Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems

Type Article
Acceptance Date 2024-02-20 IN PRESS
Language English
Author(s) Denoeud FranceORCID1, Godfroy OlivierORCID2, Cruaud CorinneORCID3, Heesch SvenjaORCID4, Nehr ZofiaORCID4, Tadrent NachidaORCID1, Couloux ArnaudORCID1, Brillet-Guéguen LoraineORCID5, 6, Delage LudovicORCID7, McKeown Dean6, Motomura Taizo8, Sussfeld DuncanORCID1, 9, Fan XiaoORCID10, 11, Mazéas Lisa2, Terrapon NicolasORCID12, 13, Barrera-Redondo JosuéORCID14, Petroll RomyORCID14, Reynes LauricORCID15, Choi Seok-WanORCID16, Jo JihoonORCID16, Uthanumallian KavithaORCID17, Bogaert KennyORCID18, Duc CélineORCID19, Ratchinski Pélagie4, Lipinska AgnieszkaORCID4, 14, Noel BenjaminORCID1, Murphy Eleanor A.ORCID20, 21, Lohr Martin22, Khatei AnanyaORCID23, Hamon-Giraud Pauline24, Vieira ChristopheORCID25, Akerfors Svea Sanja22, Akita ShingoORCID26, Avia KomlanORCID27, Badis YacineORCID4, Barbeyron TristanORCID2, Belcour ArnaudORCID24, Berrabah Wahiba1, Blanquart Samuel24, Bouguerba-Collin Ahlem2, Bringloe Trevor28, Cattolico Rose Ann29, Cormier AlexandreORCID30, Cruz De Carvalho HelenaORCID31, 32, Dallet Romain6, de Clerck OlivierORCID18, Debit Ahmed31, Denis Erwan1, Destombe ChristopheORCID15, Dinatale EricaORCID14, Dittami SimonORCID7, Drula ElodieORCID12, 13, Faugeron SylvainORCID33, Got JeanneORCID24, Graf LouisORCID16, Groisillier AgnèsORCID19, Guillemin Marie-LaureORCID15, 34, Harms LarsORCID35, Hatchett William JohnORCID36, Henrissat BernardORCID37, 38, Hoarau Galice36, Jollivet Chloé2, Jueterbock AlexanderORCID23, Kayal EhsanORCID6, Kogame KazuhiroORCID39, Le Bars Arthur6, 40, Leblanc CatherineORCID7, Ley Ronja22, Liu Xi6, Lopez Pascal Jean41, Lopez PhilippeORCID9, Manirakiza Eric19, Massau Karine6, Mauger StéphaneORCID15, Mest Laetitia4, Michel GurvanORCID2, Monteiro Catia7, Nagasato Chikako8, Nègre DelphineORCID6, Pelletier EricORCID1, Phillips NaomiORCID42, Potin PhilippeORCID7, Rensing Stefan A.ORCID43, Rousselot EllynORCID19, Rousvoal Sylvie7, Schroeder DeclanORCID44, Scornet DelphineORCID4, Siegel AnneORCID24, Tirichine LeilaORCID19, Tonon ThierryORCID45, Valentin KlausORCID35, Verbruggen HeroenORCID28, Weinberger FlorianORCID46, Wheeler GlenORCID21, Kawai HiroshiORCID47, Peters Akira F.ORCID48, Yoon Hwan SuORCID16, Hervé CecileORCID2, Ye NaihaoORCID10, 11, Bapteste EricORCID9, Valero Myriam15, Markov Gabriel V.ORCID7, Corre ErwanORCID6, Coelho Susana M.ORCID14, Wincker PatrickORCID1, Aury Jean-MarcORCID1, Cock J. MarkORCID4
Affiliation(s) 1 : Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Université Evry, Université Paris-Saclay, Evry, 91057, France
2 : Sorbonne Université, CNRS, Integrative Biology of Marine Models Laboratory, Station Biologique de Roscoff, Roscoff, France
3 : Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, Evry, 91057, France
4 : Sorbonne Université, CNRS, Algal Genetics Group, Integrative Biology of Marine Models Laboratory, Station Biologique de Roscoff, Roscoff, France
5 : CNRS, UMR 8227, Laboratory of Integrative Biology of Marine Models, Sorbonne Université, Station Biologique de Roscoff, Roscoff, France
6 : CNRS, Sorbonne Université, FR2424, ABiMS-IFB, Station Biologique, Roscoff, France
7 : Sorbonne Université, CNRS, UMR 8227, ABIE Team, Integrative Biology of Marine Models Laboratory, Station Biologique de Roscoff, Roscoff, France
8 : Muroran Marine Station, Hokkaido University, Muroran, Japan
9 : Institut de Systématique, Evolution, Biodiversité (ISYEB), UMR 7205, Sorbonne Université, CNRS, Museum
10 : State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong 266071, China
11 : Laboratory for Marine Fisheries Science and Food Production Processes, Laoshan Laboratory, Qingdao, Shandong 266237, China
