Beatriz Baselga-Cervera

Climate change urges us to better understand and predict evolutionary responses to temperature shifts. Hybridization, by increasing genetic variation, can widen the range of adaptive responses and genetic mechanisms available to survive temperature changes. However, genomic data on the long-term effect of hybridization on adaptation is rare, and the molecular mechanisms usually remain unclear. Here, we hybridized two divergent species of Saccharomyces yeast. We experimentally evolved both hybrid and parental populations for 200 generations under hot (30 °C), cold (16 °C), and fluctuating (16–30 °C) temperature regimes. Most hybrids showed intermediate growth, but the large variance produced by hybridization also led to thermally transgressive hybrids with high performance. Across regimes, response to selection scaled negatively with ancestral growth, consistent with diminishing-returns epistasis. Analysis of genes with identified mutations revealed enrichment in multiple shared annotation terms between populations evolved in cold and fluctuating environments, such as cell wall functions. Evolved hybrid populations, across all evolution regimes, accumulated significantly more de novo copy number variants than both parental species, indicating extensive genome restructuring in hybrids. This increased structural variation may provide a substrate for selection and adaptive divergence among hybrid lineages. Our results suggest that hybridization can lead to increased growth, especially in hot and thermally unstable environments, by capitalizing on the genomic content inherited from one or the other parental species.

Phenotypic diversity in genetically homogenous populations has increasingly been recognized as potentially adaptive even under constant conditions. The origins of adaptive differentiation during major evolutionary transitions, such as the evolution of multicellularity and eusociality, are generally thought to arise from pre-existing stochastic and plastic phenotypic heterogeneity. Here, we characterize phenotypic diversity in isogenic populations of experimentally-evolved multicellular yeast, Saccharomyces cerevisiae . Our results show support for a bistable system maintained across different growth conditions, consisting of two distinct morphotypes: large multicellular clusters and smaller ancestral-like clusters consisting of one to a few cells. This bistable system arises as a pleiotropic consequence of a loss-of-function mutation in ACE2 that generates the selected large multicellular clusters concomitantly with the metabolically distinct alternative small clusters phenotype. Time-course assays and mathematical modeling indicate that small clusters phenotype arise directly from the growth of derived multicellular phenotypic individuals, consistent with stochastic phenotypic switching. Furthermore, we found significant differences in gene expression between the two different morphotypes, which cannot be readily explained by microenvironmental variation and instead suggest that the morphotypes occupy distinct growth states. Our study offers insights into how stochastic phenotypic switching can influence evolution by maintaining biological diversity in nascent multicellularity.

Detecting life has driven research and exploration for centuries, but recent attempts to compile and generate a framework that summarizes life features, aimed to develop strategies for life detection missions beyond planet Earth, have disregarded a key life feature: behavior. Yet, some behaviors such as biomineralization or motility have occasionally been proposed as biosignatures to detect life. Here, we capitalize on a specific taxis’ motility behavior, magnetotaxis, to experimentally provide insights in support of behavior as an unambiguous, sensitive biosignature, and magnetic forces as a prescreening option. Using a magnetotactic bacterial species, Magnetospirillum magneticum, we conducted a lab sensitivity experiment comparing PCR with the hanging drop behavioral assay, using a dilution series. The hanging drop behavioral assay visually shows the motility of MTB toward magnetic poles. Our findings reveal that the behavioral assay exhibits higher sensitivity in the detection of M. magneticum when compared to the established PCR protocol. While both methods present similar detection sensitivities at high concentrations, at ≥ 10^–7 fold dilutions, the behavioral method proved more sensitive. The behavioral method can detect bacteria even when samples are diluted at 10^–9. Comparable results were obtained with environmental samples from the Hula Valley. We propose behavioral cues as valuable biosignatures in the ongoing efforts of life detection in unexplored aquatic habitats on Earth and to stimulate and support discussions about how to detect extant life beyond Earth. Generic and robust behavioral assays can represent a methodological revolution.

Samarium (Sm) is a rare‐earth element recently included in the list of critical elements due to its vital role in emerging new technologies. With an increasing demand for Sm, microbial bioremediation may provide a cost‐effective and a more ecologically responsible alternative to remove and recover Sm. We capitalized on a previously selected Chlamydomonas reinhardtii strain tolerant to Sm (1.33 × 10⁻⁴ M) and acidic pH and carried out settling selection to increase the Sm uptake performance. We observed a rapid response to selection in terms of cellular phenotype. Cellular size decreased and circularity increased in a stepwise manner with every cycle of selection. After four cycles of selection, the derived CSm4 strain was significantly smaller and was capable of sequestrating 41% more Sm per cell (1.7 × 10⁻⁰⁵ ± 1.7 × 10⁻⁰⁶ ng) and twice as much Sm in terms of wet biomass (4.0 ± 0.4 mg Sm · g⁻¹) compared to the ancestral candidate strain. The majority (~70%) of the Sm was bioaccumulated intracellularly, near acidocalcisomes or autophagic vacuoles as per TEM‐EDX microanalyses. However, Sm analyses suggest a stronger response toward bioabsorption resulting from settling selection. Despite working with Sm and pH‐tolerant strains, we observed an effect on fitness and photosynthesis inhibition when the strains were grown with Sm. Our results clearly show that phenotypic selection, such as settling selection, can significantly enhance Sm uptake. Laboratory selection of microalgae for rare‐earth metal bioaccumulation and sorption can be a promising biotechnological approach.

