Evolution of genome architecture in archaea: spontaneous generation of a new chromosome in Haloferax volcanii

The common ancestry of archaea and eukaryotes is evident in their genome architecture. All eukaryotic and several archaeal genomes consist of multiple chromosomes, each replicated from multiple origins. Three scenarios have been proposed for the evolution of this genome architecture: (1) mutational...

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Main Authors: Ausiannikava, Darya, Mitchell, Laura, Marriott, Hannah, Smith, Victoria, Hawkins, Michelle, Makarova, Kira S., Koonin, Eugene V., Nieduszynski, Conrad A., Allers, Thorsten
Format: Article
Published: Oxford University Press 2018
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Online Access:https://eprints.nottingham.ac.uk/51181/
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author Ausiannikava, Darya
Mitchell, Laura
Marriott, Hannah
Smith, Victoria
Hawkins, Michelle
Makarova, Kira S.
Koonin, Eugene V.
Nieduszynski, Conrad A.
Allers, Thorsten
author_facet Ausiannikava, Darya
Mitchell, Laura
Marriott, Hannah
Smith, Victoria
Hawkins, Michelle
Makarova, Kira S.
Koonin, Eugene V.
Nieduszynski, Conrad A.
Allers, Thorsten
author_sort Ausiannikava, Darya
building Nottingham Research Data Repository
collection Online Access
description The common ancestry of archaea and eukaryotes is evident in their genome architecture. All eukaryotic and several archaeal genomes consist of multiple chromosomes, each replicated from multiple origins. Three scenarios have been proposed for the evolution of this genome architecture: (1) mutational diversification of a multi-copy chromosome; (2) capture of a new chromosome by horizontal transfer; (3) acquisition of new origins and splitting into two replication-competent chromosomes. We report an example of the third scenario: the multi-origin chromosome of the archaeon Haloferax volcanii has split into two elements via homologous recombination. The newly-generated elements are bona fide chromosomes, because each bears ‘chromosomal’ replication origins, rRNA loci and essential genes. The new chromosomes were stable during routine growth but additional genetic manipulation, which involves selective bottlenecks, provoked further rearrangements. To the best of our knowledge, rearrangement of a naturally-evolved prokaryotic genome to generate two new chromosomes has not been described previously.
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spelling nottingham-511812020-05-04T19:48:03Z https://eprints.nottingham.ac.uk/51181/ Evolution of genome architecture in archaea: spontaneous generation of a new chromosome in Haloferax volcanii Ausiannikava, Darya Mitchell, Laura Marriott, Hannah Smith, Victoria Hawkins, Michelle Makarova, Kira S. Koonin, Eugene V. Nieduszynski, Conrad A. Allers, Thorsten The common ancestry of archaea and eukaryotes is evident in their genome architecture. All eukaryotic and several archaeal genomes consist of multiple chromosomes, each replicated from multiple origins. Three scenarios have been proposed for the evolution of this genome architecture: (1) mutational diversification of a multi-copy chromosome; (2) capture of a new chromosome by horizontal transfer; (3) acquisition of new origins and splitting into two replication-competent chromosomes. We report an example of the third scenario: the multi-origin chromosome of the archaeon Haloferax volcanii has split into two elements via homologous recombination. The newly-generated elements are bona fide chromosomes, because each bears ‘chromosomal’ replication origins, rRNA loci and essential genes. The new chromosomes were stable during routine growth but additional genetic manipulation, which involves selective bottlenecks, provoked further rearrangements. To the best of our knowledge, rearrangement of a naturally-evolved prokaryotic genome to generate two new chromosomes has not been described previously. Oxford University Press 2018-08-01 Article PeerReviewed Ausiannikava, Darya, Mitchell, Laura, Marriott, Hannah, Smith, Victoria, Hawkins, Michelle, Makarova, Kira S., Koonin, Eugene V., Nieduszynski, Conrad A. and Allers, Thorsten (2018) Evolution of genome architecture in archaea: spontaneous generation of a new chromosome in Haloferax volcanii. Molecular Biology and Evolution, 38 (8). pp. 1855-1868. ISSN 1537-1719 Chromosome Genome architecture Multipartite genome Homologous recombination Genome stability Archaea Haloferax volcanii https://academic.oup.com/mbe/advance-article/doi/10.1093/molbev/msy075/4972485 doi:10.1093/molbev/msy075 doi:10.1093/molbev/msy075
spellingShingle Chromosome
Genome architecture
Multipartite genome
Homologous recombination
Genome stability
Archaea
Haloferax volcanii
Ausiannikava, Darya
Mitchell, Laura
Marriott, Hannah
Smith, Victoria
Hawkins, Michelle
Makarova, Kira S.
Koonin, Eugene V.
Nieduszynski, Conrad A.
Allers, Thorsten
Evolution of genome architecture in archaea: spontaneous generation of a new chromosome in Haloferax volcanii
title Evolution of genome architecture in archaea: spontaneous generation of a new chromosome in Haloferax volcanii
title_full Evolution of genome architecture in archaea: spontaneous generation of a new chromosome in Haloferax volcanii
title_fullStr Evolution of genome architecture in archaea: spontaneous generation of a new chromosome in Haloferax volcanii
title_full_unstemmed Evolution of genome architecture in archaea: spontaneous generation of a new chromosome in Haloferax volcanii
title_short Evolution of genome architecture in archaea: spontaneous generation of a new chromosome in Haloferax volcanii
title_sort evolution of genome architecture in archaea: spontaneous generation of a new chromosome in haloferax volcanii
topic Chromosome
Genome architecture
Multipartite genome
Homologous recombination
Genome stability
Archaea
Haloferax volcanii
url https://eprints.nottingham.ac.uk/51181/
https://eprints.nottingham.ac.uk/51181/
https://eprints.nottingham.ac.uk/51181/