Metabolic differentiation of surface and invasive cells of yeast colony biofilms revealed by gene expression profiling

Abstract

BackgroundYeast infections are often connected with formation of biofilms that are extremely difficult to eradicate. An excellent model system for deciphering multifactorial determinants of yeast biofilm development is the colony biofilm, composed of surface (“aerial”) and invasive (“root”) cells. While surface cells have been partially analyzed before, we know little about invasive root cells. In particular, information on the metabolic, chemical and morphogenetic properties of invasive versus surface cells is lacking. In this study, we used a new strategy to isolate invasive cells from agar and extracellular matrix, and employed it to perform genome wide expression profiling and biochemical analyses of surface and invasive cells.ResultsRNA sequencing revealed expression differences in 1245 genes with high statistical significance, indicating large genetically regulated metabolic differences between surface and invasive cells. Functional annotation analyses implicated genes involved in stress defense, peroxisomal fatty acid β-oxidation, autophagy, protein degradation, storage compound metabolism and meiosis as being important in surface cells. In contrast, numerous genes with functions in nutrient transport and diverse synthetic metabolic reactions, including genes involved in ribosome biogenesis, biosynthesis and translation, were found to be important in invasive cells. Variation in gene expression correlated significantly with cell-type specific processes such as autophagy and storage compound accumulation as identified by microscopic and biochemical analyses. Expression profiling also provided indications of cell-specific regulations. Subsequent knockout strain analyses identified Gip2p, a regulatory subunit of type 1 protein phosphatase Glc7p, to be essential for glycogen accumulation in surface cells.ConclusionsThis is the first study reporting genome wide differences between surface and invasive cells of yeast colony biofilms. New findings show that surface and invasive cells display very different physiology, adapting to different conditions in different colony areas and contributing to development and survival of the colony biofilm as a whole. Notably, surface and invasive cells of colony biofilms differ significantly from upper and lower cells of smooth colonies adapted to plentiful laboratory conditions.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-4214-4) contains supplementary material, which is available to authorized users.

Transcriptome Profile of Yeast Strain Used for Biological Wine Aging Revealed Dynamic Changes of Gene Expression in Course of Flor Development

“…The difference of oxygen and nutrient availability, ethanol and acetaldehyde concentrations at the airbiofilm and biofilm-liquid interface may induce formation of various cell types that differ in cell metabolism etc. Such variation may lead to ultimate changes in gene expression as shown for yeast subpopulation within colonies grown on solid surfaces (Maršíková et al, 2017). Thus, whole-velum transcriptome data may in fact represent a superposition of transcriptomes of various cell subpopulations, differing in metabolic and physiological microenvironment.…”

Long Noncoding RNAs in Yeast Cells and Differentiated Subpopulations of Yeast Colonies and Biofilms

“…RNA-seq provided a detailed transcriptomic view of six cell subpopulations present in smooth BY4742 colonies grown on complete respiratory medium [ 17 ]: cells from upper, margin, and lower parts of colonies in two developmental phases (late acidic 6-day-old and alkali-phase 15-day-old). In parallel experiments, two subpopulations (a surface “aerial” cell subpopulation and a subpopulation of invasive “root” cells growing within the agar) from structured colony biofilms grown on the same medium were also studied [ 16 ] ( Figure 1 ). Every gene located within 1.5 kB of (or antisense-overlapping) each lncRNA was identified to produce a list of lncRNA/gene pairs in any of the 5 different orientations ( Figure 2(a) ) considered.…”

“…Every gene located within 1.5 kB of (or antisense-overlapping) each lncRNA was identified to produce a list of lncRNA/gene pairs in any of the 5 different orientations ( Figure 2(a) ) considered. Previous expression profiling of subpopulations of smooth colonies and colony biofilms identified some metabolic similarities but even more differences [ 16 , 17 ]. Whereas some of the expression differences in individual genes may be caused by the fact that laboratory and wild strains forming smooth colonies and colony biofilms, respectively, are not isogenic, most of the differences are in agreement with the different lifestyles of yeast populations in smooth colonies (formed by either laboratory strains or domesticated wild strains) versus colony biofilms [ 1 , 5 ].…”

“…Here, we present a mini review of yeast lncRNAs and their previously described roles in regulating gene expression under various circumstances. In the second part of the review, we focus in more detail on lncRNAs that we have recently identified in differentiated subpopulations of cells from two distinct types of yeast populations [ 16 , 17 ], each of which uses unique strategies to cope with stress and ensure longevity of the population as a whole. These are complex colony biofilms formed by wild strains of Saccharomyces cerevisiae [ 18 ] and smooth colonies of S. cerevisiae laboratory strains [ 19 ] ( Figure 1 ).…”

Influence of mitochondrial DNA loss on the development of complex structured colonies of SK1 strains of yeast Saccharomyces cerevisiae

“…Стан мітохондрій у дріжджових клітинах відіграє важливу роль у багатьох процесах регуляції клітинних функцій, зокрема таких, як відповідь на умови навколишнього середовища або на сигнальні молекули, які надходять від інших клітин у популяції [5,6]. Завдяки здатності реагувати на такі сигнали дріжджова клітинна популяція здатна утворювати складні організовані співтовариства: біоплівки на напіврідких середовищах або складні колонії на щільних поживних середовищах [7][8][9][10][11].…”