The natural biology of Saccharomyces cerevisiae, the best known unicellular model eukaryote, remains poorly documented and understood although recent progress has started to change this situation. Studies carried out recently in the Northern Hemisphere revealed the existence of wild populations associated with oak trees in North America, Asia, and in the Mediterranean region. However, in spite of these advances, the global distribution of natural populations of S. cerevisiae, especially in regions were oaks and other members of the Fagaceae are absent, is not well understood. Here we investigate the occurrence of S. cerevisiae in Brazil, a tropical region where oaks and other Fagaceae are absent. We report a candidate natural habitat of S. cerevisiae in South America and, using whole-genome data, we uncover new lineages that appear to have as closest relatives the wild populations found in North America and Japan. A population structure analysis revealed the penetration of the wine genotype into the wild Brazilian population, a first observation of the impact of domesticated microbe lineages on the genetic structure of wild populations. Unexpectedly, the Brazilian population shows conspicuous evidence of hybridization with an American population of Saccharomyces paradoxus. Introgressions from S. paradoxus were significantly enriched in genes encoding secondary active transmembrane transporters. We hypothesize that hybridization in tropical wild lineages may have facilitated the habitat transition accompanying the colonization of the tropical ecosystem.
Riparian plant litter is a major energy source for forested streams across the world and its decomposition has repercussions on nutrient cycling, food webs and ecosystem functioning. However, we know little about plant litter dynamics in tropical streams, even though the tropics occupy 40% of the Earth’s land surface. Here we investigated spatial and temporal (along a year cycle) patterns of litter inputs and storage in multiple streams of three tropical biomes in Brazil (Atlantic forest, Amazon forest and Cerrado savanna), predicting major differences among biomes in relation to temperature and precipitation regimes. Precipitation explained most of litter inputs and storage, which were generally higher in more humid biomes (litterfall: 384, 422 and 308 g m−2 y−1, storage: 55, 113 and 38 g m−2, on average in Atlantic forest, Amazon and Cerrado, respectively). Temporal dynamics varied across biomes in relation to precipitation and temperature, with uniform litter inputs but seasonal storage in Atlantic forest streams, seasonal inputs in Amazon and Cerrado streams, and aseasonal storage in Amazon streams. Our findings suggest that litter dynamics vary greatly within the tropics, but point to the major role of precipitation, which contrasts with the main influence of temperature in temperate areas.
The study of microbe domestication has witnessed major advances that contribute to a better understanding of the emergence of artificially selected phenotypes and set the foundations of their rational improvement for biotechnology. Several features make Saccharomyces cerevisiae an ideal model for such a study, notably the availability of a catalogue of signatures of artificial selection and the extensive knowledge available on its biological processes. Here, we investigate with population and comparative genomics a set of strains used for cachaça fermentation, a Brazilian beverage based on the fermentation of sugar cane juice. We ask if the selective pressures posed by this fermentation have given rise to a domesticated lineage distinct from the ones already known, like wine, beer, bread, and sake yeasts. Our results show that cachaça yeasts derive from wine yeasts that have undergone an additional round of domestication, which we define as secondary domestication. As a consequence, cachaça strains combine features of wine yeasts, such as the presence of genes relevant for wine fermentation and advantageous gene inactivations, with features of beer yeasts like resistance to the effects of inhibitory compounds present in molasses. For other markers like those related to sulfite resistance and biotin metabolism our analyses revealed distributions more complex than previously reported that support the secondary domestication hypothesis. We propose a multilayered microbe domestication model encompassing not only transitions from wild to primarily domesticated populations, as in the case of wine yeasts, but also secondary domestications like those of cachaça yeasts.
