Effects of multiple drivers of ocean global change on the physiology and functional gene expression of the coccolithophore Emiliania huxleyi

Ongoing ocean global change due to anthropogenic activities is causing multiple chemical and physical seawater properties to change simultaneously, which may affect the physiology of marine phytoplankton. The coccolithophore Emiliania huxleyi is a model species often employed in the study of the marine carbon cycle. The effect of ocean acidification (OA) on coccolithophore calcification has been extensively studied; however, physiological responses to multiple environmental drivers are still largely unknown. Here we examined two‐way and multiple driver effects of OA and other key environmental drivers—nitrate, phosphate, irradiance, and temperature—on the growth, photosynthetic, and calcification rates, and the elemental composition of E. huxleyi. In addition, changes in functional gene expression were examined to understand the molecular mechanisms underpinning the physiological responses. The single driver manipulation experiments suggest decreased nitrate supply being the most important driver regulating E. huxleyi physiology, by significantly reducing the growth, photosynthetic, and calcification rates. In addition, the interaction of OA and decreased nitrate supply (projected for year 2100) had more negative synergistic effects on E. huxleyi physiology than all other two‐way factorial manipulations, suggesting a linkage between the single dominant driver (nitrate) effects and interactive effects with other drivers. Simultaneous manipulation of all five environmental drivers to the conditions of the projected year 2100 had the largest negative effects on most of the physiological metrics. Furthermore, functional genes associated with inorganic carbon acquisition (RubisCO, AEL1, and δCA) and calcification (CAX3, AEL1, PATP, and NhaA2) were most downregulated by the multiple driver manipulation, revealing linkages between responses of functional gene expression and associated physiological metrics. These findings together indicate that for more holistic projections of coccolithophore responses to future ocean global change, it is necessary to understand the relative importance of environmental drivers both individually (i.e., mechanistic understanding) and interactively (i.e., cumulative effect) on coccolithophore physiology.     

Nitrogen source and pCO2 synergistically affect carbon allocation,growth and morphology of the coccolithophore Emiliania huxleyi: potential implications of ocean acidification for the carbon cycle

Coccolithophores are unicellular phytoplankton that produce calcium carbonate coccoliths as an exoskeleton. Emiliania huxleyi, the most abundant coccolithophore in the world's ocean, plays a major role in the global carbon cycle by regulating the exchange of CO₂ across the ocean‐atmosphere interface through photosynthesis and calcium carbonate precipitation. As CO₂ concentration is rising in the atmosphere, the ocean is acidifying and ammonium (NH₄⁺) concentration of future ocean water is expected to rise. The latter is attributed to increasing anthropogenic nitrogen (N) deposition, increasing rates of cyanobacterial N₂ fixation due to warmer and more stratified oceans, and decreased rates of nitrification due to ocean acidification. Thus, future global climate change will cause oceanic phytoplankton to experience changes in multiple environmental parameters including CO₂, pH, temperature and nitrogen source. This study reports on the combined effect of elevated pCO₂ and increased NH₄⁺ to nitrate (NO₃^?) ratio (NH₄⁺/NO₃^?) on E. huxleyi, maintained in continuous cultures for more than 200 generations under two pCO₂ levels and two different N sources. Herein, we show that NH₄⁺ assimilation under N‐replete conditions depresses calcification at both low and high pCO₂, alters coccolith morphology, and increases primary production. We observed that N source and pCO₂ synergistically drive growth rates, cell size, and the ratio of inorganic to organic carbon. These responses to N source suggest that, compared to increasing CO₂ alone, a greater disruption of the organic carbon pump could be expected in response to the combined effect of increased NH₄⁺/NO₃^? ratio and CO₂ level in the future acidified ocean. Additional experiments conducted under lower nutrient conditions are needed prior to extrapolating our findings to the global oceans. Nonetheless, our results emphasize the need to assess combined effects of multiple environmental parameters on phytoplankton biology to develop accurate predictions of phytoplankton responses to ocean acidification.     

