BUSCADOR RECOLECTA

Identifying the ecological processes that underlie the distribution and abundance of species in microbial communities is a central issue in microbial ecology and evolution. Classical trade-off based niche theories of resource competition predict that co-occurrence in microbial communities is more likely when the residing species show trait divergence and complementary resource use. We tested the prediction that niche differentiation explained the co-occurrence of two yeast species (Metschnikowia reukaufii and M. gruessii) in floral nectar. Assessment of the phenotypic landscape showed that both species displayed a significantly different physiological profile. Comparison of utilization profiles in single versus mixed cultures indicated that these two species did not compete for most carbon and nitrogen sources. In mixed cultures, M. reukaufii grew better in sucrose solutions and in the presence of the antimicrobial compound digitonin than when grown as pure culture. M. gruessii, on the other hand, grew better in mixed cultures in glucose and fructose solutions. Overall, these results provide clear evidence that M. reukaufii and M. gruessii frequently co-occur in nectar and that they differ in their phenotypic response to variation in environmental conditions, suggesting that niche differentiation and resource partitioning are important mechanisms contributing to species co-occurrence in nectar yeast communities., Permission to work in the Sierra de Cazorla was granted by the Consejería de Medio Ambiente, Junta de Andalucía. Support for this work was provided by grants from the European Union program FP7 PEOPLE‐2012‐IEF (grant 327635) to MIP and ERC starting grant 260601 – MYCASOR to HJ. MAL acknowledges funding by the Natural Sciences and Engineering Council of Canada.

Understanding the relationship between population genetic structure and phenotypic diversity is a fundamental question in evolutionary biology. Yeasts display wide genetic diversity and exhibit remarkably diverse heterotrophic metabolisms that allow a variety of niche occupations. However, little is known about how intra-species genetic population structure is related to trait diversity in yeasts. In this study, we investigated the link between intra-species genetic population structure and trait diversity in the floral nectar-inhabiting yeast Metschnikowia reukaufii (Ascomycota). A total of 73 strains obtained from 11 plant species were genotyped by whole genome sequencing, followed by single nucleotide polymorphism (SNP) calling, and phenotyped using a robot-assisted high-throughput screening platform. Analysis of the population structure estimated the number of ancestral populations to be K = 5, each one including strains from different locations and host plants, and 26% of strains showed significant genetic admixture (<80% ancestry from a single population). These mosaic strains were scattered throughout a maximum-likelihood phylogenetic tree built from SNP data, and differed widely in their ancestry. While yeast strains varied in nutrient assimilation and tolerance to inhibitors, trait differentiation among genetic lineages was in most cases negligible. Notably, outlier phenotypes largely corresponded to the mosaic strains, and removal of these from the data had a dramatic effect on the intra-species phylogenetic signal of studied phenotypes and patterns of trait evolution. Overall, these results suggest that genetic mosaicism broadens the phenotypic landscape explored by M. reukaufii and may allow adaptation to highly variable nectar environments., This work was supported by funding from the Strategic Science Investment Fund, New Zealand Ministry of Business, Innovation & Employment (to M.K.D.), the Center for Computational, Evolutionary and Human Genomics at Stanford University (to M.K.D.), the European Union program FP7 PEOPLE-2012-IEF (to M.I.P., grant no. 327635) and Fonds Wetenschappelijk Onderzoek (FWO) (to M.I.P. application no. 12A0716N). S.A.-P. acknowledges a ‘Ramón y Cajal’ contract funded by the Spanish Ministry of Science and Innovation [RYC 2018-023847-I]., Peer reviewed

Table S5.xlsx -- Pairwise correlations between phenotypic traits of Metschnikowia reukaufii.

Table S6.xlsx -- Detailed results obtained in tests of phylogenetic signal for different phenotypic traits and indices of overall performance of Metschnikowia reukaufii.

Table S7.xlsx -- Detailed model fitting results obtained for phenotypic traits and indices of overall performance of Metschnikowia reukaufii.

mronlyvcf-renamed.vcf -- High coverage SNPs obtained from whole genome mapping of 73 Metschnikowia reukaufii strains to diploid reference (mean coverage = 47.9×, range 23 – 116×).

MR_phenotypes.xlsx -- Phenotypic data obtained for 73 Metschnikowia reukaufii strains., Raw data and supplementary files for the manuscript "Genetic admixture increases phenotypic diversity in the nectar yeast Metschnikowia reukaufii"., European Commission: PHENOGENYEAST - Exploring the phenotypic landscape of nectar yeasts in relation to their genetic background (327635)., Peer reviewed