Genomic and ecological factors shaping specialism and generalism across an entire subphylum

Abstract

Organisms exhibit extensive breadth in the range of niches that they inhabit, from very narrow (specialists) to very broad (generalists). The two major paradigms proposed to explain niche breadth variation invoke either trade-offs between performance efficiency and breadth or the presence of specific intrinsic (e.g., genomic) and extrinsic (e.g., ecological) factors. To gain insights into niche breadth evolution, we assembled an unprecedented amount of genomic, metabolic, and ecological data from nearly all known known species of the Saccharomycotina, an ancient subphylum of fungi that exhibits extensive genomic, metabolic, and ecological diversity. We curated and sequenced the genomes of 1,154 yeast strains from 1,090 species, quantitatively measured the growth of 843 species in 24 carbon and nitrogen sources, and constructed an environmental ontology of 1,088 species. We classified yeasts into three niche breadth categories (specialists, standard, or generalists), and we tested for trade-offs between breadth and growth rate, measured coevolution between traits, and quantified the contributions of intrinsic and extrinsic factors to phenotype. Differences between generalists and specialists were not explained by trade-offs or by extrinsic factors. Instead, we found strong evidence that large interspecific differences in carbon breadth stem from intrinsic genomic differences in metabolic genes and linked generalism to variation in specific metabolic pathways. From this vast dataset, intrinsic genomic factors emerge as a primary driving force of microbial niche breadths.

Diverse signatures of convergent evolution in cacti-associated yeasts

“…(top) Genome-wide-based phylogeny of the subphylum Saccharomycotina 51 depicting the different types of ecological association of strictly cactophilic yeast species with the cacti environment: (necrotic) cacti tissues, which include both Opuntia spp. and columnar cacti, cacti flowers, and cacti-visiting insects.…”

“…Subtrees of three cactophilic clades: a. Tortispora , b. Starmera , and c. Pichia . Estimated times of origin, as determined in 51 , for the emergence of cactophily are represented for these three example clades.…”

“…Closely related non-cactophilic species were included according to the previously reported phylogeny in Opulente & LaBella, et. al., 2023 51 .…”

“…33 . For all these five datasets, closely related species belonging to each of the families were included based on the species phylogeny based on 51 (Fig. S3).…”

“…Benefiting from the wealth of genomic and phenotypic data available for nearly all known yeast species described in the subphylum Saccharomycotina 51 and cross-referencing with the ecological data available from the cactus-yeast-Drosophila system [35][36][37][52][53][54][55][56][57][58][59][60] , we employed a high throughput framework to detect signatures of convergent evolution in 17 independently evolved lineages of cactophilic yeasts. Using a machine learning algorithm, we uncovered distinctive phenotypic traits enriched among cacti-associated yeasts, including the ability to grow at high (≥ 37ºC) temperatures.…”