CO2-Driven Ocean Acidification Weakens Mussel Shell Defense Capacity and Induces Global Molecular Compensatory Responses
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Chemosphere 243 (2020) 125415 Contents lists available at ScienceDirect Chemosphere journal homepage: www.elsevier.com/locate/chemosphere CO2-driven ocean acidification weakens mussel shell defense capacity and induces global molecular compensatory responses * Xinguo Zhao a, b, c, Yu Han c, Bijuan Chen a, b, Bin Xia a, b, Keming Qu a, Guangxu Liu c, a Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, PR China b Laboratory for Marine Ecology and Environment Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, PR China c College of Animal Sciences, Zhejiang University, Hangzhou, 310058, PR China highlights graphical abstract OA will damage shell structure, and reduce shell strength and shell closure strength. OA will lead to extracellular acidosis þ and Ca2 deficiency. OA will significantly alter gene expression profile in mantle tissue. OA will weaken mussels’ shell de- fense capacity, and thus reduce their fitness. The findings of this study have sig- nificant ecological and economic implications. article info abstract Article history: Oceanic uptake of atmospheric CO2 is reducing seawater pH and shifting carbonate chemistry within, a Received 23 September 2019 process termed as ocean acidification (OA). Marine mussels are a family of ecologically and economically Received in revised form significant bivalves that are widely distributed along coastal areas worldwide. Studies have demon- 6 November 2019 strated that OA greatly disrupts mussels’ physiological functions. However, the underlying molecular Accepted 18 November 2019 responses (e.g., whether there were any molecular compensation mechanisms) and the extent to which Available online 19 November 2019 OA affects mussel shell defense capacity remain largely unknown. In this study, the thick shell mussels Handling Editor: Jim Lazorchak Mytilus coruscus were exposed to the ambient pH (8.1) or one of two lowered pH levels (7.8 and 7.4) for 40 days. The results suggest that future OA will damage shell structure and weaken shell strength and Keywords: shell closure strength, ultimately reducing mussel shell defense capacity. In addition, future OA will also þ þ Ocean acidification disrupt haemolymph pH and Ca2 homeostasis, leading to extracellular acidosis and Ca2 deficiency. Mussel Mantle transcriptome analyses indicate that mussels will adopt a series of molecular compensatory Calcification responses to mitigate these adverse effects; nevertheless, weakened shell defense capacity will increase Acid-base status mussels’ susceptibility to predators, parasites and pathogens, and thereby reduce their fitness. Overall, Defense capacity the findings of this study have significant ecological and economic implications, and will enhance our Mantle transcriptome sequencing understanding of the future of the mussel aquaculture industry and coastal ecosystems. © 2019 Elsevier Ltd. All rights reserved. 1. Introduction Anthropogenic activities (e.g., fossil fuel burning) emit large * Corresponding author. quantities of carbon dioxide (CO ) into the atmosphere. E-mail address: [email protected] (G. Liu). 2 https://doi.org/10.1016/j.chemosphere.2019.125415 0045-6535/© 2019 Elsevier Ltd. All rights reserved. 2 X. Zhao et al. / Chemosphere 243 (2020) 125415 Approximately one third of the CO2 is eventually absorbed by the show the physiological mechanisms underlying the observed al- global ocean (Sabine et al., 2004), leading to surface seawater pH terations in shell defense capacity. Importantly, owing to mantle’s reduction and carbonate chemistry shifts, a phenomenon known as critical roles in shell formation and growth, gene expression pro- ocean acidification (OA) (Caldeira and Wickett, 2003). Since the files of mantle tissue were investigated through transcriptome Industrial Revolution, surface seawater pH has already decreased sequencing to uncover the underlying molecular responses to OA. by 0.1 units, from approximately 8.21 to the current level of about 8.10 (Caldeira and Wickett, 2003). According to the Representative Concentration Pathway (RCP) 8.5 scenario of the Intergovern- 2. Materials and methods mental Panel on Climate Change (IPCC), the average surface seawater pH will further decrease by 0.3e0.4 and 0.7e0.8 units by 2.1. Animal collection and acclimation the end of the 21st and 23rd centuries, respectively (IPCC et al., 2014). Previous studies have suggested that OA poses a threat to Thick shell mussels M. coruscus (shell length of 21.91 ± 2.34 mm) a wide variety of marine organisms, especially calcifying organisms were collected from an intertidal site on Dongtou Island, Wenzhou, (Hofmann et al., 2010; Kerr, 2010). However, the responses of