Gephyrocapsa huxleyi (Emiliania huxleyi) as a model system for coccolithophore biology

Coccolithophores are the most abundant calcifying organisms in modern oceans and are important primary producers in many marine ecosystems. Their ability to generate a cellular covering of calcium carbonate plates (coccoliths) plays a major role in marine biogeochemistry and the global carbon cycle. Coccolithophores also play an important role in sulfur cycling through the production of the climate-active gas dimethyl sulfide. The primary model organism for coccolithophore research is Emiliania huxleyi, now named Gephyrocapsa huxleyi. G. huxleyi has a cosmopolitan distribution, occupying coastal and oceanic environments across the globe, and is the most abundant coccolithophore in modern oceans. Research in G. huxleyi has identified many aspects of coccolithophore biology, from cell biology to ecological interactions. In this perspective, we summarize the key advances made using G. huxleyi and examine the emerging tools for research in this model organism. We discuss the key steps that need to be taken by the research community to advance G. huxleyi as a model organism and the suitability of other species as models for specific aspects of coccolithophore biology.     

Effects of elevated CO2 on growth,calcification, and spectral dependence of photoinhibition in the coccolithophore Emiliania huxleyi (Prymnesiophyceae)1

We studied the effects of elevated CO₂ concentrations on cell growth, calcification, and spectral variation in the sensitivity of photosynthesis to inhibition by solar radiation in the globally important coccolithophore Emiliania huxleyi. Growth rates and chlorophyll a content per cell showed no significant differences between elevated (800 ppmv) and ambient (400 ppmv) CO₂ conditions. However, the production of organic carbon and the cell quotas for both carbon and nitrogen, increased under elevated CO₂ conditions, whilst particulate inorganic carbon production rates decreased under the same conditions. Biometric analyses of cells showed that coccoliths only presented significant differences due to treatments in the central area width. Most importantly, the size of the coccosphere decreased under elevated CO₂ conditions. The susceptibility of photosynthesis to inhibition by ultraviolet radiation (UVR) was estimated using biological weighting functions (BWFs) and a model that predicts photosynthesis under photosynthetically active radiation and UVR exposures. BWF results demonstrated that the sensitivity of photosynthesis to UVR was not significantly different between E. huxleyi cells grown under elevated and present CO₂ concentrations. We propose that the acclimation to elevated CO₂ conditions involves a physiological mechanism of regulation and allocation of energy and metabolites in the cell, which is also responsible for altering the sensitivity to UVR. In coccolithophores, this mechanism might be affected by the decrease in the calcification rates.     

Interacting effects of ocean acidification and warming on growth and DMS‐production in the haptophyte coccolithophore Emiliania huxleyi

The production of the marine trace gas dimethyl sulfide (DMS) provides 90% of the marine biogenic sulfur in the atmosphere where it affects cloud formation and climate. The effects of increasing anthropogenic CO₂ and the resulting warming and ocean acidification on trace gas production in the oceans are poorly understood. Here we report the first measurements of DMS‐production and data on growth, DMSP and DMS concentrations in pH‐stated cultures of the phytoplankton haptophyte Emiliania huxleyi. Four different environmental conditions were tested: ambient, elevated CO₂ (+CO₂), elevated temperature (+T) and elevated temperature and CO₂ (+TCO₂). In comparison to the ambient treatment, average DMS production was about 50% lower in the +CO₂ treatment. Importantly, temperature had a strong effect on DMS production and the impacts outweighed the effects of a decrease in pH. As a result, the +T and +TCO₂ treatments showed significantly higher DMS production of 36.2 ± 2.58 and 31.5 ± 4.66 μmol L^?1 cell volume (CV) h^?1 in comparison with the +CO₂ treatment (14.9 ± 4.20 μmol L^?1 CV h^?1). As the cultures were aerated with an air/CO₂ mixture, DMS was effectively removed from the incubation bottles so that concentration remained relatively low (3.6–6.1 mmol L^?1 CV). Intracellular DMSP has been shown to increase in E. huxleyi as a result of elevated temperature and/or elevated CO₂ and our results are in agreement with this finding: the ambient and +CO₂ treatments showed 125 ± 20.4 and 162 ± 27.7 mmol L^?1 CV, whereas +T and +TCO₂ showed significantly increased intracellular DMSP concentrations of 195 ± 15.8 and 211 ± 28.2 mmol L^?1 CV respectively. Growth was unaffected by the treatments, but cell diameter decreased significantly under elevated temperature. These results indicate that DMS production is sensitive to CO₂ and temperature in E. huxleyi. Hence, global environmental change that manifests in ocean acidification and warming may not result in decreased DMS as suggested by earlier studies investigating the effect of elevated CO₂ in isolation.     

