Spatially structured yeast communities: Understanding structure formation and regulation with omics tools

Abstract

Single-celled yeasts form spatially structured populations - colonies and biofilms, either alone (single-species biofilms) or in cooperation with other microorganisms (mixed-species biofilms). Within populations, yeast cells develop in a coordinated manner, interact with each other and differentiate into specialized cell subpopulations that can better adapt to changing conditions (e.g. by reprogramming metabolism during nutrient deficiency) or protect the overall population from external influences (e.g. via extracellular matrix). Various omics tools together with specialized techniques for separating differentiated cells and in situ microscopy have revealed important processes and cell interactions in these structures, which are summarized here. Nevertheless, current knowledge is still only a small part of the mosaic of complexity and diversity of the multicellular structures that yeasts form in different environments. Future challenges include the use of integrated multi-omics approaches and a greater emphasis on the analysis of differentiated cell subpopulations with specific functions.

Impaired amino acid uptake leads to global metabolic imbalance of Candida albicans biofilms

“…Embedded cells have limited access to preferential nutrients and oxygen due to the biofilm compartmentalization and structure. During biofilm maturation, specialized sub-populations differentiate to adapt to stress conditions like nutrient deficiency 31 , 32 . Amino acid homeostasis is critical for cellular growth and maintenance and this process includes three main mechanisms: amino acid uptake, de novo synthesis, and recycling by autophagy 33 .…”

A transient burst of mutations occurs during the normal development of yeast colonies

“…For example, the noise in gene expression of RAD27 or RAD52 can lead to heterogeneity in recombination rate in an isogenic population 57 . Furthermore, the complex reprogramming of the genetic networks and the formation of differentiated cell populations during the colony development lead to the formation of metabolically active and stress-resistant cells as well as starving and stress-sensitive cells [58][59][60][61][62][63][64][65] . The mutator subpopulations could also arise during the transition from one metabolism to another, indeed, spike of reactive oxygen species (ROS) had been observed during the change of carbon source or the passage to anoxia 66,67 .…”

Sticking to the Subject: Multifunctionality in Microbial Adhesins

“…Biofilms include at least four different morphologies: amorphous layers on surfaces; surface layers with perpendicular towers or mushroom-shaped constructs; well-organized mats of cells with regular wrinkles and crenellations; and pellicles, biofilms formed at air-water interfaces [7,11]. Within each biofilm morphology, individual cells have different specialized roles dependent on specific patterns of gene expression [12][13][14].…”

“…This binding leads to the modulation of host responses. In addition, biofilm adhesins mediate microbe-microbe associations, which induce changes in microbial cellular physiology [12,13,17]. This activity can be due to direct signaling between adhesins, or indirect due to adhesininduced long-term increases in population density [18,19].…”