Fungal Host Affects Photosynthesis in a Lichen Holobiont.

Corals and lichens are iconic examples of photosynthetic holobionts, i.e., ecological and evolutionary units resulting from the tightly integrated association of algae and prokaryotic microbiota with animal or fungal hosts, respectively. While the role of the coral host in modulating photosynthesis has been clarified to a large extent in coral holobionts, the role of the fungal host in this regard is far less understood. Here, we address this question by taking advantage of the recent discovery of highly specific fungal-algal pairings corresponding to climatically adapted ecotypes of the lichen-forming genus Umbilicaria. Specifically, we compared chlorophyll a fluorescence kinetics among lichen thalli consisting of different fungal-algal combinations. We show that photosynthetic performance in these lichens is not only driven by algal genotype, but also by fungal host species identity and intra-host genotype. These findings shed new light on the closely intertwined physiological processes of fungal and algal partners in the lichen symbiosis. Indeed, the specific combinations of fungal and algal genotypes within a lichen individual-and the resulting combined functional phenotype-can be regarded as a response to the environment. Our findings suggest that characterizing the genetic composition of both eukaryotic partners is an important complimentary step to understand and predict the lichen holobiont's responses to environmental change.

Climate-specific biosynthetic gene clusters in populations of a lichen-forming fungus.

Natural products can contribute to abiotic stress tolerance in plants and fungi. We hypothesize that biosynthetic gene clusters (BGCs), the genomic elements that underlie natural product biosynthesis, display structured differences along elevation gradients. We analysed biosynthetic gene variation in natural populations of the lichen-forming fungus Umbilicaria pustulata. We collected a total of 600 individuals from the Mediterranean and cold-temperate climates. Population genomic analyses indicate that U. pustulata contains three clusters that are highly differentiated between the Mediterranean and cold-temperate populations. One entire cluster is exclusively present in cold-temperate populations, and a second cluster is putatively dysfunctional in all cold-temperate populations. In the third cluster variation is fixed in all cold-temperate populations due to hitchhiking. In these two clusters the presence of consistent allele frequency differences among replicate populations/gradients suggests that selection rather than drift is driving the pattern. We advocate that the landscape of fungal biosynthetic genes is shaped by both positive and hitchhiking selection. We demonstrate, for the first time, the presence of climate-associated BGCs and BGC variations in lichen-forming fungi. While the associated secondary metabolites of the candidate clusters are presently unknown, our study paves the way for targeted discovery of natural products with ecological significance.

Mapping Early Pleistocene environments and the availability of plant food as a potential driver of early Homo presence in the Guadix-Baza Basin (Spain).

The Guadix-Baza Basin, in SE Spain, harbors hominin fossils and lithic artifacts dated to ca. 1.4-1.3 Ma, representing the first hominin habitat in the Iberian Peninsula and possibly in Western Europe. Recent palynological studies have described a high diversity of plant taxa and biomes existing in the basin at the time of hominin presence. However, the relationship between these hominins and their environment has not been fully explored. Two novel methodologies are developed. The first method maps the distribution of the Early Pleistocene vegetation units based on paleobotanical and paleogeographic data. The second method assesses the availability of edible plant parts using a combination of Early Pleistocene and modern taxa lists. The resulting vegetation maps reveal a great diversity of vegetation types. During dry (glacial) periods, the vegetation of the basin was represented mostly by steppes, with the appearance of forested vegetation only in the mountainous regions. During humid (interglacial) periods, Mediterranean woodlands represented the dominant vegetation, accompanied by deciduous and conifer forests in the areas of higher altitude. The lake system present in the basin also allowed for the presence of marshland vegetation. The assessment of the availability of edible plant parts reveals that early Homo could have found a high number of resources in marshland and riparian environments throughout the year. Mediterranean woodlands and deciduous forests also provided numerous edible plant parts. During dry periods, the availability of plant resources decreased heavily, but the prevalence of marshland and riparian vegetation and of forested vegetation in the areas of higher altitude could have sustained hominin communities during harsher climatic periods. However, the disappearance of the lake system and an increase of aridity after the Mid-Pleistocene Transition and during the Middle Pleistocene probably led to an impoverishment of plant resources available to early Homo in the Guadix-Baza Basin.

Transposable Elements in the Genome of the Lichen-Forming Fungus Umbilicaria pustulata and Their Distribution in Different Climate Zones along Elevation.

Transposable elements (TEs) are an important source of genome plasticity across the tree of life. Drift and natural selection are important forces shaping TE distribution and accumulation. Fungi, with their multifaceted phenotypic diversity and relatively small genome size, are ideal models to study the role of TEs in genome evolution and their impact on the host's ecological and life history traits. Here we present an account of all TEs found in a high-quality reference genome of the lichen-forming fungus Umbilicaria pustulata, a macrolichen species comprising two climatic ecotypes: Mediterranean and cold temperate. We trace the occurrence of the newly identified TEs in populations along three elevation gradients using a Pool-Seq approach to identify TE insertions of potential adaptive significance. We found that TEs cover 21.26% of the 32.9 Mbp genome, with LTR Gypsy and Copia clades being the most common TEs. We identified 28 insertions displaying consistent insertion frequency differences between the two host ecotypes across the elevation gradients. Most of the highly differentiated insertions were located near genes, indicating a putative function. This pioneering study of the content and climate niche-specific distribution of TEs in a lichen-forming fungus contributes to understanding the roles of TEs in fungal evolution.