The evolution of multicellularity : investigating first steps in unicellular cyanobacterial populations

Understanding the evolutionary transition to multicellularity is a key problem in evolutionary biology. Of particular importance are the ecological circumstances favoring a multicellular morphology. I here investigate the role of environmental factors in favoring a multicellular phenotype. With an approach of experimental evolution, different selective regimes are employed by exposing Cyanothece sp. ATCC 51142, a unicellular diazotrophic cyanobacteria species,to various ecological conditions (predation, salinity, population density, and nitrogen deprivation), to which end the emergence of novel undifferentiated and differentiated multicellular morphologies are expected. Consistent with expectation, predation selection was found to be a fast and efficient selective force for multicellular groups. I detected multicellular clusters of Cyanothece sp. after 24 hours of exposure to the protozoan predator Tetrahymena thermophila. However, persistent clusters were not observed, as before the end of the experiment, all bacterial cells were consumed by the predators. Population of cells grown under different salinity regimes showed a highly flexible morphology. When cultured in a reduced salinity environment, the whole unicellular population grew as filaments with cells not separating after cell division. Interestingly, this phenotype is transient and dependent on population density, with the whole culture reverting to the single-celled stage once a higher population density is reached. I provide indications that an excreted compound mediates the switch between the two morphologies in a manner very similar to quorum sensing. Although it is unlikely that, in this case, filament formation can be attributed to genetic changes, the phenotypic switch between the single-celled and the filamentous morphology constitutes an initially environmentally–dependent life cycle, which might represent an important step en route to multicellularity. When selected under conditions of nitrogen deprivation and continuous light, the cyanobacteria populations were “forced” to simultaneously accommodate the two incompatible processes of nitrogen fixation and photosynthesis. During a 56-week selection experiment a different multicellular morphology, a clumping phenotype imbedded in a layer that likely consists of extracellular polymeric substances (similar to a biofilm), was observed in 75% of the replicate populations. Simultaneously, the evolved replicate populations in this regime significantly improved their growth rates as compared to the ancestor and lines of the control treatments. This might have been due to heterogeneity in nitrogen fixation and photosynthesis, or in other words, a division of labour, which has been postulated to be a significant driver for the evolution of multicellularity. This study indicates the importance of ecological factors for the evolution of multicellularity, where various conditions may drive the formation of a range of undifferentiated and differentiated multicellular phenotypes. It also provides experimental indications for the theory that the division of labour between individuals may drive the emergence of multicellularity.


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