Four additional natural 7-deazaguanine derivatives in phages and how to make them

Liang Cui; Seetharamsing Balamkundu; Chuan Fa Liu; Hong Ye; Jacob Hourihan; Astrid Rausch; Christopher Hauß; Emelie Nilsson; Matthias Hoetzinger; Karin Holmfeldt; Weijia Zhang; Laura Martinez-Alvarez; Xu Peng; Denise Tremblay; Sylvain Moinau; Natalie Solonenko; Matthew B. Sullivan; Yan Jiun Lee; Andrew Mulholland; Peter R. Weigele; Valérie de Crécy-Lagard; Peter C. Dedon; Geoffrey Hutinet

doi:10.1093/nar/gkad657

Four additional natural 7-deazaguanine derivatives in phages and how to make them

Liang Cui, Seetharamsing Balamkundu, Chuan Fa Liu, Hong Ye, Jacob Hourihan, Astrid Rausch, Christopher Hauß, Emelie Nilsson, Matthias Hoetzinger, Karin Holmfeldt, Weijia Zhang, Laura Martinez-Alvarez, Xu Peng, Denise Tremblay, Sylvain Moinau, Natalie Solonenko, Matthew B. Sullivan, Yan Jiun Lee, Andrew Mulholland, Peter R. WeigeleValérie de Crécy-Lagard, Peter C. Dedon, Geoffrey Hutinet

Functional Genomics

Research output: Contribution to journal › Journal article › Research › peer-review

3 Citations (Scopus)

11 Downloads (Pure)

Abstract

Bacteriophages and bacteria are engaged in a constant arms race, continually evolving new molecular tools to survive one another. To protect their genomic DNA from restriction enzymes, the most common bacterial defence systems, double-stranded DNA phages have evolved complex modifications that affect all four bases. This study focuses on modifications at position 7 of guanines. Eight derivatives of 7-deazaguanines were identified, including four previously unknown ones: 2'-deoxy-7-(methylamino)methyl-7-deazaguanine (mdPreQ1), 2'-deoxy-7-(formylamino)methyl-7-deazaguanine (fdPreQ1), 2'-deoxy-7-deazaguanine (dDG) and 2'-deoxy-7-carboxy-7-deazaguanine (dCDG). These modifications are inserted in DNA by a guanine transglycosylase named DpdA. Three subfamilies of DpdA had been previously characterized: bDpdA, DpdA1, and DpdA2. Two additional subfamilies were identified in this work: DpdA3, which allows for complete replacement of the guanines, and DpdA4, which is specific to archaeal viruses. Transglycosylases have now been identified in all phages and viruses carrying 7-deazaguanine modifications, indicating that the insertion of these modifications is a post-replication event. Three enzymes were predicted to be involved in the biosynthesis of these newly identified DNA modifications: 7-carboxy-7-deazaguanine decarboxylase (DpdL), dPreQ1 formyltransferase (DpdN) and dPreQ1 methyltransferase (DpdM), which was experimentally validated and harbors a unique fold not previously observed for nucleic acid methylases.

Original language	English
Journal	Nucleic Acids Research
Volume	51
Issue number	17
Pages (from-to)	9214-9226
Number of pages	13
ISSN	0305-1048
DOIs	https://doi.org/10.1093/nar/gkad657
Publication status	Published - 2023

Bibliographical note

Publisher Copyright:
© The Author(s) 2023. Published by Oxford University Press on behalf of Nucleic Acids Research.

