Dynamics of genomic innovation in the unicellular ancestry of animals

Abstract

Which genomic innovations underpinned the origin of multicellular animals is still an open debate. Here, we investigate this question by reconstructing the genome architecture and gene family diversity of ancestral premetazoans, aiming to date the emergence of animal-like traits. Our comparative analysis involves genomes from animals and their closest unicellular relatives (the Holozoa), including four new genomes: three Ichthyosporea and Corallochytrium limacisporum. Here, we show that the earliest animals were shaped by dynamic changes in genome architecture before the emergence of multicellularity: an early burst of gene diversity in the ancestor of Holozoa, enriched in transcription factors and cell adhesion machinery, was followed by multiple and differently-timed episodes of synteny disruption, intron gain and genome expansions. Thus, the foundations of animal genome architecture were laid before the origin of complex multicellularity – highlighting the necessity of a unicellular perspective to understand early animal evolution.

DOI: http://dx.doi.org/10.7554/eLife.26036.001

eLife digest

Hundreds of millions of years ago, some single-celled organisms gained the ability to work together and form multicellular organisms. This transition was a major step in evolution and took place at separate times in several parts of the tree of life, including in animals, plants, fungi and algae.

Animals are some of the most complex organisms on Earth. Their single-celled ancestors were also quite genetically complex themselves and their genomes (the complete set of the organism’s DNA) already contained many genes that now coordinate the activity of the cells in a multicellular organism.

The genome of an animal typically has certain features: it is large, diverse and contains many segments (called introns) that are not genes. By seeing if the single-celled relatives of animals share these traits, it is possible to learn more about when specific genetic features first evolved, and whether they are linked to the origin of animals.

Now, Grau-Bové et al. have studied the genomes of several of the animal kingdom’s closest single-celled relatives using a technique called whole genome sequencing. This revealed that there was a period of rapid genetic change in the single-celled ancestors of animals during which their genes became much more diverse. Another ‘explosion’ of diversity happened after animals had evolved. Furthermore, the overall amount of the genomic content inside cells and the number of introns found in the genome rapidly increased in separate, independent events in both animals and their single-celled ancestors.

Future research is needed to investigate whether other multicellular life forms – such as plants, fungi and algae – originated in the same way as animal life. Understanding how the genetic material of animals evolved also helps us to understand the genetic structures that affect our health. For example, genes that coordinate the behavior of cells (and so are important for multicellular organisms) also play a role in cancer, where cells break free of this regulation to divide uncontrollably.

DOI: http://dx.doi.org/10.7554/eLife.26036.002