The succession of yeasts colonizing the fallen ripe amapa fruit, from Parahancornia amapa, was examined. The occupation of the substrate depended on both the competitive interactions of yeast species, such as the production of killer toxins, and the selective dispersion by the drosophilid guild of the amapa fruit. The yeast community associated with this Amazon fruit differed from those isolated from other fruits in the same forest. The physiological profile of these yeasts was mostly restricted to the assimilation of a few simple carbon sources, mainly L-sorbose, D-glycerol, DL-lactate, cellobiose, and salicin. Common fruit-associated yeasts of the genera Kloeckera and Hanseniaspora, Candida guilliermondii, and Candida krusei colonized fruits during the first three days after the fruit fell. These yeasts were dispersed and served as food for the invader Drosophila malerkotliana. The resident flies of the Drosophila willistoni group fed selectively on patches of yeasts colonizing fruits 3 to 10 days after the fruit fell. The killer toxin-producing yeasts Pichia kluyveri var. kluyveri and Candida fructus were probably involved in the exclusion of some species during the intermediate stages of fruit deterioration. An increase in pH, inhibiting toxin activity and the depletion of simple sugars, may have promoted an increase in yeast diversity in the later stages of decomposition. The yeast succession provided a patchy environment for the drosophilids sharing this ephemeral substrate.
The presence of killer and proteolytic yeasts was studied among 944 isolates representing 105 species from tropical yeast communities. We found 13 killer toxin producing species, with Pichia kluyveri being the most frequent. Other killer yeast isolates were Candida apis, Candida bombicola, Candida fructus, Candida krusei, Candida sorbosa, Hanseniaspora uvarum, Issatchenkia occidentalis, Kloeckera apis, Kluyveromyces marxianus, Pichia membranaefaciens, Pichia ohmeri-like, and Sporobolomyces roseus. The communities from which killer yeasts were isolated had strains sensitive to them, and there were interspecific and intraspecific differences in the spectra of their killer activities. Pichia kluyveri had the broadest spectra of activity against sensitive isolates, and it apparently produced different toxins. The coexistence of sensitive and killer yeasts using the same substrate suggests that there is spatial separation in microhabitats or temporal separation in different stages of successions. Basidiomycetous yeasts were more frequently proteolytic than ascomycetous yeasts. Extracellular proteases could be important for the yeasts to have access to more nitrogen nutrients and obtain a better balance with available carbon sources.
The feeding behavior of Drosophila serido on the yeast communities of necrotic stem tissue of Pilosocereus arrabidae were studied in a sand dune ecosystem of Rio de Janeiro, Brazil. The prevalence of cactophilic yeasts including Pichia barkeri, Candida sonorensis and Geotrichum sp. in the crops and external surfaces of D. serido reflected its association with the cactus habitat. The effective number of yeasts vectored on the surface of flies was higher than that in the crops. Also overlap between the yeasts from stems and from crops was partial suggesting selective feeding by the flies in the substrates visited. The females had a higher effective number of yeast species and a lower similarity than males with the yeast community of P. arrabidae. This was probably related to the search for oviposition sites by females. The presence of Pichia thermotolerans-like and Pichia amethionina var pachycereana in the flies, but not in P. arrabidae stems, indicated that D. serido was not limited to this cactus species. The larvae and adults lived in different patches with the adults feeding in patches with higher yeast species richness. The larvae had a narrower feeding niche and higher overlap with P. arrabidae, and preferred P. barkeri and Pichia cactophila as food. Adult flies fed on patches with the most frequent yeasts except for P. cactophila. Pichia caribaea was found in higher frequency in the adult crops than in the stems. Our data suggested that there was food selection and diet partitioning between adult and larval stages of D. serido.
The distribution and diversity of yeast species vectored by and from the crop of eight species groups of Drosophila is described for two rain forest sites and an urban wooded area in Rio de Janeiro, Brazil. The typical forest Drosophila groups guarani, tripunctata, and willistoni showed a higher diversity of yeasts than the cosmopolitan melanogaster species group, suggesting different strategies of utilization of substrates. Apiculate yeasts, including Kloeckera apis, Kloeckera javanica, and Kloeckera japonica, were the prevalent species. Geotrichum spp. and Candida citea were also frequent isolates in the forest sites. Similarities between the yeasts from the external surfaces and crops of Drosophila suggested that the feeding substrates were the main source of the yeasts vectored by these flies. Most of the yeasts were strong fermenters and assimilated few compounds, usually sucrose, cellobiose, and glycerol. This indicated a preference of the flies for food sources such as fruits. Some yeasts were primarily isolated from one group of Drosophila; for example, Kloeckera javanica from the melanogaster group, Debaryomyces vanrijiae var. yarrowii from the tripunctata group, and Kluyveromyces delphensis from the willistoni group. These associations and differences in the yeast communities among the fly groups suggested a differentiation of diets and specialization of the yeast-Drosophila association in the tropical forests.
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