Dynamic energy budget modeling reveals the potential of future growth and calcification for the coccolithophore Emiliania huxleyi in an acidified ocean

Ocean acidification is likely to impact the calcification potential of marine organisms. In part due to the covarying nature of the ocean carbonate system components, including pH and CO₂ and CO₃^2? levels, it remains largely unclear how each of these components may affect calcification rates quantitatively. We develop a process‐based bioenergetic model that explains how several components of the ocean carbonate system collectively affect growth and calcification rates in Emiliania huxleyi, which plays a major role in marine primary production and biogeochemical carbon cycling. The model predicts that under the IPCC A2 emission scenario, its growth and calcification potential will have decreased by the end of the century, although those reductions are relatively modest. We anticipate that our model will be relevant for many other marine calcifying organisms, and that it can be used to improve our understanding of the impact of climate change on marine systems.     

海洋酸化对海洋无脊椎动物的影响研究进展

人源二氧化碳(CO2)的大量排放,导致空气中CO2浓度越来越高,其中大约1/4至1/3被海洋吸收。过多CO2在海水中的溶解,除引起海水p H值降低外,还导致海水中碳酸盐平衡体系的变化,即"海洋酸化"现象。很多海洋无脊椎动物不但在海洋生态系统中发挥重要作用,还是重要的水产养殖种,因此具有重要的生态与经济价值。由于海洋无脊椎动物的生活史在海水中完成,因此海洋环境的变化极易对其造成影响。大量研究已证实海洋酸化能对多种海洋无脊椎动物的受精、发育、生物钙化、基因表达等生命活动产生显著影响。综述了近年来海洋酸化对海洋无脊椎动物影响研究的相关报道,归纳了其对海洋无脊椎动物不同生命活动的影响,分析了其生态学效应,探讨了现有研究在方法创新、内容拓展以及机理分析等方面存在的局限与不足,并展望了海洋酸化对海洋无脊椎动物影响研究的发展方向。     

Adaptive evolution in the coccolithophore Gephyrocapsa oceanica following 1,000 generations of selection under elevated CO2

Coccolithophores are important oceanic primary producers not only in terms of photosynthesis but also because they produce calcite plates called coccoliths. Ongoing ocean acidification associated with changing seawater carbonate chemistry may impair calcification and other metabolic functions in coccolithophores. While short‐term ocean acidification effects on calcification and other properties have been examined in a variety of coccolithophore species, long‐term adaptive responses have scarcely been documented, other than for the single species Emiliania huxleyi. Here, we investigated the effects of ocean acidification on another ecologically important coccolithophore species, Gephyrocapsa oceanica, following 1,000 generations of growth under elevated CO₂ conditions (1,000 μatm). High CO₂‐selected populations exhibited reduced growth rates and enhanced particulate organic carbon (POC) and nitrogen (PON) production, relative to populations selected under ambient CO₂ (400 μatm). Particulate inorganic carbon (PIC) and PIC/POC ratios decreased progressively throughout the selection period in high CO₂‐selected cell lines. All of these trait changes persisted when high CO₂‐grown populations were moved back to ambient CO₂ conditions for about 10 generations. The results suggest that the calcification of some coccolithophores may be more heavily impaired by ocean acidification than previously predicted based on short‐term studies, with potentially large implications for the ocean's carbon cycle under accelerating anthropogenic influences.     

Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification

Ocean acidification (OA) and its associated decline in calcium carbonate saturation states is one of the major threats that tropical coral reefs face this century. Previous studies of the effect of OA on coral reef calcifiers have described a wide variety of outcomes for studies using comparable partial pressure of CO₂ (pCO₂) ranges, suggesting that key questions remain unresolved. One unresolved hypothesis posits that heterogeneity in the response of reef calcifiers to high pCO₂ is a result of regional-scale variation in the responses to OA. To test this hypothesis, we incubated two coral taxa (Pocillopora damicornis and massive Porites) and two calcified algae (Porolithon onkodes and Halimeda macroloba) under 400, 700 and 1000 μatm pCO₂ levels in experiments in Moorea (French Polynesia), Hawaii (USA) and Okinawa (Japan), where environmental conditions differ. Both corals and H. macroloba were insensitive to OA at all three locations, while the effects of OA on P. onkodes were location-specific. In Moorea and Hawaii, calcification of P. onkodes was depressed by high pCO₂, but for specimens in Okinawa, there was no effect of OA. Using a study of large geographical scale, we show that resistance to OA of some reef species is a constitutive character expressed across the Pacific.     

Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea,French Polynesia

This study tested the hypothesis that the response of corals to temperature and pCO ₂ is consistent between taxa. Juvenile massive Porites spp. and branches of P. rus from the back reef of Moorea were incubated for 1 month under combinations of temperature (29.3 °C and 25.6 °C) and pCO ₂ (41.6 Pa and 81.5 Pa) at an irradiance of 599 μmol quanta m^?2 s^?1. Using microcosms and CO₂ gas mixing technology, treatments were created in a partly nested design (tanks) with two between‐plot factors (temperature and pCO ₂), and one within‐plot factor (taxon); calcification was used as a dependent variable. pCO ₂ and temperature independently affected calcification, but the response differed between taxa. Massive Porites spp. was largely unaffected by the treatments, but P. rus grew 50% faster at 29.3 °C compared with 25.6 °C, and 28% slower at 81.5 Pa vs. 41.6 Pa CO₂. A compilation of studies placed the present results in a broader context and tested the hypothesis that calcification for individual coral genera is independent of pH, [HCO₃ ^?], and [CO₃ ^2?]. Unlike recent reviews, this analysis was restricted to studies reporting calcification in units that could be converted to nmol CaCO₃ cm^?2 h^?1. The compilation revealed a high degree of variation in calcification as a function of pH, [HCO₃ ^?], and [CO₃ ^2?], and supported three conclusions: (1) studies of the effects of ocean acidification on corals need to pay closer attention to reducing variance in experimental outcomes to achieve stronger synthetic capacity, (2) coral genera respond in dissimilar ways to pH, [HCO₃ ^?], and [CO₃ ^2?], and (3) calcification of massive Porites spp. is relatively resistant to short exposures of increased pCO ₂, similar to that expected within 100 y.     

鱼类对海洋升温与酸化的响应

自工业革命以来,空气中人为排放CO₂量增加,引起温室效应,导致地球表面温度升高和海水升温;同时,由于海-气界面气体交换,大气中CO₂部分溶解于海洋,引起海洋酸化。海洋升温加快鱼体内生化反应和代谢速率,并通过影响生长、觅食和繁殖等生命过程中能量供给,间接影响到鱼类种群分布、群落结构及生态系统的功能。而海水酸化会干扰海洋鱼类仔稚鱼的感觉和行为,增加其被捕食率,并削弱其野外生存能力,可能威胁自然种群补给量。综述了海洋升温、海洋酸化及其两者共同作用对海洋鱼类的影响,为预测鱼类响应全球海洋环境变化的响应趋势提供相关依据。     

Coralline algae elevate pH at the site of calcification under ocean acidification

Coralline algae provide important ecosystem services but are susceptible to the impacts of ocean acidification. However, the mechanisms are uncertain, and the magnitude is species specific. Here, we assess whether species‐specific responses to ocean acidification of coralline algae are related to differences in pH at the site of calcification within the calcifying fluid/medium (pH_cf) using δ¹¹B as a proxy. Declines in δ¹¹B for all three species are consistent with shifts in δ¹¹B expected if B(OH)₄^? was incorporated during precipitation. In particular, the δ¹¹B ratio in Amphiroa anceps was too low to allow for reasonable pH_cf values if B(OH)₃ rather than B(OH)₄^? was directly incorporated from the calcifying fluid. This points towards δ¹¹B being a reliable proxy for pH_cf for coralline algal calcite and that if B(OH)₃ is present in detectable proportions, it can be attributed to secondary postincorporation transformation of B(OH)₄^?. We thus show that pH_cf is elevated during calcification and that the extent is species specific. The net calcification of two species of coralline algae (Sporolithon durum, and Amphiroa anceps) declined under elevated CO₂, as did their pH_cf. Neogoniolithon sp. had the highest pH_cf, and most constant calcification rates, with the decrease in pH_cf being ¼ that of seawater pH in the treatments, demonstrating a control of coralline algae on carbonate chemistry at their site of calcification. The discovery that coralline algae upregulate pH_cf under ocean acidification is physiologically important and should be included in future models involving calcification.     

