FLO11 gene length and transcriptional level affect biofilm-forming ability of wild flor strains of Saccharomyces cerevisiae

Zara, Giacomo; Zara, Severino; Pinna, Claudia M.A.; Marceddu, Salvatore; Budroni, Marilena

doi:10.1099/mic.0.028738-0

Cited by 83 publications

(89 citation statements)

References 29 publications

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“…The region of the colony that invades the agar also displays variability; colonies in one strain background (⌺1278b) invade the agar in a single bubble-like structure at the center of the colony, whereas colonies in another strain background (SK1) invade the agar across a much larger region of the agar-colony interface (46). Similarly, S. cerevisiae strains used in wine production differ greatly in the sizes and structures of the flors that they form (73).…”

Section: (Ii) Community Diversity and Flocculin Diversitymentioning

confidence: 99%

Cell Signals, Cell Contacts, and the Organization of Yeast Communities

Honigberg

2011

Eukaryot Cell

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Even relatively simple species have evolved mechanisms to organize individual organisms into communities, such that the fitness of the group is greater than the fitness of isolated individuals. Within the fungal kingdom, the ability of many yeast species to organize into communities is crucial for their growth and survival, and this property has important impacts both on the economy and on human health. Over the last few years, studies of Saccharomyces cerevisiae have revealed several fundamental properties of yeast communities. First, strainto-strain variation in the structures of these groups is attributable in part to variability in the expression and functions of adhesin proteins. Second, the extracellular matrix surrounding these communities can protect them from environmental stress and may also be important in cell signaling. Finally, diffusible signals between cells contribute to community organization so that different regions of a community express different genes and adopt different cell fates. These findings provide an arena in which to view fundamental mechanisms by which contacts and signals between individual organisms allow them to assemble into functional communities.In many species, including our own, individual organisms assemble into communities to increase their overall fitness. Even in unicellular organisms like Saccharomyces cerevisiae, individual cells can organize themselves into a variety of types of multicellular aggregates. These biotic communities likely provide overall benefit to these yeast populations, for example by protecting organisms in the core of the structure from environmental stresses or by specializing functions to subpopulations within the community. Yeast communities also have broad relevance to human health and to industry. For example, biofilms formed by pathogenic yeasts on medical devices, such as catheters, are a major cause of the very high mortality rates of hospital-acquired fungal infections (reviewed in references 11, 43, and 44). Furthermore, surface film communities formed on food by spoilage yeasts may result in losses of billions of dollars annually (reviewed in reference 58). Yet the mechanisms underlying the organization of these communities are still poorly understood.In the first section of this paper, I review types of yeast communities, focusing on the model yeast Saccharomyces cerevisiae, and briefly discuss broader aspects of two processes fundamental to yeast communities: cell-cell signaling and cell adhesion. In the second section, I discuss four aspects of yeast community organization highlighted by recent publications: boundary formation, cell adhesion, the extracellular matrix (ECM), and diffusible cell-cell signals. Much of this recent progress has focused on the cytological structures of these communities and on the identification of several genetic pathways required for this organization. BACKGROUND. (I) THE MULTIFARIOUSYEAST COMMUNITY

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Section: (Ii) Community Diversity and Flocculin Diversitymentioning

confidence: 99%

Cell Signals, Cell Contacts, and the Organization of Yeast Communities

Honigberg

2011

Eukaryot Cell

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“…Flo proteins have similar three-domain structures: an N-terminal domain for carbohydrate binding, a central tandem repeat domain of varied lengths, and a C-terminal domain for cell wall attachment via a GPI anchor (83,84). Changes in FLO11, namely, a deletion in the promoter region which enhances the expression of FLO11 and an increase in the number of tandem repeat sequences in the central domain, caused these "flor yeast" cells to float and form buoyant biofilms, particularly in sherry wines (85,86). Regulation of FLO gene expression is remarkably complex and generates the basis for strain-to-strain differences that can cause problems on the industrial scale (87).…”

Section: Genetic Strain Improvement Of Lager Yeastmentioning

confidence: 99%

Lager Yeast Comes of Age

Wendland

2014

Eukaryot Cell

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Alcoholic fermentations have accompanied human civilizations throughout our history. Lager yeasts have a several-centurylong tradition of providing fresh beer with clean taste. The yeast strains used for lager beer fermentation have long been recognized as hybrids between two Saccharomyces species. We summarize the initial findings on this hybrid nature, the genomics/ transcriptomics of lager yeasts, and established targets of strain improvements. Next-generation sequencing has provided fast access to yeast genomes. Its use in population genomics has uncovered many more hybridization events within Saccharomyces species, so that lager yeast hybrids are no longer the exception from the rule. These findings have led us to propose network evolution within Saccharomyces species. This "web of life" recognizes the ability of closely related species to exchange DNA and thus drain from a combined gene pool rather than be limited to a gene pool restricted by speciation. Within the domesticated lager yeasts, two groups, the Saaz and Frohberg groups, can be distinguished based on fermentation characteristics. Recent evidence suggests that these groups share an evolutionary history. We thus propose to refer to the Saaz group as Saccharomyces carlsbergensis and to the Frohberg group as Saccharomyces pastorianus based on their distinct genomes. New insight into the hybrid nature of lager yeast will provide novel directions for future strain improvement.

