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Characterization of a triad of genes in cyanophage S-2L sufficient to replace adenine by 2-aminoadenine in bacterial DNA

View ORCID ProfileD. Czernecki, F. Bonhomme, P.A. Kaminski, M. Delarue
doi: https://doi.org/10.1101/2021.04.30.442174
D. Czernecki
1Unit of Architecture and Dynamics of Biological Macromolecules, CNRS UMR 3528, 25-28 rue du Docteur Roux, Institut Pasteur, 75015 Paris, France
2Sorbonne Université, Collège Doctoral, ED 515, 75005 Paris, France
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F. Bonhomme
3Unit of Epigenetic Chemistry, CNRS UMR 3523, Institut Pasteur, 75015 Paris, France
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P.A. Kaminski
4Unit of Biology of Pathogenic Gram-Positive Bacteria, 25-28 rue du Docteur Roux, Institut Pasteur, 75015 Paris, France
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M. Delarue
1Unit of Architecture and Dynamics of Biological Macromolecules, CNRS UMR 3528, 25-28 rue du Docteur Roux, Institut Pasteur, 75015 Paris, France
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  • For correspondence: marc.delarue@pasteur.fr
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Abstract

Cyanophage S-2L is known to profoundly alter the biophysical properties of its DNA by replacing all adenines (A) with 2-aminoadenines (Z), which still pair with thymines but with a triple hydrogen bond. It was recently demonstrated that a homologue of adenylosuccinate synthase (PurZ) and a dATP triphosphohydrolase (DatZ) are two important pieces of the metabolism of 2-aminoadenine, participating in the synthesis of ZTGC-DNA. Here, we determine that S-2L PurZ can use either dATP or ATP as a source of energy, thereby also depleting the pool of nucleotides in dATP. Furthermore, we identify a conserved gene (mazZ) located between purZ and datZ genes in Siphoviridae phage genomes, and show that it encodes a (d)GTP-specific diphosphohydrolase, thereby providing the substrate of PurZ in the 2-aminoadenine synthesis pathway. High-resolution crystal structures of S-2L PurZ and MazZ with their respective substrates provide a rationale for their specificities. The Z-cluster made of these three genes – datZ, mazZ and purZ – was expressed in E. coli, resulting in a successful incorporation of 2-aminoadenine in the bacterial chromosomal and plasmidic DNA. This work opens the possibility to study synthetic organisms containing ZTGC-DNA.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted April 30, 2021.
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Characterization of a triad of genes in cyanophage S-2L sufficient to replace adenine by 2-aminoadenine in bacterial DNA
D. Czernecki, F. Bonhomme, P.A. Kaminski, M. Delarue
bioRxiv 2021.04.30.442174; doi: https://doi.org/10.1101/2021.04.30.442174
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Characterization of a triad of genes in cyanophage S-2L sufficient to replace adenine by 2-aminoadenine in bacterial DNA
D. Czernecki, F. Bonhomme, P.A. Kaminski, M. Delarue
bioRxiv 2021.04.30.442174; doi: https://doi.org/10.1101/2021.04.30.442174

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