Phylogenomics reveals the evolutionary origins of lichenization in chlorophyte algae

Camille Puginier, Cyril Libourel, Juergen Otte, Pavel Skaloud, Mireille Haon, Sacha Grisel, Malte Petersen, Jean-Guy Berrin, Pierre-Marc Delaux (), Francesco Dal Grande () and Jean Keller ()
Additional contact information
Camille Puginier: INP
Cyril Libourel: INP
Juergen Otte: Senckenberg Biodiversity and Climate Research Centre (SBiK-F)
Pavel Skaloud: Charles University
Mireille Haon: UMR1163 Biodiversité et Biotechnologie Fongiques (BBF)
Sacha Grisel: UMR1163 Biodiversité et Biotechnologie Fongiques (BBF)
Malte Petersen: University of Bonn
Jean-Guy Berrin: UMR1163 Biodiversité et Biotechnologie Fongiques (BBF)
Pierre-Marc Delaux: INP
Francesco Dal Grande: Senckenberg Biodiversity and Climate Research Centre (SBiK-F)
Jean Keller: INP

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: Abstract Mutualistic symbioses have contributed to major transitions in the evolution of life. Here, we investigate the evolutionary history and the molecular innovations at the origin of lichens, which are a symbiosis established between fungi and green algae or cyanobacteria. We de novo sequence the genomes or transcriptomes of 12 lichen algal symbiont (LAS) and closely related non-symbiotic algae (NSA) to improve the genomic coverage of Chlorophyte algae. We then perform ancestral state reconstruction and comparative phylogenomics. We identify at least three independent gains of the ability to engage in the lichen symbiosis, one in Trebouxiophyceae and two in Ulvophyceae, confirming the convergent evolution of the lichen symbioses. A carbohydrate-active enzyme from the glycoside hydrolase 8 (GH8) family was identified as a top candidate for the molecular-mechanism underlying lichen symbiosis in Trebouxiophyceae. This GH8 was acquired in lichenizing Trebouxiophyceae by horizontal gene transfer, concomitantly with the ability to associate with lichens fungal symbionts (LFS) and is able to degrade polysaccharides found in the cell wall of LFS. These findings indicate that a combination of gene family expansion and horizontal gene transfer provided the basis for lichenization to evolve in chlorophyte algae.

Date: 2024
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DOI: 10.1038/s41467-024-48787-z

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