Multicellular development in a choanoflagellate

Fairclough, Stephen R.; Dayel, Mark J.; King, Nicole

doi:10.1016/j.cub.2010.09.014

Cited by 154 publications

(175 citation statements)

References 9 publications

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“…Aggregation through floc-type adhesion was not observed in any of our experiments, possibly because this method of growth is prone to within-group conflict (25). Choanoflagellates, the closest unicellular ancestor to animals, can form multicellular colonies through postdivision adhesion (34), raising the possibility that a similar step was instrumental in the evolution of animal multicellularity. We observed adaptation of multicellular traits, indicating a shift in selection from individual cells to multicellular individuals.…”

Section: Discussionmentioning

confidence: 88%

Experimental evolution of multicellularity

Ratcliff

Denison²,

Borrello³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

473

619

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Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes.T he evolution of multicellularity was transformative for life on earth (1). In addition to larger size, multicellularity increased biological complexity through the formation of new biological structures. For example, multicellular organisms have evolved sophisticated, higher-level functionality via cooperation among component cells with complementary behaviors (2, 3). However, dissolution and death of multicellular individuals occurs when cooperation breaks down, cancer being a prime example (4). There are multiple mechanisms to help ensure cooperation of component cells in most extant multicellular species (5-8), but the origin and the maintenance of multicellularity are two distinct evolutionary problems. Component cells in a nascent multicellular organism would appear to have frequent opportunities to pursue noncooperative reproductive strategies at a cost to the reproduction of the multicellular individual. How, then, does the transition to multicellularity occur?Understanding the evolution of complex multicellular individuals from unicellular ancestors has been extremely challenging, largely because the first steps in this process occurred in the deep past (>200 million years ago) (9, 10). As a result, transitional forms have been lost to extinction, and little is known about the physiology, ecology, and evolutionary processes of incipient multicellularity (11). Nonetheless, several key steps have been identified for this transition. Because multicellular organisms are composed of multiple cells, the first step in this transition was likely the evolution of genotypes that form simple cellular clusters (1, 3, 12-16). It is not known whether this occurs more readily through aggregation of genetically distinct cells, as in biofilms, or by mother-daughter cell adhesion after division. Once simple clusters have evolved, selection among multicelled clusters must predominate over selection among single cells within clusters (1,15,17,18). T...

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Section: Discussionmentioning

confidence: 88%

Experimental evolution of multicellularity

Ratcliff

Denison²,

Borrello³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

473

619

View full text Add to dashboard Cite

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“…1). The orientation of the nascently divided cells around a central focus, the production of extracellular matrix, and the activity of a C-type lectin called Rosetteless, ultimately result in the formation of spherical, multicellular rosettes (30)(31)(32). Rosettes resemble morula-stage embryos, and the transition to multicellularity in S. rosetta evokes ancestral events that spawned the first animals (26, 27, 33).…”

mentioning

confidence: 99%

Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates

Woznica

Cantley

Beemelmanns

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

125

133

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In choanoflagellates, the closest living relatives of animals, multicellular rosette development is regulated by environmental bacteria. The simplicity of this evolutionarily relevant interaction provides an opportunity to identify the molecules and regulatory logic underpinning bacterial regulation of development. We find that the rosette-inducing bacterium Algoriphagus machipongonensis produces three structurally divergent classes of bioactive lipids that, together, activate, enhance, and inhibit rosette development in the choanoflagellate Salpingoeca rosetta. One class of molecules, the lysophosphatidylethanolamines (LPEs), elicits no response on its own but synergizes with activating sulfonolipid rosette-inducing factors (RIFs) to recapitulate the full bioactivity of live Algoriphagus. LPEs, although ubiquitous in bacteria and eukaryotes, have not previously been implicated in the regulation of a host-microbe interaction. This study reveals that multiple bacterially produced lipids converge to activate, enhance, and inhibit multicellular development in a choanoflagellate.choanoflagellates | bacteria | host-microbe | sulfonolipid | multicellularity

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confidence: 99%

Cellular packing, mechanical stress and the evolution of multicellularity

et al. 2017

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The evolution of multicellularity set the stage for sustained increases in organismal complexity [1][2][3][4][5] . However, a fundamental aspect of this transition remains largely unknown: how do simple clusters of cells evolve increased size when confronted by forces capable of breaking intracellular bonds? Here we show that multicellular snowflake yeast clusters 6-8 fracture due to crowding-induced mechanical stress. Over seven weeks (~291 generations) of daily selection for large size, snowflake clusters evolve to increase their radius 1.7-fold by reducing the accumulation of internal stress. During this period, cells within the clusters evolve to be more elongated, concomitant with a decrease in the cellular volume fraction of the clusters. The associated increase in free space reduces the internal stress caused by cellular growth, thus delaying fracture and increasing cluster size. This work demonstrates how readily natural selection finds simple, physical solutions to spatial constraints that limit the evolution of group size-a fundamental step in the evolution of multicellularity.The first step in the transition to multicellularity-prior to the origin of cellular division of labour, genetically regulated development and complex multicellular forms-was the evolution of simple multicellular clusters [1][2][3][4][5] . Long before simple clusters of cells can evolve traits characteristic of complex multicellularity, they must contend with physical forces-both internal and external-that are capable of breaking cell-cell bonds and thus limit cluster size. This physical challenge is critical for several reasons. First, large size is a likely prerequisite to the evolution of complex multicellularity 2,3 . Second, these forces act on long length scales that were probably irrelevant to a single-cell ancestor, and are thus evolutionarily novel. Finally, it is unclear how simple multicellular clusters that do not yet possess genetically regulated developmental systems can evolve novel multicellular morphology.Direct experimental investigation of the early steps in the transition to multicellularity has been challenging, largely because these transitions occurred long ago, and the evolutionary path to multicellularity has been obscured by extinction in most extant lineages 9,10 . Recently, however, this constraint has been circumvented through experimental evolution of novel multicellular organisms [6][7][8]11 , genetic reconstruction of early events 12 and experiments comparing extant multicellular taxa with their unicellular relatives 13,14 . To examine the biophysical basis of the evolution of increased size in a nascent multicellular organism, we employed the tractable 'snowflake' yeast model system [6][7][8] . Multicellular snowflake clusters evolved from the unicellular baker's yeast Saccharomyces cerevisiae under daily selection for rapid settling speed in liquid media 6 . The resulting snowflake growth form is the consequence of a single mutation in the ACE2 gene . This mutation prevents cell separation after ...

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Multicellular development in a choanoflagellate

Cited by 154 publications

References 9 publications

Experimental evolution of multicellularity

Experimental evolution of multicellularity

Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates

Cellular packing, mechanical stress and the evolution of multicellularity

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