Detrimental effects of ocean acidification on the economically important Mediterranean red coral (Corallium rubrum)

The mean predicted decrease of 0.3–0.4 pH units in the global surface ocean by the end of the century has prompted urgent research to assess the potential effects of ocean acidification on the marine environment, with strong emphasis on calcifying organisms. Among them, the Mediterranean red coral (Corallium rubrum) is expected to be particularly susceptible to acidification effects, due to the elevated solubility of its Mg‐calcite skeleton. This, together with the large overexploitation of this species, depicts a bleak future for this organism over the next decades. In this study, we evaluated the effects of low pH on the species from aquaria experiments. Several colonies of C. rubrum were long‐term maintained for 314 days in aquaria at two different pH levels (8.10 and 7.81, pH_T). Calcification rate, spicule morphology, major biochemical constituents (protein, carbohydrates and lipids) and fatty acids composition were measured periodically. Exposure to lower pH conditions caused a significant decrease in the skeletal growth rate in comparison with the control treatment. Similarly, the spicule morphology clearly differed between both treatments at the end of the experiment, with aberrant shapes being observed only under the acidified conditions. On the other hand, while total organic matter was significantly higher under low pH conditions, no significant differences were detected between treatments regarding total carbohydrate, lipid, protein and fatty acid composition. However, the lower variability found among samples maintained in acidified conditions relative to controls, suggests a possible effect of pH decrease on the metabolism of the colonies. Our results show, for the first time, evidence of detrimental ocean acidification effects on this valuable and endangered coral species.     

Ocean acidification induces biochemical and morphological changes in the calcification process of large benthic foraminifera

Large benthic foraminifera are significant contributors to sediment formation on coral reefs, yet they are vulnerable to ocean acidification. Here, we assessed the biochemical and morphological impacts of acidification on the calcification of Amphistegina lessonii and Marginopora vertebralis exposed to different pH conditions. We measured growth rates (surface area and buoyant weight) and Ca-ATPase and Mg-ATPase activities and calculated shell density using micro-computer tomography images. In A. lessonii, we detected a significant decrease in buoyant weight, a reduction in the density of inner skeletal chambers, and an increase of Ca-ATPase and Mg-ATPase activities at pH 7.6 when compared with ambient conditions of pH 8.1. By contrast, M. vertebralis showed an inhibition in Mg-ATPase activity under lowered pH, with growth rate and skeletal density remaining constant. While M. vertebralis is considered to be more sensitive than A. lessonii owing to its high-Mg-calcite skeleton, it appears to be less affected by changes in pH, based on the parameters assessed in this study. We suggest difference in biochemical pathways of calcification as the main factor influencing response to changes in pH levels, and that A. lessonii and M. vertebralis have the ability to regulate biochemical functions to cope with short-term increases in acidity.     

Framework of barrier reefs threatened by ocean acidification

To date, studies of ocean acidification (OA) on coral reefs have focused on organisms rather than communities, and the few community effects that have been addressed have focused on shallow back reef habitats. The effects of OA on outer barrier reefs, which are the most striking of coral reef habitats and are functionally and physically different from back reefs, are unknown. Using 5‐m long outdoor flumes to create treatment conditions, we constructed coral reef communities comprised of calcified algae, corals, and reef pavement that were assembled to match the community structure at 17 m depth on the outer barrier reef of Moorea, French Polynesia. Communities were maintained under ambient and 1200 μatm pCO₂ for 7 weeks, and net calcification rates were measured at different flow speeds. Community net calcification was significantly affected by OA, especially at night when net calcification was depressed ~78% compared to ambient pCO₂. Flow speed (2–14 cm s^?1) enhanced net calcification only at night under elevated pCO₂. Reef pavement also was affected by OA, with dissolution ~86% higher under elevated pCO₂ compared to ambient pCO₂. These results suggest that net accretion of outer barrier reef communities will decline under OA conditions predicted within the next 100 years, largely because of increased dissolution of reef pavement. Such extensive dissolution poses a threat to the carbonate foundation of barrier reef communities.     

