Slow algae, fast fungi: exceptionally high nucleotide substitution rate differences between lichenized fungi Omphalina and their symbiotic green algae Coccomyxa

Abstract

Omphalina basidiolichens are obligate mutualistic associations of a fungus of the genus Omphalina (the exhabitant) and a unicellular green alga of the genus Coccomyxa (the inhabitant). It has been suggested that symbiotic inhabitants have a lower rate of genetic change compared to exhabitants because the latter are more exposed to abiotic environmental variation and competition from other organisms. In order to test this hypothesis we compared substitution rates in the nuclear ribosomal internal transcribed spacer region (ITS1, 5.8S, ITS2) among fungal species with rates among their respective algal symbionts. To ensure valid comparisons, only taxon pairs (12) with a common evolutionary history were used. On average, substitution rates in the ITS1 portion of Omphalina pairs were 27.5 times higher than rates in the corresponding pairs of Coccomyxa since divergence from their respective ancestor at the base of the Omphalina/Coccomyxa lineage. Substitution rates in the 5.8S and the ITS2 portions were 2.4 and 18.0 times higher, respectively. The highest rate difference (43.0) was found in the ITS1 region. These are, to our knowledge, the highest differences of substitution rates reported for symbiotic organisms. We conclude that the Omphalina model system conforms to the proposed hypothesis of lower substitution rates in the inhabitant, but that the mode of transmission of the inhabitant (vertical versus horizontal) could be a prevailing factor in the regulation of unequal rates of nucleotide substitution between co-evolving symbionts. Our phylogenetic study of Coccomyxa revealed three main lineages within this genus, corresponding to free-living Coccomyxa, individuals isolated from basidiolichens Omphalina and Coccomyxa isolated from ascolichens belonging to the Peltigerales.