12 : Aix Marseille Univ, CNRS, UMR 7257 AFMB, Marseille, France
13 : INRAE, USC 1408 AFMB, Marseille, France
14 : Department of Algal Development and Evolution, Max Planck Institute for Biology, Max-Planck-Ring 5, 72076, Tübingen, Germany
15 : IRL 3614, UMR 7144, DISEEM, CNRS, Sorbonne Université, Station Biologique de Roscoff, Roscoff, 29688, France
16 : Department of Biological Sciences, Sungkyunkwan University, Suwon, 16419, Republic of Korea
17 : University of Melbourne, Australia
18 : Phycology Research Group, Ghent University, Krijgslaan 281 S8, 9000 Ghent, Belgium
19 : Nantes Université, CNRS, US2B, UMR 6286, F-44000 Nantes, France
20 : University of Bristol, UK
21 : Marine Biological Association, Plymouth, UK
22 : Johannes Gutenberg University, Mainz, Germany
23 : Algal and Microbial Biotechnology Division, Nord University, Norway
24 : Univ Rennes, Inria, CNRS, IRISA, Equipe Dyliss, Rennes, France
25 : Research Institute for Basic Sciences, Jeju National University, Jeju 63243, Korea
26 : Faculty of Fisheries Sciences, Hokkaido University, Minato-cho 3-1-1, Hakodate, Hokkaido, 041- 8611, Japan
27 : INRAE, Université de Strasbourg, UMR SVQV, 68000 Colmar, France
28 : University of Melbourne, Australia
29 : University of Washington, USA
30 : Ifremer, IRSI, SeBiMER Service de Bioinformatique de l'Ifremer, F-29280 Plouzané, France
31 : Institut de Biologie de l'ENS (IBENS), Département de Biologie, École normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
32 : Université Paris Est-Créteil (UPEC), Faculté des Sciences et Technologie, 61, avenue du Général De Gaulle 94000 Créteil, France
33 : Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile
34 : Núcleo Milenio MASH, Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile
35 : Alfred Wegener Institute (AWI), Bremenhaven
36 : Nord University, Norway
37 : Department of Biotechnology and Biomedicine, Technical University of Denmark, Kgs Lyngby, Denmar
38 : Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia
39 : Biological Sciences, Faculty of Science, Hokkaido University, Sapporo, 060-0810, Japan
40 : CNRS, Institut Français de Bioinformatique, IFB-core, Évry, France
41 : Centre National de la Recherche Scientifique, UMR BOREA MNHN/CNRS-8067/SU/IRD/Univ. Caen Normandie/Univ. Antilles, France
42 : Biology Department, Arcadia University, USA
43 : University of Freiburg, Germany
44 : Minneapolis-St Paul University, USA
45 : Centre for Novel Agricultural Products (CNAP), Department of Biology, University of York, Heslington, York YO10 5DD, United Kingdom
46 : GEOMAR Helmholtz Centre for Ocean Research, Kiel, Germany
47 : Kobe University Research Center for Inland Seas, Kobe, Japan
48 : Bezhin Rosko, 29250 Santeg, France
Source bioRxiv (Cold Spring Harbor Laboratory) In Press
DOI 10.1101/2024.02.19.579948
Note This article is a preprint and has not been certified by peer review
Abstract

 Brown 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. 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. Finally, 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.
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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, Kogame Kazuhiro, Le Bars Arthur, Leblanc Catherine, Ley Ronja, Liu Xi, 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 Cecile, Ye Naihao, Bapteste Eric, Valero Myriam, Markov Gabriel V., Corre Erwan, Coelho Susana M., Wincker Patrick, Aury Jean-Marc, Cock J. Mark. Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems. bioRxiv IN PRESS. Publisher's official version : https://doi.org/10.1101/2024.02.19.579948 , Open Access version : https://archimer.ifremer.fr/doc/00879/99116/