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. 2024 Nov 18:S0092-8674(24)01272-8.
doi: 10.1016/j.cell.2024.10.049. Online ahead of print.

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

France Denoeud  1 , Olivier Godfroy  2 , Corinne Cruaud  3 , Svenja Heesch  4 , Zofia Nehr  4 , Nachida Tadrent  1 , Arnaud Couloux  1 , Loraine Brillet-Guéguen  5 , Ludovic Delage  6 , Dean Mckeown  7 , Taizo Motomura  8 , Duncan Sussfeld  9 , Xiao Fan  10 , Lisa Mazéas  2 , Nicolas Terrapon  11 , Josué Barrera-Redondo  12 , Romy Petroll  12 , Lauric Reynes  13 , Seok-Wan Choi  14 , Jihoon Jo  14 , Kavitha Uthanumallian  15 , Kenny Bogaert  16 , Céline Duc  17 , Pélagie Ratchinski  4 , Agnieszka Lipinska  18 , Benjamin Noel  1 , Eleanor A Murphy  19 , Martin Lohr  20 , Ananya Khatei  21 , Pauline Hamon-Giraud  22 , Christophe Vieira  23 , Komlan Avia  24 , Svea Sanja Akerfors  20 , Shingo Akita  25 , Yacine Badis  4 , Tristan Barbeyron  2 , Arnaud Belcour  22 , Wahiba Berrabah  1 , Samuel Blanquart  22 , Ahlem Bouguerba-Collin  2 , Trevor Bringloe  15 , Rose Ann Cattolico  26 , Alexandre Cormier  27 , Helena Cruz de Carvalho  28 , Romain Dallet  7 , Olivier De Clerck  16 , Ahmed Debit  29 , Erwan Denis  1 , Christophe Destombe  13 , Erica Dinatale  12 , Simon Dittami  6 , Elodie Drula  11 , Sylvain Faugeron  30 , Jeanne Got  22 , Louis Graf  14 , Agnès Groisillier  17 , Marie-Laure Guillemin  31 , Lars Harms  32 , William John Hatchett  33 , Bernard Henrissat  34 , Galice Hoarau  33 , Chloé Jollivet  2 , Alexander Jueterbock  21 , Ehsan Kayal  7 , Andrew H Knoll  35 , Kazuhiro Kogame  36 , Arthur Le Bars  37 , Catherine Leblanc  6 , Line Le Gall  38 , Ronja Ley  20 , Xi Liu  7 , Steven T LoDuca  39 , Pascal Jean Lopez  40 , Philippe Lopez  38 , Eric Manirakiza  17 , Karine Massau  7 , Stéphane Mauger  13 , Laetitia Mest  4 , Gurvan Michel  2 , Catia Monteiro  6 , Chikako Nagasato  8 , Delphine Nègre  7 , Eric Pelletier  1 , Naomi Phillips  41 , Philippe Potin  6 , Stefan A Rensing  42 , Ellyn Rousselot  17 , Sylvie Rousvoal  6 , Declan Schroeder  43 , Delphine Scornet  4 , Anne Siegel  22 , Leila Tirichine  17 , Thierry Tonon  44 , Klaus Valentin  32 , Heroen Verbruggen  15 , Florian Weinberger  45 , Glen Wheeler  46 , Hiroshi Kawai  47 , Akira F Peters  48 , Hwan Su Yoon  49 , Cécile Hervé  50 , Naihao Ye  51 , Eric Bapteste  52 , Myriam Valero  53 , Gabriel V Markov  54 , Erwan Corre  55 , Susana M Coelho  56 , Patrick Wincker  57 , Jean-Marc Aury  58 , J Mark Cock  59
Affiliations

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

France Denoeud et al. Cell. .

Abstract

Brown seaweeds are keystone species of coastal ecosystems, often forming extensive underwater forests, and are under considerable threat from climate change. In this study, analysis of multiple genomes has provided insights across the entire evolutionary history of this lineage, from initial emergence, through later diversification of the brown algal orders, down to microevolutionary events at the genus level. Emergence of the brown algal lineage was associated with a marked gain of new orthologous gene families, enhanced protein domain rearrangement, increased horizontal gene transfer events, and the acquisition of novel signaling molecules and key metabolic pathways, the latter notably related to biosynthesis of the alginate-based extracellular matrix, and halogen and phlorotannin biosynthesis. We show that brown algal genome diversification is tightly linked to phenotypic divergence, including changes in life cycle strategy and zoid flagellar structure. The study also showed that integration of large viral genomes has had a significant impact on brown algal genome content throughout the emergence of the lineage.

Keywords: Ectocarpus; Phaeophyceae; Phaeovirus; brown algae; genome; intertidal and subtidal; multicellularity; stramenopile; viral genome insertions.

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Conflict of interest statement

Declaration of interests The authors declare no competing interests.

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