Metabolic and Chaperone Gene Loss Marks the Origin of Animals: Evidence for Hsp104 and Hsp78 Sharing Mitochondrial Clients

TL;DR

This study investigates gene loss during animal evolution, highlighting the loss of mitochondrial and cytosolic chaperones Hsp78 and Hsp104, and suggests their joint role in mitochondrial client protein management related to developmental changes.

Contribution

It identifies specific gene losses in animals, including ClpB disaggregases, and proposes a shared client relationship, linking gene loss to developmental and metabolic evolution.

Findings

Loss of mitochondrial and cytosolic chaperones Hsp78 and Hsp104 in animals.

Evidence for a shared client relationship between mitochondrial Fe/S homoaconitase and ClpB chaperones.

Gene loss correlates with metabolic shifts during animal evolution.

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.