Deciphering microbial spatial organization: insights from synthetic and engineered communities

Abstract

Microbial communities are frequently organized into complex spatial structures, shaped by intrinsic cellular traits, interactions between community members, initial growth condition or environmental factors. Understanding the mechanisms that drive these spatial patterns is essential for uncovering fundamental principles of microbial ecology and for developing applications. Using genetic engineering and synthetic microbial communities allows us to decipher how specific parameters influence spatial organization. In this review, we highlight recent studies that leverage synthetic microbial communities to deepen our understanding of microbial spatial ecology. We begin by exploring how initial conditions, such as cell density and relative species abundance, influence spatial organization. We then focus on studies that examine the role of individual microbial traits, such as cell shape and motility. Next, we discuss the impact of contact-dependent and long-range interactions, including metabolite exchange and toxin release. Furthermore, we highlight the influence of environmental factors on spatial dynamics. Finally, we address the current limitations of synthetic approaches and propose future directions to bridge the gap between engineered and natural systems.

Keywords: microbial communities; microbial interactions; spatial organization; synthetic communities.

Graphical Abstract

Figure 1

Effects of initial conditions on spatial patterns. (A) On agar plates, initial cell density influences spatial segregation, with higher starting densities leading to lower assortment levels between strains. Adapted with permission from [38]. (B) Similarly, in open trap microfluidics, initial cell density can influence spatial pattern formation, with higher starting densities leading to more intermixing. Adapted with permission from [39]. (C) Varying the initial ratio of cells in a producer and consumer community leads to distinct spatial patterns during expansion. Adapted with permission from [40]. (D) Short-range inhibition (SRI) causes strains to segregate more sharply at the expanding front, with higher initial ratios of one strain leading to a more pronounced separation between the two. Adapted with permission from [41].

Figure 2

Individual microbial properties can influence spatial self-arrangement. (A) Cell shape influences spatial patterning in E. coli colonies, with strains of different aspect ratios showing variations in boundary smoothness and mixing complexity, ranging from fractal-like intermixing between the two strains with rod-shape to smoother group boundaries in more round strains. Confocal images of edge sections of each colony are shown alongside orthogonal projections. Adapted with permission from [45]. (B) Motility differences among cells influence spatial patterning in dual-species colonies, as shown by varying degrees of strain overlap and area colonization. Adapted with permission from [46]. (C) The spatial pattern of a yeast colony is influenced by growth rate differences, with slower-growing cells forming distinct monoclonal sectors that expand at varying rates and persist at the colony front before they are eventually expelled. Adapted with permission from [47].

Figure 3

Interactions between cells affects spatial patterns. (A) Contact-based interactions. Contact-dependent inhibition shapes spatial patterns by promoting strain segregation and altering the relative abundance of strains at the expanding front [41]. EPS production, can create spatial structures by protecting both EPS-producing and non-producing strains from T6SS attacks, influencing survival and strain distribution in mixed colonies [53]. (B) Diffusion-based interactions. Long-range inhibition extends the spatial scale of interference, accelerating the exclusion of sensitive species compared to CDI [41]. Obligate mutualism alters spatial patterns by promoting the formation of smaller, intertwined patches in colonies [44, 54, 55].

Figure 4

Effects of the environment on spatial patterns. (A) The presence of physical objects on a surface creates local deformities along the expansion frontier, which influence spatial pattern formation by altering the densities and orientations of interspecific boundaries (adapted with permission from [77]). (B) Fluid flow in the environment influences spatial arrangement by transporting metabolic by-products between species, impacting biofilm formation and altering the distribution of populations within the community. Adapted with permission from [78]. (C) The concentration of exchanged molecules (i.e. amino acids) alters spatial organization during range expansions by modulating the interactions between mutualistic strains, with higher concentrations promoting competition and larger single-strain patches, while lower concentrations support stable mutualism and smaller patches. Adapted with permission from [54].