Molecular response of Sargassum vulgare to acidification at volcanic CO₂ vents: Insights from proteomic and metabolite analyses

Abstract

Ocean acidification is impacting marine life all over the world. Understanding how species can cope with the changes in seawater carbonate chemistry represents a challenging issue. We addressed this topic using underwater CO2 vents that naturally acidify some marine areas off the island of Ischia. In the most acidified area of the vents, having a mean pH value of 6.7, comparable to far‐future predicted acidification scenarios (by 2300), the biomass is dominated by the brown alga Sargassum vulgare. The novelty of the present study is the characterization of the S. vulgare proteome together with metabolite analyses to identify the key proteins, metabolites, and pathways affected by ocean acidification. A total of 367 and 387 proteins were identified in populations grown at pH that approximates the current global average (8.1) and acidified sites, respectively. Analysis of their relative abundance revealed that 304 proteins are present in samples from both sites: 111 proteins are either higher or exclusively present under acidified conditions, whereas 120 proteins are either lower or present only under control conditions. Functionally, under acidification, a decrease in proteins related to translation and post‐translational processes and an increase of proteins involved in photosynthesis, glycolysis, oxidation–reduction processes, and protein folding were observed. In addition, small‐molecule metabolism was affected, leading to a decrease of some fatty acids and antioxidant compounds under acidification. Overall, the results obtained by proteins and metabolites analyses, integrated with previous transcriptomic, physiological, and biochemical studies, allowed us to delineate the molecular strategies adopted by S. vulgare to grow in future acidified environments, including an increase of proteins involved in energetic metabolism, oxidation–reduction processes, and protein folding at the expense of proteins involved in translation and post‐translational processes.

Functional changes across marine habitats due to ocean acidification

“…Thus, the observed benthic assemblage structure and the abundance of species with these life‐history traits confirm that non‐calcifying macroalgal species (e.g., Dictyota dichotoma , Halopteris scoparia ) are generally physiologically tolerant to OA and even can exhibit enhanced growth under these conditions (Harvey, Kon, et al., 2021; Koch et al., 2013; Porzio et al., 2011). This tolerance to low pH conditions is explained by the ability of macroalgal species to increase photosynthetic rates, as they benefit from increased p CO 2 and higher availability of dissolved inorganic carbon (DIC) forms under OA conditions (Connell et al., 2013; Cornwall et al., 2017; Kumar et al., 2022).…”

Comparison and improvement of RNA extraction methods in Sargassum (Phaeophyta)

“…As a result, Sargassum has attracted more attention in recent years, especially in the fields of algal biomass analysis, distribution, adaptation, and artificial reproduction (Brooks et al, 2019; Chai et al, 2014; Kumar, AbdElgawad, et al, 2017; Kumar, Castellano, et al, 2017; Seo et al, 2022). In addition, molecular‐level research on Sargassum is rapidly increasing with advances in high‐throughput sequencing (Kumar et al, 2022; Kumar, AbdElgawad, et al, 2017; Kumar, Castellano, et al, 2017). However, there are still few reports about the genome assembly (Wang et al, 2020) and molecular mechanisms of Sargassum in response to climate change, partly due to the lack of detailed genome annotation information.…”

Responses of the Macroalga Ulva prolifera Müller to Ocean Acidification Revealed by Complementary NMR- and MS-Based Omics Approaches

“…In addition, indirect effects of the OA, such as the impacts on infochemical communications among organisms, may encompass the direct effect of the pH on the phenotype of plants and animals because the adaptation of organisms to a given environment is a complex process involving chemical defenses and communications that can be impaired even by minor changes of pH [21][22][23]. However, only few metabolomic studies are dedicated to macroalgae, despite their ecological importance in marine ecosystems [24][25][26][27][28].…”

“…Liquid chromatography-mass spectrometry (LC-MS)and nuclear magnetic resonance (NMR)-based metabolomics/lipidomics have steadily evolved during the last decade, allowing the elucidation of a greater variety of metabolites in complex biological samples and providing sufficient information to directly determine active biochemical pathways. Although some studies have already assessed the metabolic changes of marine organisms due to OA, information about the chemical adaptations of marine algae is still incomplete [24][25][26][27][28][48][49][50][51].…”