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Division of labour and the origin of multicellularity

Periodic Reporting for period 1 - MULTICELL (Division of labour and the origin of multicellularity)

Reporting period: 2015-07-01 to 2017-06-30

Understanding the evolution of multicellularity and cellular differentiation/ complexity is one of the greatest challenges in biology. The oldest transition, that of cyanobacteria, has happened more than 3 to 3.5 billion years ago. Of particular interest is to determine the evolutionary processes and mechanisms underlying the evolutionary transition from single cells to multicellular organisms.
This project uses cyanobacteria as a model system to determine whether division of labour may drive the transition to multicellularity by eliminating the trade-off between two incompatible processes that cannot be performed simultaneously in one cell. To this end, the overall objectives were to follow the evolution of multicellularity in real time using unicellular cyanobacteria exposed to different selection pressures, and to reconstruct the order of events that might have happened during the transition to multicellularity in the earliest epochs of life’s history.
Results from this work provide insights into the origin of multicellularity and the division of labour but also into the maintenance of multicellularity despite the threat of selfish, cancerous cell types.
The project adopted an interdisciplinary approach through combining experimental evolution with phylogenomics. More specifically, populations of unicellular cyanobacteria have been subjected to long-term experimental evolution under different regimes that favour either the specialization of cells into performing different physiologically incompatible processes within a multicellular group, or the formation of non-differentiated aggregates. While only the focal selection regime has resulted in the formation of multicellular groups, the underlying genotype and gene expression patterns will still need to be determined. The ultimate goal is it to establish the critical steps for the transition to multicellularity at the genome level.
The bioinformatics part of the project provides the first account ever that reconstruct a concrete evolutionary scenario for a transition to multicellularity that happened in cyanobacteria in the earliest epochs of life’s history. Our results show that the prime driver of multicellularity in cyanobacteria was the capability of nitrogen fixation, which was accompanied by the emergence of the filamentous morphology and a reproductive life cycle. This was followed by a range of niche expansions and interactions with other species, and the progression of multicellularity into higher complexity in the form of differentiated cells and patterned multicellularity.
Results from the bioinformatics part of the project have been summarized for publication, which is currently available as a preprint (Hammerschmidt et al 2019, bioRxiv 570788). They have also been disseminated at seminars, workshops, and conferences (total of 14), and communicated to the public (four talks and one poster).
Results from the bioinformatics part of the project present a major conceptual development in the field of phylogenetics and we expect it to open up new avenues of investigations on the evolution of organisms from all domains of life, as well as the development of novel approaches for the reconstruction of ancient evolutionary events.
The findings provide insight into the key events during the transition to multicellularity. Additionally, once the experimental evolution study is completed, it will also be the first study that directly relates a transition that was achieved under artificial conditions in the laboratory to one that actually happened more than 3 billion years ago.
Results from this work provide insights into the origin and maintenance of multicellularity, which is of importance when considering the threat of a dissolution of multicellularity as is happening during cancer.
Chronology of cyanobacterial multicellularity evolution as inferred from genomic data.