Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems
Authors: Denoeud France , Godfroy Olivier , Cruaud Corinne , Heesch Svenja , Nehr Zofia , Tadrent Nachida , Couloux Arnaud , Brillet-Guéguen Loraine , Delage Ludovic , Mckeown Dean , Motomura Taizo , Sussfeld Duncan , Fan Xiao , Mazéas Lisa , Terrapon Nicolas , Barrera-Redondo Josué , Petroll Romy , Reynes Lauric , Choi Seok-Wan , Jo Jihoon , Uthanumallian Kavitha , Bogaert Kenny , Duc Céline , Ratchinski Pélagie , Lipinska Agnieszka , Noel Benjamin , Murphy Eleanor A. , Lohr Martin , Khatei Ananya , Hamon-Giraud Pauline , Vieira Christophe , Akerfors Svea Sanja , Akita Shingo , Avia Komlan , Badis Yacine , Barbeyron Tristan , Belcour Arnaud , Berrabah Wahiba , Blanquart Samuel , Bouguerba-Collin Ahlem , Bringloe Trevor , Cattolico Rose Ann , Cormier Alexandre , Cruz de Carvalho Helena , Dallet Romain , De Clerck Olivier , Debit Ahmed , Denis Erwan , Destombe Christophe , Dinatale Erica , Dittami Simon , Drula Elodie , Faugeron Sylvain , Got Jeanne , Graf Louis , Groisillier Agnès , Guillemin Marie-Laure , Harms Lars , Hatchett William John , Henrissat Bernard , Hoarau Galice , Jollivet Chloé , Jueterbock Alexander , Kayal Ehsan , Knoll Andrew H. , Kogame Kazuhiro , Le Bars Arthur , Leblanc Catherine , Le Gall Line , Ley Ronja , Liu Xi , LoDuca Steven T. , Lopez Pascal Jean , Lopez Philippe , Manirakiza Eric , Massau Karine , Mauger Stéphane , Mest Laetitia , Michel Gurvan , Monteiro Catia , Nagasato Chikako , Nègre Delphine , Pelletier Eric , Phillips Naomi , Potin Philippe , Rensing Stefan A. , Rousselot Ellyn , Rousvoal Sylvie , Schroeder Declan , Scornet Delphine , Siegel Anne , Tirichine Leila , Tonon Thierry , Valentin Klaus , Verbruggen Heroen , Weinberger Florian , Wheeler Glen , Kawai Hiroshi , Peters Akira F. , Yoon Hwan Su , Hervé Cécile , Ye Naihao , Bapteste Eric , Valero Myriam , Markov Gabriel V. , Corre Erwan , Coelho Susana M. , Wincker Patrick , Aury Jean-Marc , Cock Mark 
Published: February 2024

SUMMARYBrown seaweeds are keystone species of coastal ecosystems, often forming extensive underwater forests, that are under considerable threat from climate change. Despite their ecological and evolutionary importance, this phylogenetic group, which is very distantly related to animals and land plants, is still poorly characterised at the genome level. Here we analyse 60 new genomes that include species from all the major brown algal orders. Comparative analysis of these genomes indicated the occurrence of several major events coinciding approximately with the emergence of the brown algal lineage. These included marked gain of new orthologous gene families, enhanced protein domain rearrangement, horizontal gene transfer events and the acquisition of novel signalling molecules and metabolic pathways. The latter include enzymes implicated in processes emblematic of the brown algae such as biosynthesis of the alginate-based extracellular matrix, and halogen and phlorotannin biosynthesis. These early genomic innovations enabled the adaptation of brown algae to their intertidal habitats. The subsequent diversification of the brown algal orders tended to involve loss of gene families, and genomic features were identified that correlated with the emergence of differences in life cycle strategy, flagellar structure and halogen metabolism. Analysis of microevolutionary patterns within the genusEctocarpusindicated that deep gene flow between species may be an important factor in genome evolution on more recent timescales. Finally, we show that integration of large viral genomes has had a significant impact on brown algal genome content and propose that this process has persisted throughout the evolutionary history of the lineage.