Cyanobacteria morphology has apparently remained almost unchanged for billions of years, exhibiting remarkable evolutionary stasis. Cyanobacteria appear to have reached their maximum morphological complexity in terms of size, modes of multicellularity, and cellular types by ~2 Ga. This contrasts with the increased complexity observed in other multicellular lineages, such as plants. Using experimental evolution, we show that morphological diversity can rapidly evolve in a species of filamentous cyanobacteria. Since size has such significance with regard to organismal complexity, we subjected the heterocyst-forming cyanobacterium Trichornus variabilis (syn. Anabaena variabilis) to selection for larger size. We observed increases in size of more than 30-fold, relative to the ancestral population, after 45 cycles of selection. Two distinguishable nascent morphological elaborations were identified in all the selected populations: Tangle (long, tangled filaments) and Cluster (clusters of short filaments) morphology. Growth from single cells indicates heritability of the evolved Tangle and Cluster morphological phenotypes. Cyanobacteria evolutionary conservatism is ascribed to developmental constraints, slow evolution rates, or ecological flexibility. These results open opportunities to study possibilities and constraints for the evolution of higher integrated biological levels of organization within this lineage.

Determining how adaptive possibilities do or do not become evolutionary realities is central to understanding the tempo and mode of evolutionary change. Some of the simplest evolutionary landscapes arise from underdominance at a single locus where the fitness valley consists of only one less-fit genotype. Despite their potential for rapid evolutionary change, few such examples have been investigated. We capitalized on an experimental system in which a significant evolutionary shift, the transition from uni-to-multicellularity, was observed in asexual diploid populations ofSaccharomyces cerevisiaeexperimentally selected for increased settling rates. The multicellular phenotype results from recessive single-locus mutations that undergo loss-of-heterozygosity (LOH) events. By reconstructing the necessary heterozygous intermediate steps, we found that the evolution of multicellularity involves a decrease in size during the first steps. Heterozygous genotypes are 20% smaller in size than genotypes with functional alleles. Nevertheless, populations of heterozygotes give rise to multicellular genotypes more readily than unicellular genotypes with two functional alleles, by rapid LOH events. LOH drives adaptation that may enable rapid evolution in diploid yeast. Together these results show discordance between the phenotypic and genotypic multicellular transition. The evolutionary path to multicellularity, and the adaptive benefits of increased size, requires initial size reductions.

Electronic scraps (e‐scraps) represent an attractive raw material to mine demanded metals, as well as rare earth elements (REEs). A sequential microbial‐mediated process developed in two steps was examined to recover multiple elements. First, we made use of an acidophilic bacteria consortium, mainly composed of Acidiphilium multivorum and Leptospidillum ferriphilum, isolated from acid mine drainages. The consortium was inoculated in a dissolution of e‐scraps powder and cultured for 15 days. Forty‐five elements were analyzed in the liquid phase over time, including silver, gold, and 15 REEs. The bioleaching efficiencies of the consortium were >99% for Cu, Co, Al, and Zn, 53% for Cd, and around 10% for Cr and Li on Day 7. The second step consisted of a microalgae‐mediated uptake from e‐scraps leachate. The strains used were two acidophilic extremotolerant microalgae, Euglena sp. (EugVP) and Chlamydomonas sp. (ChlSG) strains, isolated from the same extreme environment. Up to 7.3, 4.1, 1.3, and 0.7 µg by wet biomass (WB) of Zn, Al, Cu, and Mn, respectively, were uptaken by ChlSG biomass in 12 days, presenting higher efficiency than EugVP. Concerning REEs, ChlSG biouptake 14.9, 20.3, 13.7, 8.3 ng of Gd, Pr, Ce, La per WB. Meanwhile, EugVP captured 1.1, 1.5, 1.4, and 7.5, respectively. This paper shows the potential of a microbial sequential process to revalorize e‐scraps and recover metals and REEs, harnessing extremotolerant microorganisms.

Anthropogenic extreme environments are emphasized as interesting sites for the study of evolutionary pathways, biodiversity, and extremophile bioprospection. Organisms that grow under these conditions are usually regarded as extremophiles; however, the extreme novelty of these environments may have favor adaptive radiations of facultative extremophiles. At the Iberian Peninsula, uranium mining operations have rendered highly polluted extreme environments in multiple locations. In this study, we examined the phytoplankton diversity, community structure, and possible determining factors in separate uranium mining-impacted waters. Some of these human-induced extreme environments may be able to sustain indigenous facultative extremophile phytoplankton species, as well as alleged obligate extremophiles. Therefore, we investigated the adaptation capacity of three laboratory strains, two Chlamydomonas reinhardtii and a Dictyosphaerium chlorelloides, to uranium-polluted waters. The biodiversity among the sampled waters was very low, and despite presenting unique taxonomic records, ecological patterns can be identified. The microalgae adaptation experiments indicated a gradient of ecological novelty and different phenomena of adaptation, from acclimation in some waters to non-adaptation in the harshest anthropogenic environment. Certainly, phytoplankton extremophiles might have been often overlooked, and the ability to flourish in extreme environments might be a functional feature in some neutrophilic species. Evolutionary biology and microbial biodiversity can benefit the study of recently evolved systems such as uranium-polluted waters. Moreover, anthropogenic extremophiles can be harnessed for industrial applications.