Metabolic and chaperone gene loss marks the origin of animals: evidence for Hsp104 and Hsp78 chaperones sharing mitochondrial enzymes as clients

Albert J Erives; Jan S Fassler

doi:10.1371/journal.pone.0117192

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Metabolic and chaperone gene loss marks the origin of animals: evidence for Hsp104 and Hsp78 chaperones sharing mitochondrial enzymes as clients

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Metabolic and chaperone gene loss marks the origin of animals: evidence for Hsp104 and Hsp78 chaperones sharing mitochondrial enzymes as clients

Albert J Erives and Jan S Fassler

PloS one, Vol.10(2), pp.e0117192-e0117192

2015

DOI: 10.1371/journal.pone.0117192

PMID: 25710177

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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.

Mitochondria - enzymology

Promoter Regions, Genetic

Saccharomyces cerevisiae - genetics

Heat-Shock Proteins - metabolism

Aconitate Hydratase - classification

Endopeptidase Clp - genetics

Mitochondria - metabolism

Phylogeny

Saccharomyces cerevisiae Proteins - genetics

Saccharomyces cerevisiae - metabolism

Heat-Shock Proteins - genetics

Likelihood Functions

Animals

Endopeptidase Clp - classification

Bayes Theorem

Saccharomyces cerevisiae Proteins - metabolism

Aconitate Hydratase - genetics

Choanoflagellata - genetics

Mutation

Details

Title: Subtitle: Metabolic and chaperone gene loss marks the origin of animals: evidence for Hsp104 and Hsp78 chaperones sharing mitochondrial enzymes as clients
Creators: Albert J Erives - Department of Biology, University of Iowa, Iowa City, IA, 52242-1324, United States of America
Jan S Fassler - Department of Biology, University of Iowa, Iowa City, IA, 52242-1324, United States of America
Resource Type: Journal article
Publication Details: PloS one, Vol.10(2), pp.e0117192-e0117192
DOI: 10.1371/journal.pone.0117192
PMID: 25710177
NLM abbreviation: PLoS One
ISSN: 1932-6203
eISSN: 1932-6203
Publisher: United States
Language: English
Date published: 2015
Academic Unit: Biology
Record Identifier: 9983992064702771

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