Phylogenomics reveals the evolutionary origins of lichenization in chlorophyte algae

Abstract

Mutualistic symbioses, such as lichens formed between fungi and green algae or cyanobacteria, have contributed to major transitions in the evolution of life and are at the center of extant ecosystems. However, our understanding of their evolution and function remains elusive in most cases. Here, we investigated the evolutionary history and the molecular innovations at the origin of lichens in green algae. We de novo sequenced the genomes or transcriptomes of 15 lichen-forming and closely-related non-lichen-forming algae and performed comparative phylogenomics with 22 genomes previously generated. We identified more than 350 functional categories significantly enriched in chlorophyte green algae able to form lichens. Among them, functions such as light perception or resistance to dehydration were shared between lichenizing and other terrestrial algae but lost in non-terrestrial ones, indicating that the ability to live in terrestrial habitats is a prerequisite for lichens to evolve. We detected lichen-specific expansions of glycosyl hydrolase gene families known to remodel cell walls, including the glycosyl hydrolase 8 which was acquired in lichenizing Trebouxiophyceae by horizontal gene transfer from bacteria, concomitantly with the ability to form lichens. Mining genome-wide orthogroups, we found additional evidence supporting at least two independent origins of lichen-forming ability in chlorophyte green algae. We conclude that the lichen-forming ability evolved multiple times in chlorophyte green algae, following a two-step mechanism which involves an ancestral adaptation to terrestrial lifestyle and molecular innovations to modify the partners cell walls.

Genomic analysis ofCoccomyxa viridis, a common low-abundance alga associated with lichen symbioses

“…Presence of InterProScan gene functional families across Trebouxiophyceae genomes. Here we show only functional families highlighted by Puginier et al [27] as potentially relevant to lichenization in green algae. The size of the bubbles represent the number of genes assigned to each family in a given genome.…”

“…Compared to other Coccomyxa species, C. viridis genome encoded comparable number of aquaporins, catalases, and domains similar to tryptophan-rich sensory protein/mitochondrial benzodiazepine receptor (TspO/MBR) (Fig. 6B) – groups of genes involved in stress response [27](Puginier et al 2022). Unlike other studied Coccomyxa species, C. viridis genome did not encode any proteins from the Glycoside Hydrolase (GH) 8 family (as confirmed by both IntrePro and CAZy annotations) – a diverse family of hydrolases that includes licheninases, cellulases, chitosanases, and others.…”

“…Comparative genomics analysis of C. viridis (highlighted in red) and other Trebouxiophyceae genomes. Information for the genomes other than C. viridis is taken from Puginier et al [27]. A.…”

Rhizocarpon geographicumlichen discloses a highly diversified microbiota carrying antibiotic resistance and Persistent Organic Pollutants tolerance

“…Despite the extraordinary ecological features harbored by lichens, studies on their ecology and evolution are still in their infancy and mostly addressed on the fungal partner. Nevertheless, a recent work from Keller et al ., 2022 [3] focuses on the impact of algae genomic diversity to explain the evolutionary trajectories of a wide range of terrestrial and aquatic lichens. A third partner, the lichen-associated-microbiota, not strictly associated with the symbiotic interaction, has been described as a key element of the lichen evolutionary history [2, 4–6].…”

Rhizocarpon geographicum Lichen Discloses a Highly Diversified Microbiota Carrying Antibiotic Resistance and Persistent Organic Pollutant Tolerance

“…Despite the extraordinary ecological features harbored by lichens, studies on their ecology and evolution are still in their infancy and mostly addressed to the fungal partner. Nevertheless, a recent work described the impact of algae genomic diversity on the evolutionary trajectories of a wide range of terrestrial and aquatic lichens [3]. A third partner-the lichenassociated microbiota-not strictly associated with the symbiotic interaction, has been described as a key element of the lichen evolutionary history [2,[4][5][6].…”