Abstract
The evolution of animals involved acquisition of an emergent gene repertoire for gastrulation. Whether loss of genes also co-evolved with this developmental reprogramming has not yet been addressed. Here, we identify twenty-four genetic functions that are retained in fungi and choanoflagellates but undetectable in animals. These lost genes encode: (i) sixteen distinct biosynthetic functions; (ii) the two ancestral eukaryotic ClpB disaggregases, Hsp78 and Hsp104, which function in the mitochondria and cytosol, respectively; and (iii) six other assorted functions. We present computational and experimental data that are consistent with a joint function for the differentially localized ClpB disaggregases, and with the possibility of a shared client/chaperone relationship between the mitochondrial Fe/S homoaconitase encoded by the lost LYS4 gene and the two ClpBs. Our analyses lead to the hypothesis that the evolution of gastrulation-based multicellularity in animals led to efficient extraction of nutrients from dietary sources, loss of natural selection for maintenance of energetically expensive biosynthetic pathways, and subsequent loss of their attendant ClpB chaperones.
Highlights
By the time of the last common ancestor of animals, the uniquely animal process of gastrulation had evolved
For Dikarya fungi we worked with the ascomycetes, S. cerevisiae and Schizosaccharomyces pombe genomes; for the basidiomycetes, Cryptococcus neoformans and Puccinia graminis (Ensembl BioMart); and for chytridiomycetes, Batrachochytrium dendrobatidis (JGI)
We show for the first time that Hsp78 and Hsp104 (i) were both definitively lost in an ancestor of animals despite their presence in all non-animals; (ii) were uniquely co-regulated by a multimeric and ordered array of perfect binding sites for Heat Shock Factor 1 (Hsf1) in an ancestor of animals based on the shared presence and restricted use of this regulatory signature in fungal and choanoflagellate genomes; (iii) function together in thermotolerance (Fig. 5A); and (iv) make specific contacts with Lys4 and Lys20, two nuclear encoded, mitochondrial enzymes (Fig. 6A and 6B)
Summary
By the time of the last common ancestor of animals, the uniquely animal process of gastrulation had evolved. Many post-genomic studies have detailed the evolutionary expansion of eukaryotic transcription factor (TF) families and the emergence of new developmental genes during this major evolutionary transition [1,2,3,4,5]; these genes include those controlling the gastrulation program, which is shared from humans to sponges [6,7]. Identification of pre-metazoan gene losses may be important because they may indicate the context, origins, and constraints associated with new transcription programs. No study has yet focused on systematically identifying genes that are widely retained in the closest relatives of animals but undetectable in animals themselves.
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