Cryptic surface-associated multicellularity emerges through cell adhesion and its regulation

The repeated evolution of multicellularity led to a wide diversity of organisms, many of which are sessile, including land plants, many fungi, and colonial animals. Sessile organisms adhere to a surface for most of their lives, where they grow and compete for space. Despite the prevalence of surface-associated multicellularity, little is known about its evolutionary origin. Here, we introduce a novel theoretical approach, based on spatial lineage tracking of cells, to study this origin. We show that multicellularity can rapidly evolve from two widespread cellular properties: cell adhesion and the regulatory control of adhesion. By evolving adhesion, cells attach to a surface, where they spontaneously give rise to primitive cell collectives that differ in size, life span, and mode of propagation. Selection in favor of large collectives increases the fraction of adhesive cells until a surface becomes fully occupied. Through kin recognition, collectives then evolve a central-peripheral polarity in cell adhesion that supports a division of labor between cells and profoundly impacts growth. Despite this spatial organization, nascent collectives remain cryptic, lack well-defined boundaries, and would require experimental lineage tracking technologies for their identification. Our results suggest that cryptic multicellularity could readily evolve and originate well before multicellular individuals become morphologically evident

The evolution of bacterial cell differentiation and multicellular organization

Een populatie van bacteriën wordt vaak gezien als een verzameling van cellen die min of meer hetzelfde simpele gedrag vertonen. Door een combinatie van experimenten en theorie laat ik zien dat deze kijk op bacteriën te simplistisch is. Bacteriële populaties zijn sterk gestructureerd. Cellen kunnen zich zowel in de ruimte als over tijd organiseren en daarbij verschillende celtypen tot expressie brengen. Deze celtypen gaan vaak complexe interacties met elkaar aan. In één van mijn experimenten laat ik bijvoorbeeld zien dat cellen een hoge mate van samenwerking kunnen bereiken. Dit is mogelijk doordat de groei dynamiek van de kolonie de samenwerkende cellen beschermt tegen eventuele valsspelers die misbruik maken van de samenwerking. Ik laat ook zien dat cellen taken verdelen. Sommige cellen worden bijvoorbeeld geholpen door andere cellen om over een grote afstand te migreren, hierdoor kunnen deze cellen ontsnappen aan een tekort aan voedsel. Bacteriële cellen zijn zelfs in staat een gokje te wagen. Wanneer het onduidelijk is wat er in de toekomst gaat gebeuren, kunnen bacteriën het risico spreiden door verschillende celtypen te vormen, ieder van deze celtypen is voorbereidt op een andere toekomst. Door middel van theoretische modellen bestudeer ik ook hoe de regulatie netwerken, die cel differentiatie reguleren, evolueren over tijd. Deze modellen tonen aan dat de regulatie netwerken in belangrijke mate bepalen hoe cellen evolueren. Onze kennis over deze regulatie netwerken is daarom van groot belang om te bepalen of en hoe organismen zich kunnen passen aan nieuwe condities

Microbial life cycles link global modularity in regulation to mosaic evolution

Microbes are exposed to changing environments, to which they can respond by adopting various lifestyles such as swimming, colony formation or dormancy. These lifestyles are often studied in isolation, thereby giving a fragmented view of the life cycle as a whole. Here, we study lifestyles in the context of this whole. We first use machine learning to reconstruct the expression changes underlying life cycle progression in the bacterium Bacillus subtilis, based on hundreds of previously acquired expression profiles. This yields a timeline that reveals the modular organization of the life cycle. By analysing over 380 Bacillales genomes, we then show that life cycle modularity gives rise to mosaic evolution in which life stages such as motility and sporulation are conserved and lost as discrete units. We postulate that this mosaic conservation pattern results from habitat changes that make these life stages obsolete or detrimental. Indeed, when evolving eight distinct Bacillales strains and species under laboratory conditions that favour colony growth, we observe rapid and parallel losses of the sporulation life stage across species, induced by mutations that affect the same global regulator. We conclude that a life cycle perspective is pivotal to understanding the causes and consequences of modularity in both regulation and evolution

The protective layer of biofilm:A repellent function for a new class of amphiphilic proteins

Bacteria can survive harsh conditions when growing in complex communities of cells known as biofilms. The matrix of the biofilm presents a scaffold where cells are attached to each other and to the surface. The biofilm matrix is also a protective barrier that confers tolerance against various antimicrobial agents. In this issue of Molecular Microbiology, Kobayashi and Iwano (2012) show that the liquid permeability of Bacillus subtilis biofilms is determined by a small secreted protein, i.e. BslA (formerly called YuaB). BslA is important for the proper development of biofilms, but unlike exopolysaccharide and TasA, is not directly involved in cell cluster formation, and is synthesized following the production of exopolysaccharide and amyloid fibres. The amphiphilic BslA protein forms a polymer in vitro and localizes in vivo to the surface of the biofilm. The microstructures of the biofilm wrinkles are reduced in the bslA mutant strain and the liquid repellency of the biofilm surface is diminished. Exogenously added BslA42181 protein complements the bslA mutation and restores not only water repellency, but also the formation of aerial structures. This study demonstrates that amphiphilic proteins have an important role in liquid repellency of biofilms and it suggests that these polymers contribute to antimicrobial resistance

On the origin of biological construction, with a focus on multicellularity

Biology is marked by a hierarchical organization: all life consists of cells; in some cases, these cells assemble into groups, such as endosymbionts or multicellular organisms; in turn, multicellular organisms sometimes assemble into yet other groups, such as primate societies or ant colonies. The construction of new organizational layers results from hierarchical evolutionary transitions, in which biological units (e.g., cells) form groups that evolve into new units of biological organization (e.g., multicellular organisms). Despite considerable advances, there is no bottom-up, dynamical account of how, starting from the solitary ancestor, the first groups originate and subsequently evolve the organizing principles that qualify them as new units. Guided by six central questions, we propose an integrative bottom-up approach for studying the dynamics underlying hierarchical evolutionary transitions, which builds on and synthesizes existing knowledge. This approach highlights the crucial role of the ecology and development of the solitary ancestor in the emergence and subsequent evolution of groups, and it stresses the paramount importance of the life cycle: only by evaluating groups in the context of their life cycle can we unravel the evolutionary trajectory of hierarchical transitions. These insights also provide a starting point for understanding the types of subsequent organizational complexity. The central research questions outlined here naturally link existing research programs on biological construction (e.g., on cooperation, multilevel selection, self-organization, and development) and thereby help integrate knowledge stemming from diverse fields of biology

Phenotypic Heterogeneity and the Evolution of Bacterial Life Cycles

Most bacteria live in colonies, where they often express different cell types. The ecological significance of these cell types and their evolutionary origin are often unknown. Here, we study the evolution of cell differentiation in the context of surface colonization. We particularly focus on the evolution of a ‘sticky’ cell type that is required for surface attachment, but is costly to express. The sticky cells not only facilitate their own attachment, but also that of non-sticky cells. Using individual-based simulations, we show that surface colonization rapidly evolves and in most cases leads to phenotypic heterogeneity, in which sticky and non-sticky cells occur side by side on the surface. In the presence of regulation, cell differentiation leads to a remarkable set of bacterial life cycles, in which cells alternate between living in the liquid and living on the surface. The dominant life stage is formed by the surface-attached colony that shows many complex features: colonies reproduce via fission and by producing migratory propagules; cells inside the colony divide labour; and colonies can produce filaments to facilitate expansion. Overall, our model illustrates how the evolution of an adhesive cell type goes hand in hand with the evolution of complex bacterial life cycles