The origins of multicellularity: Correlation between morphological and genomic complexity in micrioorganisms

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2017-05

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Abstract

The earth's remarkable biodiversity is a testament to the evolution of organismal complexity. The fact that some kinds of complexity, including multicellularity, have arisen many times suggests that there are repeating selection pressure to become more complex, but our current knowledge of the mechanisms allowing for increased complexity is still far from complete. Most of the work that has been done focused on a few groups, primarily multicellular animals and plants. In this work, I study the evolution of phenotypic complexity across the entire tree of life. I use cell type number as a measure of phenotypic complexity. Unlike previous researchers, I focus mostly on unicellular taxa, both because they can exhibit great complexity on their own, and because they set the stage for the evolution of multicellularity. This means that cell type number is calculated over all life cycle stages of a species. As a result, a single celled organism can be "polycellular", in the sense of expressing multiple cell types throughout its lifecycle. I collected cell type data for 83 prokaryotes and 45 eukaryotes that met two criteria: First, there must be genome scale data available for genomic traits that might correlate with phenotypic complexity, such as coding gene number and number of transcription factors. Second, because ignoring phylogenetic relationships can easily lead to incorrect conclusions, I used only organisms for which good phylogenies exist. A natural expectation is that organismal complexity will correlate with genomic complexity, and some researchers have indeed reported a positive correlation between these two kinds of complexity. However, most of the work done so far did not take phylogeny into account, so any correlations observed may be artifacts. Using phylogenetic independent contrasts, I found that among prokaryotes (67 bacteria and 16 archaea), cell type number is indeed positively correlated with genome size, protein number, coding gene number and especially transcription factors. The correlation between cell type number and transcription factors was much stronger than for any of the other genomic variables. Thus, it seems that prokaryotes build their complex structures in the intuitively expected manner, with the help of more genes, proteins, and, especially, increasing capacity for complex gene regulation. Surprisingly, the eukaryote groups (45 species spread across the eukaryote tree) showed a completely different pattern. None of the genomic characters showed a statistically significant correlation with phenotypic complexity. Furthermore, the correlations between cell type number and both gene and protein number, though not significant, were actually negative. Eukaryotes therefore seem to achieve their organismal complexity not by simply accumulating genes or proteins, but in a novel way not seen in prokaryotes. Intrigued by this phenomenon, I went on to test the role of these genomic traits in the evolution of eukaryotic multicellularity. Firstly, I distinguished two different types of multicellularity, divisional and aggregative. Mapping these on to the eukaryotic tree of life, I identified 19 independent origins of multicellularity, 11 divisional and 8 aggregative. I then used the data for unicellular eukaryotes to estimate the character states (cell type number, gene number, etc.) for all internal (unicellular) branches of the eukaryote tree. I found that division-based multicellular groups consistently arose from simple ancestors, meaning that they arose from branches of fewer than average cell types, proteins and genes. Aggregation-based multicellularity, however, did not show this tendency. In summary, this study contributed to our understanding of organismal complexity and the origins of multicellularity at least in three ways. Firstly, it generated an annotated dataset for microbial cell type number spanning the tree of life. Secondly, this study revealed that prokaryotes and eukaryotes achieved their phenotypic complexity in fundamentally different ways: the former did it by recruiting more genes and proteins, especially those involved in gene regulation, while the latter did not follow this path. Thirdly, this study showed that the most complex modern multicellular organisms evolved from the simplest unicellular ancestors, and that this pattern holds for both morphological and genomic complexity.

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Cell type, Complexity, Multicellular, Evolution, Microorganisms

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