Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world

Minglei Wang, Liudmila Sergeevna Mainzer, Derek Caetano-Anollés, Jay E. Mittenthal, Gustavo Caetano-Anolles

Research output: Contribution to journalArticle

Abstract

The repertoire of protein architectures in proteomes is evolutionarily conserved and capable of preserving an accurate record of genomic history. Here we use a census of protein architecture in 185 genomes that have been fully sequenced to generate genome-based phylogenies that describe the evolution of the protein world at fold (F) and fold superfamily (FSF) levels. The patterns of representation of F and FSF architectures over evolutionary history suggest three epochs in the evolution of the protein world: (1) architectural diversification, where members of an architecturally rich ancestral community diversified their protein repertoire; (2) superkingdom specification, where superkingdoms Archaea, Bacteria, and Eukarya were specified; and (3) organismal diversification, where F and FSF specific to relatively small sets of organisms appeared as the result of diversification of organismal lineages. Functional annotation of FSF along these architectural chronologies revealed patterns of discovery of biological function. Most importantly, the analysis identified an early and extensive differential loss of architectures occurring primarily in Archaea that segregates the archaeal lineage from the ancient community of organisms and establishes the first organismal divide. Reconstruction of phylogenomic trees of proteomes reflects the timeline of architectural diversification in the emerging lineages. Thus, Archaea undertook a minimalist strategy using only a small subset of the full architectural repertoire and then crystallized into a diversified superkingdom late in evolution. Our analysis also suggests a communal ancestor to all life that was molecularly complex and adopted genomic strategies currently present in Eukarya.

Original languageEnglish (US)
Pages (from-to)1572-1585
Number of pages14
JournalGenome Research
Volume17
Issue number11
DOIs
StatePublished - Nov 1 2007

Fingerprint

Proteome
Parturition
Archaea
Proteins
Eukaryota
History
Genome
Chronology
Censuses
Phylogeny
Bacteria

ASJC Scopus subject areas

  • Genetics

Cite this

Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world. / Wang, Minglei; Mainzer, Liudmila Sergeevna; Caetano-Anollés, Derek; Mittenthal, Jay E.; Caetano-Anolles, Gustavo.

In: Genome Research, Vol. 17, No. 11, 01.11.2007, p. 1572-1585.

Research output: Contribution to journalArticle

@article{e1a4bf33c3404e029a69de7e68331068,
title = "Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world",
abstract = "The repertoire of protein architectures in proteomes is evolutionarily conserved and capable of preserving an accurate record of genomic history. Here we use a census of protein architecture in 185 genomes that have been fully sequenced to generate genome-based phylogenies that describe the evolution of the protein world at fold (F) and fold superfamily (FSF) levels. The patterns of representation of F and FSF architectures over evolutionary history suggest three epochs in the evolution of the protein world: (1) architectural diversification, where members of an architecturally rich ancestral community diversified their protein repertoire; (2) superkingdom specification, where superkingdoms Archaea, Bacteria, and Eukarya were specified; and (3) organismal diversification, where F and FSF specific to relatively small sets of organisms appeared as the result of diversification of organismal lineages. Functional annotation of FSF along these architectural chronologies revealed patterns of discovery of biological function. Most importantly, the analysis identified an early and extensive differential loss of architectures occurring primarily in Archaea that segregates the archaeal lineage from the ancient community of organisms and establishes the first organismal divide. Reconstruction of phylogenomic trees of proteomes reflects the timeline of architectural diversification in the emerging lineages. Thus, Archaea undertook a minimalist strategy using only a small subset of the full architectural repertoire and then crystallized into a diversified superkingdom late in evolution. Our analysis also suggests a communal ancestor to all life that was molecularly complex and adopted genomic strategies currently present in Eukarya.",
author = "Minglei Wang and Mainzer, {Liudmila Sergeevna} and Derek Caetano-Anoll{\'e}s and Mittenthal, {Jay E.} and Gustavo Caetano-Anolles",
year = "2007",
month = "11",
day = "1",
doi = "10.1101/gr.6454307",
language = "English (US)",
volume = "17",
pages = "1572--1585",
journal = "Genome Research",
issn = "1088-9051",
publisher = "Cold Spring Harbor Laboratory Press",
number = "11",

}

TY - JOUR

T1 - Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world

AU - Wang, Minglei

AU - Mainzer, Liudmila Sergeevna

AU - Caetano-Anollés, Derek

AU - Mittenthal, Jay E.

AU - Caetano-Anolles, Gustavo

PY - 2007/11/1

Y1 - 2007/11/1

N2 - The repertoire of protein architectures in proteomes is evolutionarily conserved and capable of preserving an accurate record of genomic history. Here we use a census of protein architecture in 185 genomes that have been fully sequenced to generate genome-based phylogenies that describe the evolution of the protein world at fold (F) and fold superfamily (FSF) levels. The patterns of representation of F and FSF architectures over evolutionary history suggest three epochs in the evolution of the protein world: (1) architectural diversification, where members of an architecturally rich ancestral community diversified their protein repertoire; (2) superkingdom specification, where superkingdoms Archaea, Bacteria, and Eukarya were specified; and (3) organismal diversification, where F and FSF specific to relatively small sets of organisms appeared as the result of diversification of organismal lineages. Functional annotation of FSF along these architectural chronologies revealed patterns of discovery of biological function. Most importantly, the analysis identified an early and extensive differential loss of architectures occurring primarily in Archaea that segregates the archaeal lineage from the ancient community of organisms and establishes the first organismal divide. Reconstruction of phylogenomic trees of proteomes reflects the timeline of architectural diversification in the emerging lineages. Thus, Archaea undertook a minimalist strategy using only a small subset of the full architectural repertoire and then crystallized into a diversified superkingdom late in evolution. Our analysis also suggests a communal ancestor to all life that was molecularly complex and adopted genomic strategies currently present in Eukarya.

AB - The repertoire of protein architectures in proteomes is evolutionarily conserved and capable of preserving an accurate record of genomic history. Here we use a census of protein architecture in 185 genomes that have been fully sequenced to generate genome-based phylogenies that describe the evolution of the protein world at fold (F) and fold superfamily (FSF) levels. The patterns of representation of F and FSF architectures over evolutionary history suggest three epochs in the evolution of the protein world: (1) architectural diversification, where members of an architecturally rich ancestral community diversified their protein repertoire; (2) superkingdom specification, where superkingdoms Archaea, Bacteria, and Eukarya were specified; and (3) organismal diversification, where F and FSF specific to relatively small sets of organisms appeared as the result of diversification of organismal lineages. Functional annotation of FSF along these architectural chronologies revealed patterns of discovery of biological function. Most importantly, the analysis identified an early and extensive differential loss of architectures occurring primarily in Archaea that segregates the archaeal lineage from the ancient community of organisms and establishes the first organismal divide. Reconstruction of phylogenomic trees of proteomes reflects the timeline of architectural diversification in the emerging lineages. Thus, Archaea undertook a minimalist strategy using only a small subset of the full architectural repertoire and then crystallized into a diversified superkingdom late in evolution. Our analysis also suggests a communal ancestor to all life that was molecularly complex and adopted genomic strategies currently present in Eukarya.

UR - http://www.scopus.com/inward/record.url?scp=35948990789&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=35948990789&partnerID=8YFLogxK

U2 - 10.1101/gr.6454307

DO - 10.1101/gr.6454307

M3 - Article

C2 - 17908824

AN - SCOPUS:35948990789

VL - 17

SP - 1572

EP - 1585

JO - Genome Research

JF - Genome Research

SN - 1088-9051

IS - 11

ER -