Elemental stoichiometry of the key calcifying marine phytoplankton Emiliania huxleyi under ocean climate change: A meta-analysis

The elemental composition of marine microorganisms (their C:N:P ratio, or stoichiometry) is central to understanding the biotic and biogeochemical processes underlying key marine ecosystem functions. Phytoplankton C:N:P is species specific and flexible to changing environmental conditions. However, bulk or fixed phytoplankton stoichiometry is usually assumed in biogeochemical and ecological models because more realistic, environmentally responsive C:N:P ratios have yet to be defined for key functional groups. Here, a comprehensive meta-analysis of experimental laboratory data reveals the variable C:N:P stoichiometry of Emiliania huxleyi, a globally significant calcifying phytoplankton species. Mean C:N:P of E. huxleyi is 124C:16N:1P under control conditions (i.e. growth not limited by one or more environmental stressors) and shows a range of responses to changes in nutrient and light availability, temperature and pCO₂. Macronutrient limitation caused strong shifts in stoichiometry, increasing N:P and C:P under P deficiency (by 305% and 493% respectively) and doubling C:N under N deficiency. Responses to light, temperature and pCO₂ were mixed but typically shifted cellular elemental content and C:N:P stoichiometry by ca. 30% or less. Besides these independent effects, the interactive effects of multiple environmental changes on E. huxleyi stoichiometry under future ocean conditions could be additive, synergistic or antagonistic. To synthesise our meta-analysis results, we explored how the cellular elemental content and C:N:P stoichiometry of E. huxleyi may respond to two hypothetical future ocean scenarios (increased temperature, irradiance and pCO₂ combined with either N deficiency or P deficiency) if an additive effect is assumed. Both future scenarios indicate decreased calcification (which is predominantly sensitive to elevated pCO₂), increased C:N, and up to fourfold shifts in C:P and N:P. Our results strongly suggest that climate change will significantly alter the role of E. huxleyi (and potentially other calcifying phytoplankton species) in marine biogeochemical processes.     

Short- and long-term conditioning of a temperate marine diatom community to acidification and warming

Ocean acidification and greenhouse warming will interactively influence competitive success of key phytoplankton groups such as diatoms, but how long-term responses to global change will affect community structure is unknown. We incubated a mixed natural diatom community from coastal New Zealand waters in a short-term (two-week) incubation experiment using a factorial matrix of warming and/or elevated pCO₂ and measured effects on community structure. We then isolated the dominant diatoms in clonal cultures and conditioned them for 1 year under the same temperature and pCO₂ conditions from which they were isolated, in order to allow for extended selection or acclimation by these abiotic environmental change factors in the absence of interspecific interactions. These conditioned isolates were then recombined into ‘artificial’ communities modelled after the original natural assemblage and allowed to compete under conditions identical to those in the short-term natural community experiment. In general, the resulting structure of both the unconditioned natural community and conditioned ‘artificial’ community experiments was similar, despite differences such as the loss of two species in the latter. pCO₂ and temperature had both individual and interactive effects on community structure, but temperature was more influential, as warming significantly reduced species richness. In this case, our short-term manipulative experiment with a mixed natural assemblage spanning weeks served as a reasonable proxy to predict the effects of global change forcing on diatom community structure after the component species were conditioned in isolation over an extended timescale. Future studies will be required to assess whether or not this is also the case for other types of algal communities from other marine regimes.     

Biomineralization changes with food supply confer juvenile scallops (Argopecten purpuratus) resistance to ocean acidification

Future ocean acidification (OA) will affect physiological traits of marine species, with calcifying species being particularly vulnerable. As OA entails high energy demands, particularly during the rapid juvenile growth phase, food supply may play a key role in the response of marine organisms to OA. We experimentally evaluated the role of food supply in modulating physiological responses and biomineralization processes in juveniles of the Chilean scallop, Argopecten purpuratus, that were exposed to control (pH ~ 8.0) and low pH (pH ~ 7.6) conditions using three food supply treatments (high, intermediate, and low). We found that pH and food levels had additive effects on the physiological response of the juvenile scallops. Metabolic rates, shell growth, net calcification, and ingestion rates increased significantly at low pH conditions, independent of food. These physiological responses increased significantly in organisms exposed to intermediate and high levels of food supply. Hence, food supply seems to play a major role modulating organismal response by providing the energetic means to bolster the physiological response of OA stress. On the contrary, the relative expression of chitin synthase, a functional molecule for biomineralization, increased significantly in scallops exposed to low food supply and low pH, which resulted in a thicker periostracum enriched with chitin polysaccharides. Under reduced food and low pH conditions, the adaptive organismal response was to trade‐off growth for the expression of biomineralization molecules and altering of the organic composition of shell periostracum, suggesting that the future performance of these calcifiers will depend on the trajectories of both OA and food supply. Thus, incorporating a suite of traits and multiple stressors in future studies of the adaptive organismal response may provide key insights on OA impacts on marine calcifiers.