently to ocean acidification due to their pre-adaptations to different regimes of mixing, nutrient and diel pH changes. In coastal waters, photosynthetic carbon fixation, and night-time respiration per volume of seawater is much higher, leading to high pH during the day and low pH during the night. Little is known about diatom responses to diel pH changes under elevated CO₂ concentrations as well as to diel changes in the respiration index of the water.
To guide the scope of studies responses of diatoms to ocean acidification should be examined under expected combinations of environmental changes. Although UV radiation appears not to influence the growth of some diatoms under elevated CO₂ level (Wu et al. 2012a), UV-B (280–315 nm) seems to counteract some effects of high CO₂ and low pH (Li et al. 2012a). Further studies are needed to explore physiological responses of diatoms to reasonable exposures to UV, temperature rise (Shatwell et al. 2012), fluctuation of irradiance to model changing mixing conditions, nutrient limitation and deoxygenation under elevated CO₂ and acidification conditions. Hundreds of genes in P. tricornutum are upregulated after acclimation to ocean acidification conditions (Y Li, F Su, Y Wu, KJ Wang, K Gao, unpubl. data), but little has been documented on long-term acclimation of open ocean diatoms, and studies on interactions between ocean acidification and the progression from exponential to stationary phase are just beginning (Orellana et al. 2013).
Evolutionary responses to increasing CO₂ concentration in diatoms should be examined for hundreds to thousands of generations. The coastal strain Thalassiosira pseudonana CCMP 1335 showed little evidence of evolutionary adaptation over months of growth at elevated CO₂ (Crawfurd et al. 2011). Evolutionary responses of the freshwater green alga Chlamydomonas sp. at high CO₂ demonstrated that some adapted cell lines lost CCM capabilities (Collins and Bell 2004; Collins et al. 2006). Lohbeck et al. (2012) found that 500 generations of selection at high CO₂ led to recovery of a coccolithophore’s growth rates and calcification, although 680 generations of selection at high CO₂ did not show such a trend in Gephyrocapsa oceanica (Jin et al. 2013b).
Monitoring community abundance of diatoms together with other key taxa over longer time scales is important to gain in situ information on their responses to environmental changes (Mutshinda et al. 2013). These field data obtained from different waters, when combined with mechanistic from controlled experiments would provide valuable insight into future climate change impacts upon phytoplankton communities.

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