Selective drivers of simple multicellularity

Tong, Khim Leng; Bozdag, G. Ozan; Ratcliff, William C.

doi:10.1016/j.mib.2022.102141

Cited by 39 publications

(36 citation statements)

References 96 publications

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“…A round aggregate shape ensures maximum contact between cells within the group, reducing the chance of a cell disassociating and thus being vulnerable to predation. Other proposed selective pressures for multicellularity include selection for sedimentation rate ( Dudin et al, 2022 ; Tong et al, 2022 ) or selection for multicellular groups that can shield interior cells from external stresses ( Kuzdzal-Fick et al, 2019 ). By increasing the roundness of aggregates, coYki could potentially affect either of these phenotypes: the shape of particles affects sedimentation rate ( Yokojima et al, 2021 ), and a more round shape minimizes surface area, thus potentially resulting in more interior cells that are shielded from stress.…”

Section: Discussionmentioning

confidence: 99%

Genome editing in the unicellular holozoan Capsaspora owczarzaki suggests a premetazoan role for the Hippo pathway in multicellular morphogenesis

Phillips

Santos

Konchwala

et al. 2022

eLife

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Animal development is mediated by a surprisingly small set of canonical signaling pathways such as Wnt, Hedgehog, TGF-beta, Notch, and Hippo pathways. Although once thought to be present only in animals, recent genome sequencing has revealed components of these pathways in the closest unicellular relatives of animals. These findings raise questions about the ancestral functions of these developmental pathways and their potential role in the emergence of animal multicellularity. Here, we provide the first functional characterization of any of these developmental pathways in unicellular organisms by developing techniques for genetic manipulation in Capsaspora owczarzaki, a close unicellular relative of animals that displays aggregative multicellularity. We then use these tools to characterize the Capsaspora ortholog of the Hippo signaling nuclear effector YAP/TAZ/Yorkie (coYki), a key regulator of tissue size in animals. In contrast to what might be expected based on studies in animals, we show that coYki is dispensable for cell proliferation but regulates cytoskeletal dynamics and the three-dimensional (3D) shape of multicellular structures. We further demonstrate that the cytoskeletal abnormalities of individual coYki mutant cells underlie the abnormal 3D shape of coYki mutant aggregates. Taken together, these findings implicate an ancestral role for the Hippo pathway in cytoskeletal dynamics and multicellular morphogenesis predating the origin of animal multicellularity, which was co-opted during evolution to regulate cell proliferation.

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Section: Discussionmentioning

confidence: 99%

Genome editing in the unicellular holozoan Capsaspora owczarzaki suggests a premetazoan role for the Hippo pathway in multicellular morphogenesis

Phillips

Santos

Konchwala

et al. 2022

eLife

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“…More broadly, given our finding of a morphodynamic instability that emerges generically from the coupling between diffusion and uptake of essential substrates for cellular growth in 3D, we expect that similar behavior could arise in other growing systems, with possible implications for the evolution of form and function [50,55,[140][141][142]. Indeed, similar 3D patterns of rough growth have been observed in other living systems, namely in multicellular clusters of Saccharomyces cerevisiae, usually referred to as 'snowflake yeast clusters', or in aggregation clusters of the green alga Volvox carteri.…”

Section: Substrate Concentration Cinmentioning

confidence: 94%

Roughening instability of growing 3D bacterial colonies

Martínez-Calvo

Bhattacharjee

Bay

et al. 2022

Preprint

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How do growing bacterial colonies get their shapes? While colony morphogenesis is well-studied in 2D, many bacteria grow as large colonies in 3D environments, such as gels and tissues in the body, or soils, sediments, and subsurface porous media. Here, we describe a morphological instability exhibited by large colonies of bacteria growing in 3D. Using experiments in transparent 3D granular hydrogel matrices, we show that dense colonies of four different species of bacteria—Escherichia coli, Vibrio cholerae, Pseudomonas aeruginosa, and Komagataeibacter sucrofermentans—generically roughen as they consume nutrients and grow beyond a critical size, eventually adopting a characteristic branched, broccoli-like, self-affine morphology independent of variations in the cell type and environmental conditions. This behavior reflects a key difference between 2D and 3D colonies: while a 2D colony may access the nutrients needed for growth from the third dimension, a 3D colony inevitably becomes nutrient-limited in its interior, driving a transition to rough growth at its surface. We elucidate the onset of roughening using linear stability analysis and numerical simulations of a continuum model that treats the colony as an ‘active fluid’ whose dynamics are driven by nutrient-dependent cellular growth. We find that when all dimensions of the growing colony substantially exceed the nutrient penetration length, nutrient-limited growth drives a 3D morphological instability that recapitulates essential features of the experimental observations. Our work thus provides a framework to predict and control the organization of growing colonies—as well as other forms of growing active matter, such as tumors and engineered living materials—in 3D environments.

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“…Clumping has been previously explored using mathematical models that consider multicellular clumps as 'public goods' [11] that could facilitate the emergence of MC traits. Here the clumps are explicitly defined as embodied systems and we refer to them as simple MC, for which efficient exploitation of patchy resources is a main driver [7]. Specifically, we have used a simple resource description as a circular area C whose linear size (the diameter ϕ) is used as a key parameter.…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, we can identify a diverse range of selective drivers that might have operated in the first steps towards MC, but also shown to be in action in artificially evolved systems [5,6]. They include mechanisms of predator avoidance (associated with larger assemblies), faster sedimentation, stress resistance or division of labour, among others [7]. The selective pressure is here associated with a specific, efficient functional trait.…”

Section: Introductionmentioning

confidence: 99%

Unicellular–multicellular evolutionary branching driven by resource limitations

Bonforti

Solé

2022

J. R. Soc. Interface.

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Multicellular life forms have evolved many times on our planet, suggesting that this is a common evolutionary innovation. Multiple advantages have been proposed for the emergence of multicellularity (MC). In this paper, we address the problem of how the first precondition for MC, namely ‘stay together’, might have occurred under spatially limited resources exploited by a population of unicellular agents. Using a minimal model of evolved cell–cell adhesion among growing and dividing cells that exploit a localized resource with a given size, we show that a transition occurs at a critical resource size separating a phase of evolved multicellular aggregates from a phase where unicellularity (UC) is favoured. The two phases are separated by an intermediate domain where both UC and MC can be selected by evolution. This model provides a minimal approach to the early stages that were required to transition from individuality to cohesive groups of cells associated with a physical cooperative effect: when resources are present only in a localized portion of the habitat, MC is a desirable property as it helps cells to keep close to the available local nutrients.

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Selective drivers of simple multicellularity

Cited by 39 publications

References 96 publications

Genome editing in the unicellular holozoan Capsaspora owczarzaki suggests a premetazoan role for the Hippo pathway in multicellular morphogenesis

Genome editing in the unicellular holozoan Capsaspora owczarzaki suggests a premetazoan role for the Hippo pathway in multicellular morphogenesis

Roughening instability of growing 3D bacterial colonies

Unicellular–multicellular evolutionary branching driven by resource limitations

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