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Final Report Summary - EVOXY (Evolutionary origin of multicellularity and the oxygenation of Earth)


The history of Earth and life has been shaped by multiple evolutionary transitions, each broadening the confines on which selection may act. Among these, the origin of multicellularity represents one of the most formative of evolutionary transitions, requiring mechanisms for the coordination of cell division, growth, differentiation, adhesion and death.

However, multicellular organisms have evolved from unicellular ancestors various times. Yet, very little is known of the genetic basis for multicellularity among more than twenty independent multicellular pro- and eukaryote lineages. The prokaryotic fossil record indicates that the first transition to multicellularity in the history of life may be almost as old as life itself. Filamentous prokaryotes, potentially anoxic photosynthesisers, have been identified in 3.4 billion year old cherts in South Africa and Australia. Nevertheless, the taxonomic identity of these early fossils is unresolved. The earliest unequivocal filamentous (i.e. multicellular) fossils belong to cyanobacterial ancestors and date back more than 2.0 Ga. This study has focused on cyanobacteria, because: (i) Multicellular cyanobacteria seem to have evolved very early during Earth history; (ii) multicellularity evolved multiple times in this lineage; (iii) they exhibit differing grades of multicellular complexity; and (iv) the evolution of multicellularity in cyanobacteria coincides with, and has been considered causal to, the beginning of the Great Oxidation Event 2.4 billion years ago.

To investigate the evolutionary origins of multicellular cyanobacteria, this study has focused on two main objectives:
(objective 1) to identify the molecular basis underpinning the multiple independent transitions to multicellularity, and (objective 2) to characterise the implications of multicellularity on the evolution of cyanobacteria and consequently on Earth’s atmosphere and oceans.
To achieve those major objectives, the project is separated into three different parts: The basis for this study depicts, next generation sequencing and phylogenomic analyses (PHYLO), objective 1 that is exploring the evolution of the genetic bases underlying the origin of multicellularity (GENETIC) and objective 2 which will explore the cyanobacterial fossil record using state of the art imaging techniques (PALAEO).

Although parts of the project regarding the genetic machinery underlying bacterial multicellularity are still ongoing, several results could be established regarding the early evolution of cyanobacteria. Very little is known about the early evolution of this phylum and ongoing debates about cyanobacterial fossils, biomarkers and molecular clock analyses highlight the difficulties in this field of research. Phylogenetic analyses can provide promising glimpses into the early evolution of cyanobacteria. However, estimated divergence ages are often very uncertain, because of vague and insufficient tree-calibrations and novel approaches should seek to combine phylogenetic inferences with Precambrian microfossils, biomarkers and geochemical markers that inform upon the early evolution of cyanobacteria. Novel imaging techniques could improve taxonomic affiliation of many Precambrian microfossils. I have discussed various lines of evidence and the conclusions for early cyanobacterial evolution as well as the focus of possible future research in that field (Schirrmeister et al. 2016). Applying genome scale data and a re-evaluated the Precambrian fossil record I have reconstructed the evolutionary history of cyanobacteria using relaxed clock divergence time analyses. Phylogenomic reconstructions are based on 756 conserved gene sequences of 65 cyanobacterial taxa, of which eight genomes have been sequenced in this study. Character state reconstructions based on maximum likelihood and Bayesian phylogenetic inference confirm previous findings, of an ancient multicellular cyanobacterial lineage ancestral to the majority of modern cyanobacteria. Relaxed clock analyses provide firm support for an origin of cyanobacteria in the Archean and a transition to multicellularity before the GOE. It is likely that multicellularity had a greater impact on cyanobacterial fitness and thus abundance, than previously assumed. Multicellularity, as a major evolutionary innovation, forming a novel unit for selection to act upon, may have served to overcome evolutionary constraints and enabled diversification of the variety of morphotypes seen in cyanobacteria today (Schirrmeister et al. 2015). To further evaluate the Precambrian fossil record and potential presence of cyanobacteria, with special focus on multicellular taxa prior to the GOE, fossil deposits have been analysed applying novel imaging techniques (Synchrotron Radiation X-ray tomographic microscopy, SRXTM). Among others, one of the fossil richest early Proterozoic deposits, the 1.9 Ga Gunflint Chert was analysed and compared to 3dimensional SRXTM reconstructions of modern Lake Thetis microbialites. The Gunflint Chert harbors remnants of an impressively rich microbial community and could provide fundamental knowledge regarding bacterial diversity of an infant aerobic planet. To confirm identities of large fillamentous structures, results were compared to a previously reconstructed phylogenomic trees of modern eubacterial phyla, for which the evolution of multicellularity and divergence times have been estimated. Results strongly support the presence of Cyanobacteria, yet not of Proteobacteria. Previously suggested increasing morphological diversity of Cyanobacteria after the GOE, as an adaptive response to newly available oxygenated habitats, is supported by these results. The combination of SRXTM data and phylogenetic analyses is a powerful approach to further resolve the evolutionary history of ancient fossil deposits (in progress).

With this funded research project I have investigated fundamental questions regarding early evolutionary transitions in the history of Earth, investigating (i) how multicellularity evolved in early cyanobacteria, (ii) whether this could be linked to atmospheric oxygen accumulation on Earth at the end of the Archean Eon, and (iii) how this might have affected cyanobacterial diversity on a young Earth.

Major questions that will have been resolved include: Did multicellular cyanobacteria evolve before the GOE? Combining 3D imaging techniques, such as Synchrotron X-ray Tomographic Microscopy with phylogenomic reconstructions Precambrian microfossil community structures have been investigated and compared to modern analogs. Multicellular cyanobacteria seem to have been already present in deposits from the Archean, before the rapid increase of atmospheric oxygen. Furthermore, an increased diversity of cyanobacterial fossils can be observed in deposits following the GOE, such as the 1.9 Ga old Gunflint Chert. Ongoing research, with the aim to be published soon include, whether the genes responsible for multicellularity evolved in Archean cyanobacteria, or do different lineages of modern cyanobacteria show distinct genomic patterns?

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