ma- China (121.22 E, 27.75 N), where the natural seawater pH ranges rine organisms to OA have been found to be species-specific and to from 8.0 to 8.2. The mussels were directly transported to the vary with life stage (Kroeker et al., 2010, 2013; Ries et al., 2009). For Qingjiang Station of Zhejiang Mariculture Research Institute, gently example, OA leads to decreases in metabolic rates in the blood clam cleaned of epibionts without damaging the shells, and acclimated Tegillarca granosa (Zhao et al., 2017b), wherease it leads to increases for two weeks in filtered and UV-irradiated natural seawater with in metabolic rates in the blue mussel Mytilus edulis (Thomsen and þ continuous aeration prior to the experiments. The seawater pH was Melzner, 2010). Similarly, the Ca2 content of the red king crab controlled at 8.10 ± 0.06, the temperature was controlled at Paralithodes camtschaticus is increased at the larvae stage, but re- 23 ± 0.4 C, and the salinity was controlled at 23 ± 0.5‰. The mains unchanged at the juvenile stage upon OA exposure (Long mussels were fed twice daily with the microalgae Platymonas et al., 2013a, 2013b). Regarding the species-specific and life stage subcordiformis at a rate of ~5% dry tissue weight, according to variations, the current understanding of biological responses to OA O’Donnell et al. (2013). Excess food and feces were removed daily cannot be simply applied to other species and/or life stages. through seawater changes, in which seawater was removed by Therefore, more research is needed to increase our understanding siphoning, followed by refilling with seawater pre-equilibrated to of the effects of OA on marine organisms and ecosystems. the desired pH values. Marine mussels are a family of ecologically and economically significant bivalve species that are widely distributed along coastal areas worldwide. By aggregating into beds, marine mussels create habitats for other organisms, and are thus recognized as important 2.2. Experimental design and seawater parameters marine ecosystem engineers (Borthagaray and Carranza, 2007). Many of them are important aquaculture species and have been Following acclimation, the mussels were randomly assigned to human food for thousands of years (Ponce Oliva et al., 2019). Ac- an ambient pH (8.1) group and two lowered pH (7.8 and 7.4) groups. cording to a report by the Food and Agriculture Organization of the The ambient seawater pH level (8.1) served as the control, while the United Nations (FAO), the mussel aquaculture industry was worth lowered pH levels of 7.8 and 7.4 were set to mimic the oceanic approximately 4.0 billion USD in 2016 (FAO yearbook, 2018). surface pH conditions projected for the years 2100 and 2300, Therefore, increasing attention has been paid to understanding respectively (IPCC et al., 2014). The seawater pH levels were ach- how OA affects marine mussels. Current evidence demonstrates ieved and maintained by continuously bubbling with CO2 gas that OA will exert significant negative effects on various physio- mixture, obtained by mixing CO2-free air and pure CO2 gas at logical processes in marine mussels, especially leading to the controlled flow rates, according to Zhao et al. (2017a). All pH levels reduction in calcification and even to shell damage (Asplund et al., were conducted with 10 replicate chambers that contained 10 in- 2014; Fitzer et al., 2015; Li et al., 2015a; Melzner et al., 2011; Sadler dividuals each and filled with approximately 10 L of filtered and et al., 2018; Thomsen et al., 2010, 2013). However, previous studies UV-irradiated natural seawater with the desired pH value have mainly focused on the physiological effects of OA, leaving the (Table S1). The mussels were fed with the microalgae underlying molecular responses (e.g., whether there were any P. subcordiformis as described above. The seawater was maintained molecular compensation mechanisms) largely overlooked. In at 23 C using temperature regulators, and was changed daily. addition, previous studies have mostly been performed with the Seawater chemistry parameters, including the pH, salinity, total blue mussel M. edulis. Considering the species-specific variations in alkalinity (TA) and carbonate system parameters, were monitored responses to OA mentioned above, whether findings in other spe- daily to ensure that no substantial fluctuations occurred cies also apply to mussel species such as M. coruscus needs to be throughout the experiment period. Seawater pH levels were investigated. Moreover, although shell defense capacity is crucial measured using a Sartorius PB-10 pH meter (Sartorius, Germany) for the survival of individual mussels, the extent to which OA affects calibrated with standard NBS buffers. Salinity was determined with this capacity remains largely unknown. a Multi 3410 conductivity meter