Unexpected Evolution of Lesion-Recognition Modules in Eukaryotic NER and Kinetoplast DNA Dynamics Proteins from Bacterial Mobile Elements

Summary: The provenance of several components of major uniquely eukaryotic molecular machines are increasingly being traced back to prokaryotic biological conflict systems. Here, we demonstrate that the N-terminal single-stranded DNA-binding domain from the anti-restriction protein ArdC, deployed by...

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Main Authors: Arunkumar Krishnan, A. Maxwell Burroughs, Lakshminarayan M. Iyer, L. Aravind
Format: Article
Language:English
Published: Elsevier 2018-11-01
Series:iScience
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004218301767
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spelling doaj-75e971a5937c4a4ca332a6cda8e74af62020-11-24T21:53:22ZengElsevieriScience2589-00422018-11-019192208Unexpected Evolution of Lesion-Recognition Modules in Eukaryotic NER and Kinetoplast DNA Dynamics Proteins from Bacterial Mobile ElementsArunkumar Krishnan0A. Maxwell Burroughs1Lakshminarayan M. Iyer2L. Aravind3National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USANational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USANational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USANational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA; Corresponding authorSummary: The provenance of several components of major uniquely eukaryotic molecular machines are increasingly being traced back to prokaryotic biological conflict systems. Here, we demonstrate that the N-terminal single-stranded DNA-binding domain from the anti-restriction protein ArdC, deployed by bacterial mobile elements against their host, was independently acquired twice by eukaryotes, giving rise to the DNA-binding domains of XPC/Rad4 and the Tc-38-like proteins in the stem kinetoplastid. In both instances, the ArdC-N domain tandemly duplicated forming an extensive DNA-binding interface. In XPC/Rad4, the ArdC-N domains (BHDs) also fused to the inactive transglutaminase domain of a peptide-N-glycanase ultimately derived from an archaeal conflict system. Alongside, we delineate several parallel acquisitions from conjugative elements/bacteriophages that gave rise to key components of the kinetoplast DNA (kDNA) replication apparatus. These findings resolve two outstanding questions in eukaryote biology: (1) the origin of the unique DNA lesion-recognition component of NER and (2) origin of the unusual, plasmid-like features of kDNA. : Genetics; Molecular Biology; Microbiology; Evolutionary Biology Subject Areas: Genetics, Molecular Biology, Microbiology, Evolutionary Biologyhttp://www.sciencedirect.com/science/article/pii/S2589004218301767
collection DOAJ
language English
format Article
sources DOAJ
author Arunkumar Krishnan
A. Maxwell Burroughs
Lakshminarayan M. Iyer
L. Aravind
spellingShingle Arunkumar Krishnan
A. Maxwell Burroughs
Lakshminarayan M. Iyer
L. Aravind
Unexpected Evolution of Lesion-Recognition Modules in Eukaryotic NER and Kinetoplast DNA Dynamics Proteins from Bacterial Mobile Elements
iScience
author_facet Arunkumar Krishnan
A. Maxwell Burroughs
Lakshminarayan M. Iyer
L. Aravind
author_sort Arunkumar Krishnan
title Unexpected Evolution of Lesion-Recognition Modules in Eukaryotic NER and Kinetoplast DNA Dynamics Proteins from Bacterial Mobile Elements
title_short Unexpected Evolution of Lesion-Recognition Modules in Eukaryotic NER and Kinetoplast DNA Dynamics Proteins from Bacterial Mobile Elements
title_full Unexpected Evolution of Lesion-Recognition Modules in Eukaryotic NER and Kinetoplast DNA Dynamics Proteins from Bacterial Mobile Elements
title_fullStr Unexpected Evolution of Lesion-Recognition Modules in Eukaryotic NER and Kinetoplast DNA Dynamics Proteins from Bacterial Mobile Elements
title_full_unstemmed Unexpected Evolution of Lesion-Recognition Modules in Eukaryotic NER and Kinetoplast DNA Dynamics Proteins from Bacterial Mobile Elements
title_sort unexpected evolution of lesion-recognition modules in eukaryotic ner and kinetoplast dna dynamics proteins from bacterial mobile elements
publisher Elsevier
series iScience
issn 2589-0042
publishDate 2018-11-01
description Summary: The provenance of several components of major uniquely eukaryotic molecular machines are increasingly being traced back to prokaryotic biological conflict systems. Here, we demonstrate that the N-terminal single-stranded DNA-binding domain from the anti-restriction protein ArdC, deployed by bacterial mobile elements against their host, was independently acquired twice by eukaryotes, giving rise to the DNA-binding domains of XPC/Rad4 and the Tc-38-like proteins in the stem kinetoplastid. In both instances, the ArdC-N domain tandemly duplicated forming an extensive DNA-binding interface. In XPC/Rad4, the ArdC-N domains (BHDs) also fused to the inactive transglutaminase domain of a peptide-N-glycanase ultimately derived from an archaeal conflict system. Alongside, we delineate several parallel acquisitions from conjugative elements/bacteriophages that gave rise to key components of the kinetoplast DNA (kDNA) replication apparatus. These findings resolve two outstanding questions in eukaryote biology: (1) the origin of the unique DNA lesion-recognition component of NER and (2) origin of the unusual, plasmid-like features of kDNA. : Genetics; Molecular Biology; Microbiology; Evolutionary Biology Subject Areas: Genetics, Molecular Biology, Microbiology, Evolutionary Biology
url http://www.sciencedirect.com/science/article/pii/S2589004218301767
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