Ocean Acidification Affects the Cytoskeleton, Lysozymes, and Nitric Oxide of Hemocytes: A Possible Explanation for the Hampered Phagocytosis in Blood Clams, Tegillarca granosa

Abstract

An enormous amount of anthropogenic carbon dioxide (CO2) has been dissolved into the ocean, leading to a lower pH and changes in the chemical properties of seawater, which has been termed ocean acidification (OA). The impacts of pCO2-driven acidification on immunity have been revealed recently in various marine organisms. However, the mechanism causing the reduction in phagocytosis still remains unclear. Therefore, the impacts of pCO2-driven OA at present and near-future levels (pH values of 8.1, 7.8, and 7.4) on the rate of phagocytosis, the abundance of cytoskeleton components, the levels of nitric oxide (NO), and the concentration and activity of lysozymes (LZM) of hemocytes were investigated in a commercial bivalve species, the blood clam (Tegillarca granosa). In addition, the effects of OA on the expression of genes regulating actin skeleton and nitric oxide synthesis 2 (NOS2) were also analyzed. The results obtained showed that the phagocytic rate, cytoskeleton component abundance, concentration and activity of LZM of hemocytes were all significantly reduced after a 2-week exposure to the future OA scenario of a pH of 7.4. On the contrary, a remarkable increase in the concentration of NO compared to that of the control was detected in clams exposed to OA. Furthermore, the expression of genes regulating the actin cytoskeleton and NOS were significantly up-regulated after OA exposure. Though the mechanism causing phagocytosis seemed to be complicated based on the results obtained in the present study and those reported previously, our results suggested that OA may reduce the phagocytosis of hemocytes by (1) decreasing the abundance of cytoskeleton components and therefore hampering the cytoskeleton-mediated process of engulfment, (2) reducing the concentration and activity of LZM and therefore constraining the degradation of the engulfed pathogen through an oxygen-independent pathway, and (3) inducing the production of NO, which may negatively regulate immune responses.

Ocean Acidification Impairs Foraging Behavior by Interfering With Olfactory Neural Signal Transduction in Black Sea Bream, Acanthopagrus schlegelii

“…In recent years, OA has drawn worldwide concern over its physiological and ecological effects on marine organisms, and it has been shown that a series of physiological processes, such as fertilization ( Parker et al, 2009 ; Sewell et al, 2013 ; Shi et al, 2017a , b ), embryonic development ( Egilsdottir et al, 2009 ; Przeslawski et al, 2015 ; Gravinese, 2017 ), metabolism ( Lannig et al, 2010 ; Carter et al, 2013 ; Kroeker et al, 2013 ; Wittmann and Pörtner, 2013 ; Zhao et al, 2017a , b ), immunity ( Bibby et al, 2008 ; Liu et al, 2016 ; Wang et al, 2016 ; Su et al, 2017 , 2018 ), and behavior ( Clements and Hunt, 2015 ; Nagelkerken and Munday, 2016 ; Peng et al, 2017 ), in various marine species can be affected by ocean acidification. In addition to altering pH, OA also reduces the availability of carbonate ions by decreasing the saturation state of calcium carbonate (CaCO 3 ) ( Kleypas et al, 1999 ).…”

Exposure to Decreased pH and Caffeine Affects Hemocyte Parameters in the Mussel Mytilus galloprovincialis

“…It is well documented that changes in environmental parameters can influence hemocyte functionality as shown in various studies concerning the effects of temperature [29,57,58] and salinity [59,60], as well as their combination [27]. Similarly, effects of pH alone [61][62][63] under various temperature and salinity values [28] were demonstrated in several bivalve species.…”

An Explanation Based on Energy-Related Changes for Blue Mussel Mytilus edulis Coping With Seawater Acidification

“…The average seawater surface pH has declined by approximately 0.1units compared with pre-industrial levels, and it is predicted to decline by an additional 0.3–0.4units by the end of this century ( Fabry et al, 2008 ; Gattuso et al, 2015 ). OA has been reported to exerted adverse effects on marine organisms, including fertilization ( Shi et al, 2017 ; Han et al, 2021 ), physiological responses ( Peng et al, 2017 ; Zhao et al, 2017a , b , 2020 ), immune responses ( Liu et al, 2016 ; Su et al, 2018 ), behavioral responses ( Peng et al, 2017 ; Rong et al, 2018 , 2020 ), and so on ( Liu, 2021 ). Kroeker et al (2011) findings indicated that OA decreased the diversity, biomass, and trophic complexity of benthic marine communities in reduced pH zones, with the highest reduction seen in the key calcifying species.…”