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Cite this

Cui, L., Balamkundu, S., Liu, C. F., Ye, H., Hourihan, J., Rausch, A., Hauß, C., Nilsson, E., Hoetzinger, M., Holmfeldt, K., Zhang, W., Martinez-Alvarez, L., Peng, X., Tremblay, D., Moinau, S., Solonenko, N., Sullivan, M. B., Lee, Y. J., Mulholland, A., ... Hutinet, G. (2023). Four additional natural 7-deazaguanine derivatives in phages and how to make them. Nucleic Acids Research, 51(17), 9214-9226. https://doi.org/10.1093/nar/gkad657

Four additional natural 7-deazaguanine derivatives in phages and how to make them. / Cui, Liang; Balamkundu, Seetharamsing; Liu, Chuan Fa; Ye, Hong; Hourihan, Jacob; Rausch, Astrid; Hauß, Christopher; Nilsson, Emelie; Hoetzinger, Matthias; Holmfeldt, Karin; Zhang, Weijia; Martinez-Alvarez, Laura ; Peng, Xu; Tremblay, Denise; Moinau, Sylvain; Solonenko, Natalie; Sullivan, Matthew B.; Lee, Yan Jiun; Mulholland, Andrew; Weigele, Peter R.; de Crécy-Lagard, Valérie; Dedon, Peter C.; Hutinet, Geoffrey.

In: Nucleic Acids Research, Vol. 51, No. 17, 2023, p. 9214-9226.

Research output: Contribution to journal › Journal article › Research › peer-review

Cui, L, Balamkundu, S, Liu, CF, Ye, H, Hourihan, J, Rausch, A, Hauß, C, Nilsson, E, Hoetzinger, M, Holmfeldt, K, Zhang, W, Martinez-Alvarez, L , Peng, X, Tremblay, D, Moinau, S, Solonenko, N, Sullivan, MB, Lee, YJ, Mulholland, A, Weigele, PR, de Crécy-Lagard, V, Dedon, PC & Hutinet, G 2023, 'Four additional natural 7-deazaguanine derivatives in phages and how to make them', Nucleic Acids Research, vol. 51, no. 17, pp. 9214-9226. https://doi.org/10.1093/nar/gkad657

Cui, Liang ; Balamkundu, Seetharamsing ; Liu, Chuan Fa ; Ye, Hong ; Hourihan, Jacob ; Rausch, Astrid ; Hauß, Christopher ; Nilsson, Emelie ; Hoetzinger, Matthias ; Holmfeldt, Karin ; Zhang, Weijia ; Martinez-Alvarez, Laura ; Peng, Xu ; Tremblay, Denise ; Moinau, Sylvain ; Solonenko, Natalie ; Sullivan, Matthew B. ; Lee, Yan Jiun ; Mulholland, Andrew ; Weigele, Peter R. ; de Crécy-Lagard, Valérie ; Dedon, Peter C. ; Hutinet, Geoffrey. / Four additional natural 7-deazaguanine derivatives in phages and how to make them. In: Nucleic Acids Research. 2023 ; Vol. 51, No. 17. pp. 9214-9226.

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abstract = "Bacteriophages and bacteria are engaged in a constant arms race, continually evolving new molecular tools to survive one another. To protect their genomic DNA from restriction enzymes, the most common bacterial defence systems, double-stranded DNA phages have evolved complex modifications that affect all four bases. This study focuses on modifications at position 7 of guanines. Eight derivatives of 7-deazaguanines were identified, including four previously unknown ones: 2'-deoxy-7-(methylamino)methyl-7-deazaguanine (mdPreQ1), 2'-deoxy-7-(formylamino)methyl-7-deazaguanine (fdPreQ1), 2'-deoxy-7-deazaguanine (dDG) and 2'-deoxy-7-carboxy-7-deazaguanine (dCDG). These modifications are inserted in DNA by a guanine transglycosylase named DpdA. Three subfamilies of DpdA had been previously characterized: bDpdA, DpdA1, and DpdA2. Two additional subfamilies were identified in this work: DpdA3, which allows for complete replacement of the guanines, and DpdA4, which is specific to archaeal viruses. Transglycosylases have now been identified in all phages and viruses carrying 7-deazaguanine modifications, indicating that the insertion of these modifications is a post-replication event. Three enzymes were predicted to be involved in the biosynthesis of these newly identified DNA modifications: 7-carboxy-7-deazaguanine decarboxylase (DpdL), dPreQ1 formyltransferase (DpdN) and dPreQ1 methyltransferase (DpdM), which was experimentally validated and harbors a unique fold not previously observed for nucleic acid methylases.",

