Asparagopsis armata Exudate Cocktail: The Quest for the Mechanisms of Toxic Action of an Invasive Seaweed on Marine Invertebrates

Abstract

The seaweed Asparagopsis armata exhibits a strong invasive behavior, producing halogenated compounds with effective biological effects. This study addresses the biochemical responses to sublethal concentrations of A. armata exudate on the marine snail Gibbula umbilicalis whole body and the shrimp Palaemon elegans eyes and hepatopancreas. Antioxidant defenses superoxide dismutase (SOD) and glutathione-S-transferase (GST), oxidative damage endpoints lipid peroxidation (LPO) and DNA damage, the neuronal parameter acetylcholinesterase (AChE), and the fatty acid profile were evaluated. Results revealed different metabolic responses in both species. Despite previous studies indicating that the exudate affected G. umbilicalis’ survival and behavior, this does not seem to result from oxidative stress or neurotoxicity. For P. elegans, the inhibition of AChE and the decrease of antioxidant capacity is concomitant with the increase of LPO, suggesting neurotoxicity and oxidative stress as contributor mechanisms of toxicity for this species. Fatty acid profile changes were more pronounced for P. elegans with a general increase in polyunsaturated fatty acids (PUFAs) with the exudate exposure, which commonly means a defense mechanism protecting from membrane disruption. Nonetheless, the omega-3 PUFAs arachidonic acid (ARA) and docosapentaenoic acid (DPA) increased in both invertebrates, indicating a common regulation mechanism of inflammation and immunity responses.

Biomarker Studies in Stress Biology: From the Gene to Population, from the Organism to the Application

“…If exposure rate outperforms intrinsic repair process, it will result in processes such as inflammation, ageing, and the development of multiple age-related diseases, such as neurodegenerative disorders and cancer [ 28 ]. This damage is most often assessed by addressing DNA strand breaks, either by using a comet assay technique [ 33 ] or a more high-throughput colorimetric assay [ 34 ]. The whole of oxidative damage may not represent solely a structural damage to the organism, but may in fact, alter metabolic functions by affecting proteins, which of course includes enzymes that, as mentioned, are involved in the detoxification process of ROS.…”

“…For instance, concerning oxidative stress, if one decides to choose one enzyme as a proxy, e.g., CAT, one will be looking for an increase in case of oxidative stress. Nevertheless, this might not be the case as the organism may be using other enzymes rather than CAT for the process (several organisms may not even possess this enzyme or few, e.g., Rato et al [ 37 ]) or an apparent normal or decreased activity might be the consequence of protein damage or production issues derived from severe systemic toxicity [ 34 ]. This is the framework where the need for a decision to choose from a limited, yet diverse array of biomarkers is paramount.…”

“…On the other hand, a non-hypothesis driven approach, where the overall view and expected and non-expected mechanisms are targeted, may suit a distantiation and better search for the unknown and intrinsic complexity of interconnected responses, but most often decreasing method sensitivity and increasing the challenge and risk of falling into too much indigestible information [ 9 ]. A more complete array of explanatory non-hypothesis driven tools such as a vaster selection of target biomarkers with higher throughput techniques like OMICS [ 35 , 43 , 44 , 45 ] or the fatty acid profile [ 34 , 46 , 47 , 48 , 49 ], e.g., may help us to hold a comprehensive knowledge of multipart biological processes as integrated systems rather than an assembly of isolated parts, but comes with an array of associated challenges and complex methods falling beyond the scope of this work.…”

“…Likewise, by allowing an understanding of how organisms respond to different environmental situations and their trade-offs that may relate to the capability of a population to thrive under those conditions [ 49 , 62 , 63 ], biomarkers may further provide important information about how species will cope in an introduced environment and how they will compete with native species for a given niche, under a current or changing environment, and potential adaptation and spread, disclosing potential invasive setups [ 58 , 64 , 65 ]. Also, and regarding biological invasions, studies have been reported on the impacts of the invasive species on native species biomarker endpoints which may lead to a community impairment and invasion success, as in the case of Asparagopsis armata , a red seaweed producing halogenated compounds and releasing them into the environment and with ecosystem impacts [ 34 ], namely survival, and also reported impacts on macrofauna energetic biomarkers [ 40 ], and oxidative stress and damage, neurotoxic effects, and inflammation and immune responses [ 34 ], limiting the number of foraging herbivores and creating a thriving environment for this species and modulating the landscape and biodiversity.…”

Ocean Warming May Enhance Biochemical Alterations Induced by an Invasive Seaweed Exudate in the Mussel Mytilus galloprovincialis

“…These alterations may be observed not only in terms of macroinvertebrates [9] but also of other seaweeds [12], possibly due to competition for resources (space and nutrients) and to the exudation of chemical compounds into the tide pools [13,14] produced as a chemical defense [10,15]. In fact, this red macroalga has been found to pose toxic effects to the physiological status of surrounding biota [16,17] when in contact with its exudate and even deterred feeding from potential consumers [18,19]. Algae from the genus Asparagopsis are a great source of halogenated organic compounds (such as halomethanes, haloacetates, haloacetones) and other secondary metabolites [14], which are thought to be the major responsible for these effects.…”