Unique and universal features of Epsilonproteobacterial origins of chromosome replication and DnaA-DnaA box interactions
In bacteria, chromosome replication is initiated by the interaction of the initiator protein DnaA with a defined region of a chromosome at which DNA replication starts (oriC). While DnaA proteins share significant homology regardless of phylogeny, oriC regions exhibit more variable structures. The g...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2016-09-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01555/full |
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| author | Pawel Jaworski Rafal Donczew Thorsten Mielke Marcel Thiel Stanislaw Oldziej Christoph Weigel Anna Magdalena Pawlik |
| author_facet | Pawel Jaworski Rafal Donczew Thorsten Mielke Marcel Thiel Stanislaw Oldziej Christoph Weigel Anna Magdalena Pawlik |
| author_sort | Pawel Jaworski |
| collection | DOAJ |
| description | In bacteria, chromosome replication is initiated by the interaction of the initiator protein DnaA with a defined region of a chromosome at which DNA replication starts (oriC). While DnaA proteins share significant homology regardless of phylogeny, oriC regions exhibit more variable structures. The general architecture of oriCs is universal, i.e. they are composed of a cluster of DnaA binding sites, a DNA-unwinding element, and sequences that bind regulatory proteins. However, detailed structures of oriCs are shared by related species while being significantly different in unrelated bacteria. In this work, we characterised Epsilonproteobacterial oriC regions. Helicobacter pylori was the only species of the class for which oriC was characterised. A few unique features were found such as bipartite oriC structure, not encountered in any other Gram-negative species, and topology-sensitive DnaA-DNA interactions, which have not been found in any other bacterium. These unusual H. pylori oriC features raised questions of whether oriC structure and DnaA-DNA interactions are unique to this bacterium or they are common to related species. By in silico and in vitro analyses we identified putative oriCs in three Epsilonproteobacterial species: pathogenic Arcobacter butzleri, symbiotic Wolinella succinogenes and free-living Sulfurimonas denitrificans. We propose that oriCs typically co-localize with ruvC-dnaA-dnaN in Epsilonproteobacteria, with the exception of Helicobacteriaceae species. The clusters of DnaA boxes localize upstream (oriC1) and downstream (oriC2) of dnaA, and they likely constitute bipartite origins. In all cases, DNA unwinding was shown to occur in oriC2. Unlike the DnaA box pattern, which is not conserved in Epsilonproteobacterial oriCs, the consensus DnaA box sequences and the mode of DnaA-DnaA box interactions are common to the class. We propose that the typical Epsilonproteobacterial DnaA box consists of the core nucleotide sequence 5’-TTCAC-3’ (4-8 nt), which, together with the significant changes in the DNA-binding motif of corresponding DnaAs, determines the unique molecular mechanism of DnaA-DNA interaction. Our results will facilitate identification of oriCs and subsequent identification of factors which regulate chromosome replication in other Epsilonproteobacteria. Since replication is controlled at the initiation step, it will help to better characterise life cycles of these species, many of which are considered as emerging pathogens. |
| first_indexed | 2024-04-14T04:46:30Z |
| format | Article |
| id | doaj.art-4fef70691ab34bedb72047f6dcbb8a75 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-14T04:46:30Z |
| publishDate | 2016-09-01 |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-4fef70691ab34bedb72047f6dcbb8a752022-12-22T02:11:27ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2016-09-01710.3389/fmicb.2016.01555219615Unique and universal features of Epsilonproteobacterial origins of chromosome replication and DnaA-DnaA box interactionsPawel Jaworski0Rafal Donczew1Thorsten Mielke2Marcel Thiel3Stanislaw Oldziej4Christoph Weigel5Anna Magdalena Pawlik6Hirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of SciencesHirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of SciencesMax Planck Institute for Molecular GeneticsIntercollegiate Faculty of Biotechnology, University of Gdańsk and Medical University of GdańskIntercollegiate Faculty of Biotechnology, University of Gdańsk and Medical University of GdańskHTW BerlinHirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of SciencesIn bacteria, chromosome replication is initiated by the interaction of the initiator protein DnaA with a defined region of a chromosome at which DNA replication starts (oriC). While DnaA proteins share significant homology regardless of phylogeny, oriC regions exhibit more variable structures. The general architecture of oriCs is universal, i.e. they are composed of a cluster of DnaA binding sites, a DNA-unwinding element, and sequences that bind regulatory proteins. However, detailed structures of oriCs are shared by related species while being significantly different in unrelated bacteria. In this work, we characterised Epsilonproteobacterial oriC regions. Helicobacter pylori was the only species of the class for which oriC was characterised. A few unique features were found such as bipartite oriC structure, not encountered in any other Gram-negative species, and topology-sensitive DnaA-DNA interactions, which have not been found in any other bacterium. These unusual H. pylori oriC features raised questions of whether oriC structure and DnaA-DNA interactions are unique to this bacterium or they are common to related species. By in silico and in vitro analyses we identified putative oriCs in three Epsilonproteobacterial species: pathogenic Arcobacter butzleri, symbiotic Wolinella succinogenes and free-living Sulfurimonas denitrificans. We propose that oriCs typically co-localize with ruvC-dnaA-dnaN in Epsilonproteobacteria, with the exception of Helicobacteriaceae species. The clusters of DnaA boxes localize upstream (oriC1) and downstream (oriC2) of dnaA, and they likely constitute bipartite origins. In all cases, DNA unwinding was shown to occur in oriC2. Unlike the DnaA box pattern, which is not conserved in Epsilonproteobacterial oriCs, the consensus DnaA box sequences and the mode of DnaA-DnaA box interactions are common to the class. We propose that the typical Epsilonproteobacterial DnaA box consists of the core nucleotide sequence 5’-TTCAC-3’ (4-8 nt), which, together with the significant changes in the DNA-binding motif of corresponding DnaAs, determines the unique molecular mechanism of DnaA-DNA interaction. Our results will facilitate identification of oriCs and subsequent identification of factors which regulate chromosome replication in other Epsilonproteobacteria. Since replication is controlled at the initiation step, it will help to better characterise life cycles of these species, many of which are considered as emerging pathogens.http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01555/fullEpsilonproteobacteriaDNAAoriCinitiation of chromosome replicationorisomednaA box |
| spellingShingle | Pawel Jaworski Rafal Donczew Thorsten Mielke Marcel Thiel Stanislaw Oldziej Christoph Weigel Anna Magdalena Pawlik Unique and universal features of Epsilonproteobacterial origins of chromosome replication and DnaA-DnaA box interactions Frontiers in Microbiology Epsilonproteobacteria DNAA oriC initiation of chromosome replication orisome dnaA box |
| title | Unique and universal features of Epsilonproteobacterial origins of chromosome replication and DnaA-DnaA box interactions |
| title_full | Unique and universal features of Epsilonproteobacterial origins of chromosome replication and DnaA-DnaA box interactions |
| title_fullStr | Unique and universal features of Epsilonproteobacterial origins of chromosome replication and DnaA-DnaA box interactions |
| title_full_unstemmed | Unique and universal features of Epsilonproteobacterial origins of chromosome replication and DnaA-DnaA box interactions |
| title_short | Unique and universal features of Epsilonproteobacterial origins of chromosome replication and DnaA-DnaA box interactions |
| title_sort | unique and universal features of epsilonproteobacterial origins of chromosome replication and dnaa dnaa box interactions |
| topic | Epsilonproteobacteria DNAA oriC initiation of chromosome replication orisome dnaA box |
| url | http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01555/full |
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