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AU - Cui, Liang

AU - Balamkundu, Seetharamsing

AU - Liu, Chuan Fa

AU - Ye, Hong

AU - Hourihan, Jacob

AU - Rausch, Astrid

AU - Hauß, Christopher

AU - Nilsson, Emelie

AU - Hoetzinger, Matthias

AU - Holmfeldt, Karin

AU - Zhang, Weijia

AU - Martinez-Alvarez, Laura

AU - Peng, Xu

AU - Tremblay, Denise

AU - Moinau, Sylvain

AU - Solonenko, Natalie

AU - Sullivan, Matthew B.

AU - Lee, Yan Jiun

AU - Mulholland, Andrew

AU - Weigele, Peter R.

AU - de Crécy-Lagard, Valérie

AU - Dedon, Peter C.

AU - Hutinet, Geoffrey

PY - 2023

Y1 - 2023

N2 - Bacteriophages and bacteria are engaged in a constant arms race, continually evolving new molecular tools to survive one another. To protect their genomic DNA from restriction enzymes, the most common bacterial defence systems, double-stranded DNA phages have evolved complex modifications that affect all four bases. This study focuses on modifications at position 7 of guanines. Eight derivatives of 7-deazaguanines were identified, including four previously unknown ones: 2'-deoxy-7-(methylamino)methyl-7-deazaguanine (mdPreQ1), 2'-deoxy-7-(formylamino)methyl-7-deazaguanine (fdPreQ1), 2'-deoxy-7-deazaguanine (dDG) and 2'-deoxy-7-carboxy-7-deazaguanine (dCDG). These modifications are inserted in DNA by a guanine transglycosylase named DpdA. Three subfamilies of DpdA had been previously characterized: bDpdA, DpdA1, and DpdA2. Two additional subfamilies were identified in this work: DpdA3, which allows for complete replacement of the guanines, and DpdA4, which is specific to archaeal viruses. Transglycosylases have now been identified in all phages and viruses carrying 7-deazaguanine modifications, indicating that the insertion of these modifications is a post-replication event. Three enzymes were predicted to be involved in the biosynthesis of these newly identified DNA modifications: 7-carboxy-7-deazaguanine decarboxylase (DpdL), dPreQ1 formyltransferase (DpdN) and dPreQ1 methyltransferase (DpdM), which was experimentally validated and harbors a unique fold not previously observed for nucleic acid methylases.

AB - Bacteriophages and bacteria are engaged in a constant arms race, continually evolving new molecular tools to survive one another. To protect their genomic DNA from restriction enzymes, the most common bacterial defence systems, double-stranded DNA phages have evolved complex modifications that affect all four bases. This study focuses on modifications at position 7 of guanines. Eight derivatives of 7-deazaguanines were identified, including four previously unknown ones: 2'-deoxy-7-(methylamino)methyl-7-deazaguanine (mdPreQ1), 2'-deoxy-7-(formylamino)methyl-7-deazaguanine (fdPreQ1), 2'-deoxy-7-deazaguanine (dDG) and 2'-deoxy-7-carboxy-7-deazaguanine (dCDG). These modifications are inserted in DNA by a guanine transglycosylase named DpdA. Three subfamilies of DpdA had been previously characterized: bDpdA, DpdA1, and DpdA2. Two additional subfamilies were identified in this work: DpdA3, which allows for complete replacement of the guanines, and DpdA4, which is specific to archaeal viruses. Transglycosylases have now been identified in all phages and viruses carrying 7-deazaguanine modifications, indicating that the insertion of these modifications is a post-replication event. Three enzymes were predicted to be involved in the biosynthesis of these newly identified DNA modifications: 7-carboxy-7-deazaguanine decarboxylase (DpdL), dPreQ1 formyltransferase (DpdN) and dPreQ1 methyltransferase (DpdM), which was experimentally validated and harbors a unique fold not previously observed for nucleic acid methylases.

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