The Reemergence of Phycopathology_ When Algal Biology Meets Ecology.pdf

PY61CH11_MuruaARjats.clsAugust 14,202312:31Annual Review of PhytopathologyThe Reemergence ofPhycopathology:WhenAlgal Biology MeetsEcology and BiosecurityPedro Mura,1,2Andrea Garvetto,2,3Suhelen Egan,4and Claire M.M.Gachon2,51Instituto de Acuicultura,Universidad Austral de ChileSede Puerto Montt,Los Lagos,Chile;email:pedro.muruauach.cl2Scottish Association for Marine Science,Scottish Marine Institute,Oban,United Kingdom3Institute of Microbiology,Universitt Innsbruck,Innsbruck,Tyrol,Austria4Centre for Marine Science and Innovation,School of Biological,Earth and EnvironmentalSciences,University of New South Wales,Sydney,Australia5Musum National dHistoire Naturelle,CNRS,Paris,FranceAnnu.Rev.Phytopathol.2023.61:23155First published as a Review in Advance onMay 30,2023The Annual Review of Phytopathology is online atphyto.annualreviews.orghttps:/doi.org/10.1146/annurev-phyto-020620-120425Copyright 2023 by the author(s).This work islicensed under a Creative Commons Attribution 4.0International License,which permits unrestricteduse,distribution,and reproduction in any medium,provided the original author and source are credited.See credit lines of images or other third-partymaterial in this article for license information.Keywordsalgal diseases,algal aquaculture,algal ecology,algal parasitologyAbstractViruses,bacteria,and eukaryotic symbionts interact with algae in a varietyof ways to cause disease complexes,often shaping marine and freshwaterecosystems.The advent of phyconomy(a.k.a.seaweed agronomy)repre-sents a need for a greater understanding of algal disease interactions,whereunderestimated cryptic diversity and lack of phycopathological basis areprospective constraints for algal domestication.Here,we highlight thelimited yet increasing knowledge of algal pathogen biodiversity and the eco-logical interaction with their algal hosts.Finally,we discuss how ecologyand cultivation experience contribute to and reinforce aquaculture prac-tice,with the potential to reshape biosecurity policies of seaweed cultivationworldwide.231Annu.Rev.Phytopathol.2023.61:231-255.Downloaded from www.annualreviews.org Access provided by Xinjiang Institute of Ecology and Geography,CAoS on 09/06/23.See copyright for approved use.PY61CH11_MuruaARjats.clsAugust 14,202312:31ALGAE ARE NUMEROUS,TAXONOMICALLY AND PHYSIOLOGICALLYDIVERSE,AND MORE CULTIVATED THAN EVERAlgae are a polyphyletic group of phototrophic,mostly aquatic protists that have permanentlyacquired plastids through various independent endosymbiotic events(45).Sometimes,as is thecase here,photosynthetic prokaryotes such as cyanobacteria are also designated under this name.For convenience(especially in applied contexts),algae are further categorized with the de-scriptive terms microalgae and macroalgae,which encompass microscopic(typically unicellular)or macroscopic(typically multicellular)algae,respectively;in ecology,a similar distinction iswidely made between phytoplankton and seaweeds(for marine systems).Phytoplankton mainlyincludes diatoms(Stramenopiles:Bacillariophyceae),dinoflagellates(Alveolata:Dinoflagellata),coccolithophorids(Haptophyta),and cyanobacteria.Seaweeds comprise red(Rhodophyta),green(Chlorophyta sensu lato),and brown algae(Stramenopiles:Phaeophyceae)(23).Thediversityofapplicationsandkeyecologicalimportanceofalgaeinbothfreshwaterandma-rine ecosystems ensue from their broad phylogenetic diversity.Understanding of these ecologicalfunctions and diversity is currently undergoing rapid revision,not least thanks to the ongoing dis-covery of novel taxonomic and functional diversity by culture-independent metagenomics(e.g.,71)or novel single-cell imaging technologies(175).Collectively,algae are the basal part of foodchains in aquatic systems;they are estimated to account for more than half of the global pri-mary production(195)and thus play an essential role in global nutrient cycling processes(87).Macroalgae such as kelps(i.e.,large brown algae)form magnificent underwater forests in temper-ate and cold coastal seas worldwide,providing habitat and supporting fisheries;many seaweedsare considered bioengineers or foundation species because of their key importance in creatinglarge three-dimensional habitats that support diverse ecosystems(151).In this context,it is nowwell documented that the interactions of algae with pathogens have profound consequences onecosystem dynamics and structure as well as biogeochemical and evolutionary processes.In recent years,algae have also attracted renewed interest in the context of food safety,sustain-able energy supply,and the production of high-value products;algal aquaculture is developingexponentially worldwide,with multiple applications in the food,chemical,and pharmaceuticalindustries(152).The seaweed market is currently the fastest-growing aquaculture sector(approx-imately 8%per year)and represents 25%of the world global aquaculture production,reaching30 metric tonnes(Mt)for a total value of US$11.5 billion in 2019(55)(Figure 1).Al