Small, libertine and fit: did recombination and sex promote the evolutionary success of microalgae, from the origin of life to present days?

Microalgae are among the more ancient organisms on Earth. This group of photosynthetic unicells includes pro- and eukaryotes. The first “invented” photosynthesis, the second compartmentalized this metabolic process into plastids, derived from the intracellular domestication of cyanobacteria (endosymbiosis). Microalgae form large populations in all aquatic environments, play a key role in biogeochemical cycles and include several taxa capable to proliferate at extreme, quasi-primordial conditions. The large size and consequent fitness of microalgal populations are explained by their dominant clonal reproduction and the frequent genetic mutations during DNA duplications. Nonetheless, genetic and genomic observations suggest that genetic recombination frequently occurs in both prokaryotic and eukaryotic lineages. Moreover, many eukaryotic microalgae have life cycles including a sexual phase that can provide a regular genetic reassortment. In this contribute, we review studies on natural populations of aquatic and extremophilic microalgal taxa, both pro- and eukaryotes, whose evolutionary origins span 2-0.2  Billions years ago, namely the genera Planktothrix (freshwater cyanobacteria), Galdieria (extremophilic unicellular rhodophytes) and Pseudo-nitzschia (marine diatoms). The data gained so far suggest that genetic recombination and sex appear to play an important role in driving microevolution and promoting population fitness in each of the abovementioned microbial organisms. In a study focused on natural populations of Planktothrix spp. sampled in the subalpine lake district in North Italy, recombination signals were observed by analysing four molecular loci interspersed in the genome. Computational analyses suggest that recombination introduced genetic diversity at a rate more than double than mutations. Recombination provides natural populations of Planktothrix spp. wit h a background genetic diversity from which successful genotypes can eventually emerge and conquer new ecological niches, mimicking population developments typical of pathogenic (epidemic) bacteria. A study on Icelandic strains of Galdieria sulphuraria showed signals of recombination at the level of plastidial genome (i.e., the gene rbcL) in this putatively asexual microalga. A wide post-recombination diversification was inferred in G. sulphuraria populations, suggesting the occurrence of an intense spreading and a high fitness of recombinant lineages. Such recombinations without proper sex (i.e., nuclear recombination), could have been maintained even after primary endosymbiosis. The usefulness of this processes is that it probably promotes RuBisCo stability at extreme temperatures, as already demonstrated in other photosynthetic extremophiles (i.e., the cyanobacterium Synechococcus). Finally, molecular investigations on the diatom Pseudo -nitzschia multistriata reported signals of intra-specific recombination in natural populations (ribosomal ITS). This species showed a highly synchronized and strictly periodic sexual phase in nature, which makes it an obligate sexual organism, since geographically isolated populations would go eventually extinct in absence of sex. Nonetheless, species in the genus Pseudo-nitzschia also showed signals of recombination in the rbcL gene at both intra- and inter-specific level, suggesting that a putatively cyanobacteria-derived plastidial recombination could have been maintained in the course of the evolution of photosynthetic lineages, besides the emergence of proper sex. In presenting and discussing these cases, we aim to develop a conceptual scenario on the origin and benefit of recombination and sex in microlgae, an ecologically and evolutionary relevant group of organisms at global scale.