Poikilohydria, polyols, and homeoviscosity: lichen metabolomic remodeling across environmental gradients

Lichens are poikilohydric organisms whose biochemistry is strongly shaped by environmental conditions, yet their metabolome-wide adaptations across habitats remain unexplored.

Here, we established a continent-scale reference for the in-situ metabolome of the model lichen Ramalina farinacea, from thalli collected across six European regions during winter and summer, using untargeted GC-MS.

In total, 187 small molecules were annotated, including a compact core of 12 metabolites shared across all sites and seasons. Notably, the most abundant and core metabolites have recognized osmoprotective roles. The metabolome was primarily centered on polyols: arabitol was the predominant metabolite (49.9% of total relative abundance), followed by ribitol, sucrose, sorbitol, and mannitol. Multivariate analyses revealed season, region, and climate-similarity groups as the main drivers of metabolomic dissimilarity. GABA and mannose were consistent summer markers, while linoleic acid and arabitol emerged as the top regional and climatic markers, respectively. Glycerol levels increased towards colder regimes alongside monoglycerides and mono/polyunsaturated fatty acids, reflecting patterns consistent with homeoviscous adaptation. Hierarchical clustering resolved coordinated metabolite modules that distinguish cold-continental from warm-Mediterranean regimes while preserving region-specific chemical fingerprints. Pathway over-representation analyses converged on alanine, aspartate, and glutamate metabolism. This and other differential pathways indicated coupled adjustments in carbon handling and stress physiology.

This is the first continent-scale characterization of low-molecular-weight metabolomic variation in a lichen, revealing environmentally linked metabolic remodeling beyond the traditionally studied secondary metabolites and defining new chemoenvironmental markers as the metabolic basis of poikilohydric resilience in lichens.