Gene flow and biological conflict systems in the origin and evolution of eukaryotes

The endosymbiotic origin of eukaryotes brought together two disparate genomes in the cell. Additionally, eukaryotic natural history has included other endosymbiotic events, phagotrophic consumption of organisms, and intimate interactions with viruses and endoparasites. These phenomena facilitated la...

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Main Authors: L eAravind, Vivek eAnantharaman, Dapeng eZhang, Robson Francisco De Souza, Lakshminarayan M Iyer
Format: Article
Language:English
Published: Frontiers Media S.A. 2012-06-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fcimb.2012.00089/full
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author L eAravind
Vivek eAnantharaman
Dapeng eZhang
Robson Francisco De Souza
Lakshminarayan M Iyer
author_facet L eAravind
Vivek eAnantharaman
Dapeng eZhang
Robson Francisco De Souza
Lakshminarayan M Iyer
author_sort L eAravind
collection DOAJ
description The endosymbiotic origin of eukaryotes brought together two disparate genomes in the cell. Additionally, eukaryotic natural history has included other endosymbiotic events, phagotrophic consumption of organisms, and intimate interactions with viruses and endoparasites. These phenomena facilitated large-scale lateral gene transfer and biological conflicts. We synthesize information from nearly two decades of genomics to illustrate how the interplay between lateral gene transfer and biological conflicts has impacted the emergence of new adaptations in eukaryotes. Using apicomplexans as example, we illustrate how lateral transfer from animals has contributed to unique parasite-host interfaces comprised of adhesion- and O-linked glycosylation-related domains. Adaptations, emerging due to intense selection for diversity in the molecular participants in organismal and genomic conflicts, being dispersed by lateral transfer, were subsequently exapted for eukaryote-specific innovations. We illustrate this using examples relating to eukaryotic chromatin, RNAi and RNA-processing systems, signaling pathways, apoptosis and immunity. We highlight the major contributions from catalytic domains of bacterial toxin-systems to the origin of signaling enzymes (e.g. ADP-ribosylation and small-molecule messenger synthesis), mutagenic enzymes for immune receptor diversification and RNA-processing. Similarly, we discuss contributions of bacterial antibiotic/siderophore synthesis systems and intra-genomic and intra-cellular selfish elements (e.g. restriction-modification, mobile elements and lysogenic phages) in the emergence of chromatin remodeling/modifying enzymes and RNA-based regulation. We develop the concept that biological conflict systems served as evolutionary nurseries for innovations in the protein world, which were delivered to eukaryotes via lateral gene flow to spur key evolutionary innovations all the way from nucleogenesis to lineage-specific adaptations.
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spelling doaj.art-c5e367c3018d43ccbcb6616ff359ae252022-12-21T19:40:21ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882012-06-01210.3389/fcimb.2012.0008930179Gene flow and biological conflict systems in the origin and evolution of eukaryotesL eAravind0Vivek eAnantharaman1Dapeng eZhang2Robson Francisco De Souza3Lakshminarayan M Iyer4National Institutes of HealthNational Institutes of HealthNational Institutes of HealthNational Institutes of HealthNational Institutes of HealthThe endosymbiotic origin of eukaryotes brought together two disparate genomes in the cell. Additionally, eukaryotic natural history has included other endosymbiotic events, phagotrophic consumption of organisms, and intimate interactions with viruses and endoparasites. These phenomena facilitated large-scale lateral gene transfer and biological conflicts. We synthesize information from nearly two decades of genomics to illustrate how the interplay between lateral gene transfer and biological conflicts has impacted the emergence of new adaptations in eukaryotes. Using apicomplexans as example, we illustrate how lateral transfer from animals has contributed to unique parasite-host interfaces comprised of adhesion- and O-linked glycosylation-related domains. Adaptations, emerging due to intense selection for diversity in the molecular participants in organismal and genomic conflicts, being dispersed by lateral transfer, were subsequently exapted for eukaryote-specific innovations. We illustrate this using examples relating to eukaryotic chromatin, RNAi and RNA-processing systems, signaling pathways, apoptosis and immunity. We highlight the major contributions from catalytic domains of bacterial toxin-systems to the origin of signaling enzymes (e.g. ADP-ribosylation and small-molecule messenger synthesis), mutagenic enzymes for immune receptor diversification and RNA-processing. Similarly, we discuss contributions of bacterial antibiotic/siderophore synthesis systems and intra-genomic and intra-cellular selfish elements (e.g. restriction-modification, mobile elements and lysogenic phages) in the emergence of chromatin remodeling/modifying enzymes and RNA-based regulation. We develop the concept that biological conflict systems served as evolutionary nurseries for innovations in the protein world, which were delivered to eukaryotes via lateral gene flow to spur key evolutionary innovations all the way from nucleogenesis to lineage-specific adaptations.http://journal.frontiersin.org/Journal/10.3389/fcimb.2012.00089/fullRNAitoxinsantibioticsendosymbiosisbiological conflictimmunity proteins
spellingShingle L eAravind
Vivek eAnantharaman
Dapeng eZhang
Robson Francisco De Souza
Lakshminarayan M Iyer
Gene flow and biological conflict systems in the origin and evolution of eukaryotes
Frontiers in Cellular and Infection Microbiology
RNAi
toxins
antibiotics
endosymbiosis
biological conflict
immunity proteins
title Gene flow and biological conflict systems in the origin and evolution of eukaryotes
title_full Gene flow and biological conflict systems in the origin and evolution of eukaryotes
title_fullStr Gene flow and biological conflict systems in the origin and evolution of eukaryotes
title_full_unstemmed Gene flow and biological conflict systems in the origin and evolution of eukaryotes
title_short Gene flow and biological conflict systems in the origin and evolution of eukaryotes
title_sort gene flow and biological conflict systems in the origin and evolution of eukaryotes
topic RNAi
toxins
antibiotics
endosymbiosis
biological conflict
immunity proteins
url http://journal.frontiersin.org/Journal/10.3389/fcimb.2012.00089/full
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AT robsonfranciscodesouza geneflowandbiologicalconflictsystemsintheoriginandevolutionofeukaryotes
AT lakshminarayanmiyer geneflowandbiologicalconflictsystemsintheoriginandevolutionofeukaryotes