Co-Flocculation of Yeast Species, a New Mechanism to Govern Population Dynamics in Microbial Ecosystems

Abstract

Flocculation has primarily been studied as an important technological property of Saccharomyces cerevisiae yeast strains in fermentation processes such as brewing and winemaking. These studies have led to the identification of a group of closely related genes, referred to as the FLO gene family, which controls the flocculation phenotype. All naturally occurring S. cerevisiae strains assessed thus far possess at least four independent copies of structurally similar FLO genes, namely FLO1, FLO5, FLO9 and FLO10. The genes appear to differ primarily by the degree of flocculation induced by their expression. However, the reason for the existence of a large family of very similar genes, all involved in the same phenotype, has remained unclear. In natural ecosystems, and in wine production, S. cerevisiae growth together and competes with a large number of other Saccharomyces and many more non-Saccharomyces yeast species. Our data show that many strains of such wine-related non-Saccharomyces species, some of which have recently attracted significant biotechnological interest as they contribute positively to fermentation and wine character, were able to flocculate efficiently. The data also show that both flocculent and non-flocculent S. cerevisiae strains formed mixed species flocs (a process hereafter referred to as co-flocculation) with some of these non-Saccharomyces yeasts. This ability of yeast strains to impact flocculation behaviour of other species in mixed inocula has not been described previously. Further investigation into the genetic regulation of co-flocculation revealed that different FLO genes impact differently on such adhesion phenotypes, favouring adhesion with some species while excluding other species from such mixed flocs. The data therefore strongly suggest that FLO genes govern the selective association of S. cerevisiae with specific species of non-Saccharomyces yeasts, and may therefore be drivers of ecosystem organisational patterns. Our data provide, for the first time, insights into the role of the FLO gene family beyond intraspecies cellular association, and suggest a wider evolutionary role for the FLO genes. Such a role would explain the evolutionary persistence of a large multigene family of genes with apparently similar function.

Genome Sequencing and Comparative Analysis of Three Hanseniaspora uvarum Indigenous Wine Strains Reveal Remarkable Biotechnological Potential

“…In particular, the significant difference with respect to terms related to flocculin repeats, found in lectin-like proteins, and flocculation (Flo11) observed in H2 and H4 strains is an intriguing and industrially relevant trait (Tables 5, 6). Flocculation, the process by which yeast cells spontaneously aggregate to form flocs with sediment in the culture, has been observed in different yeast species, including non-Saccharomyces isolates and H. uvarum (Rossouw et al, 2015). Beyond its physiological relevance as a protective mechanism to enhance the survival under environmental stresses (Marika et al, 1993), flocculation is a desirable technological feature allowing the separation of cells from media in fermentation processes such as brewing and winemaking (Pretorius, 2000;Soares, 2011), in particular sparkling wine obtained by the so-called Method Champenoise.…”

Application of Non-Saccharomyces Yeasts Isolated from Kombucha in the Production of Alcohol-Free Beer

“…The flocculation characteristics of yeast are strongly strain-dependent and largely defined by which members of the FLO genes, which encode for lectin proteins, are functional in each strain. Rossouw et al [36] showed that for 17 out of 18 investigated, non-Saccharomyces strains the flocculation phenotypes were calcium-dependent, thus indicating a FLO-dependency much like in Saccharomyces cerevisiae.…”

Ecological interactions are a primary driver of population dynamics in wine yeast microbiota during fermentation

“…Recent data suggest that such biotic impacts may be significant and that their role in defining population dynamics and fermentation outcomes may have been underestimated. A number of recent articles, for instance, suggest that physical contact between species has significant impact on the performance of these species 37,38 . The data by Rossouw et al 38 suggest that modifying the level of physical contact will lead to complex changes in population dynamics, either favouring or inhibiting certain species.…”