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“…The loss or gain of FLO11D allele events can be explained by the dendrogram, which suggested that the FLO11D allele originated from a single origin and that sequence alteration in the third FLO11D allele occurred in Z3 after its acquisition. In S. cerevisiae, it has been reported that the length and type of repetitive units in the Flo11p coding repeats domain affect the Flo11p-associated functions, including cellular hydrophobicity (Fidalgo et al 2006;Fidalgo et al 2008;Zara et al 2009); however, the relationship between its functions and the copy number of the FLO gene itself has not been elucidated. To investigate this relationship, we measured the cellular hydrophobicity of FLO11D mutants in Z3.…”

Section: Flo11d Copy Number Variationsmentioning

confidence: 99%

“…The latter domain is also referred to as a domain with intragenic tandem repeats. The variation in the intragenic repeat number and/or the distribution of the different repetitive units provides a functional diversity of the cellsurface antigens that allows rapid adaptation to the environment (Verstrepen et al 2005;Fidalgo et al 2006Fidalgo et al , 2008Zara et al 2009). However, the relationship between adaptation and the copy number of the FLO gene itself, but not the number of the intragenic repeat units, has not been investigated.…”

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confidence: 99%

Adaptation of the Osmotolerant Yeast Zygosaccharomyces rouxii to an Osmotic Environment Through Copy Number Amplification of FLO11D

2013

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Copy number variations (CNVs) contribute to the adaptation process in two possible ways. First, they may have a direct role, in which a certain number of copies often provide a selective advantage. Second, CNVs can also indirectly contribute to adaptation because a higher copy number increases the so-called "mutational target size." In this study, we show that the copy number amplification of FLO11D in the osmotolerant yeast Zygosaccharomyces rouxii promotes its further adaptation to a florformative environment, such as osmostress static culture conditions. We demonstrate that a gene, which was identified as FLO11D, is responsible for flor formation and that its expression is induced by osmostress under glucose-free conditions, which confer unique characteristics to Z. rouxii, such as osmostress-dependent flor formation. This organism possesses zero to three copies of FLO11D, and it appears likely that the FLO11D copy number increased in a branch of the Z. rouxii tree. The cellular hydrophobicity correlates with the FLO11D copy number, and the strain with a higher copy number of FLO11D exhibits a fitness advantage compared to a reference strain under osmostress static culture conditions. Our data indicate that the FLO gene-related system in Z. rouxii has evolved remarkably to adapt to osmostress environments.A N organism adapts to adverse environments to survive and produce progeny. Adaptive evolution is the process through which a population becomes better suited to its environment via mutation, selection, and random drift (Bürger 2000;Cressman 2003;Ewens 2004;Nowak and Sigmund 2004). Types of mutations include nucleotide changes (Steiner et al. 2007;Barrick and Lenski 2009), transposition events (Wilke and Adams 1992;Aminetzach et al. 2005), and copy number variations (CNVs), including gene amplifications (duplication) and deletions (Brown et al. 1998;Perry et al. 2007;Gresham et al. 2010). CNVs can have a phenotypic impact and can consequently alter the fitness of an allele through the following mechanisms: (i) changing the coding sequence of a gene (Yamanaka et al. 2009;Schlattl et al. 2011), (ii) creating paralogs that can diverge from each other and take on new or specialized functions (neofunctionalization or subfunctionalization, respectively) (Ohno 1970;Innan and Kondrashov 2010), and (iii) altering the expression level of a gene (gene dosage effect) (Stranger et al. 2007;Yamanaka et al. 2009;Iskow et al. 2012). In humans, most CNVs overlapping genes are under purifying (negative) selection (Conrad et al. 2010), but a handful of CNVs are thought to be under positive selection (Cooper et al. 2007;Hurles et al. 2010;Iskow et al. 2012) such as AMY1 (Perry et al. 2007). In yeast, there are several examples of how the (increased) copy number can provide a direct selective advantage (Gresham et al. 2008;Voordeckers et al. 2012).In nature, budding yeast exhibits a number of adaptive responses, such as filamentation, invasive growth, flocculation, and biofilm formation, to overcome a deleterious enviro...

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FLO11 gene length and transcriptional level affect biofilm-forming ability of wild flor strains of Saccharomyces cerevisiae

Cited by 83 publications

References 29 publications

Cell Signals, Cell Contacts, and the Organization of Yeast Communities

Cell Signals, Cell Contacts, and the Organization of Yeast Communities

Lager Yeast Comes of Age

Adaptation of the Osmotolerant Yeast Zygosaccharomyces rouxii to an Osmotic Environment Through Copy Number Amplification of FLO11D

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