Modelling Antifouling compounds of Macroalgal Holobionts in Current and Future pH Conditions

Abstract

Marine macroalgae are important ecosystem engineers in marine coastal habitats. Macroalgae can be negatively impacted through excessive colonization by harmful bacteria, fungi, microalgae, and macro-colonisers and thus employ a range of chemical compounds to minimize such colonization. Recent research suggests that environmental pH conditions potentially impact the functionality of such chemical compounds. Here we predict if and how naturally fluctuating pH conditions and future conditions caused by ocean acidification will affect macroalgal (antifouling) compounds and thereby potentially alter the chemical defence mediated by these compounds. We defined the relevant ecological pH range, analysed and scored the pH-sensitivity of compounds with antifouling functions based on their modelled chemical properties before assessing their distribution across the phylogenetic macroalgal groups, and the proportion of sensitive compounds for each investigated function. For some key compounds, we also predicted in detail how the associated ecological function may develop across the pH range. The majority of compounds were unaffected by pH, but compounds containing phenolic and amine groups were found to be particularly sensitive to pH. Future pH changes due to predicted average open ocean acidification pH were found to have little effect. Compounds from Rhodophyta were mainly pH-stable. However, key algal species amongst Phaeophyceae and Chlorophyta were found to rely on highly pH-sensitive compounds for their chemical defence against harmful bacteria, microalgae, fungi, and biofouling by macro-organisms. All quorum sensing disruptive compounds were found the be unaffected by pH, but the other ecological functions were all conveyed in part by pH-sensitive compounds. For some ecological keystone species, all of their compounds mediating defence functions were found to be pH-sensitive based on our calculations, which may not only affect the health and fitness of the host alga resulting in host breakdown but also alter the associated ecological interactions of the macroalgal holobiont with micro and macrocolonisers, eventually causing ecosystem restructuring and the functions (e.g. habitat provision) provided by macroalgal hosts. Our study investigates a question of fundamental importance because environments with fluctuating or changing pH are common and apply not only to coastal marine habitats and estuaries but also to freshwater environments or terrestrial systems that are subject to acid rain. Hence, whilst warranting experimental validation, this investigation with macroalgae as model organisms can serve as a basis for future investigations in other aquatic or even terrestrial systems.

Keywords: Macroalgae; and macro-colonizers; antifouling; chemical communication; climate change; micro; ocean acidification.