Cyanophage MazG is a Pyrophosphohydrolase but Unable to Hydrolyse Magic Spot Nucleotides

Overview

Journal Environ Microbiol Rep

Date 2019 Feb 28

PMID 30809954

Citations 24

Authors

Branko Rihtman

Sabine Bowman-Grahl

Andrew Millard

Rebecca M Corrigan

Martha R J Clokie

David J Scanlan

Affiliations

Soon will be listed here.

Abstract

Bacteriophage possess a variety of auxiliary metabolic genes of bacterial origin. These proteins enable them to maximize infection efficiency, subverting bacterial metabolic processes for the purpose of viral genome replication and synthesis of the next generation of virion progeny. Here, we examined the enzymatic activity of a cyanophage MazG protein - a putative pyrophosphohydrolase previously implicated in regulation of the stringent response via reducing levels of the central alarmone molecule (p)ppGpp. We demonstrate, however, that the purified viral MazG shows no binding or hydrolysis activity against (p)ppGpp. Instead, dGTP and dCTP appear to be the preferred substrates of this protein, consistent with a role preferentially hydrolysing deoxyribonucleotides from the high GC content host Synechococcus genome. This showcases a new example of the fine-tuned nature of viral metabolic processes.

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References

Lin X, Ding H, Zeng Q . Transcriptomic response during phage infection of a marine cyanobacterium under phosphorus-limited conditions. Environ Microbiol. 2015; 18(2):450-60. DOI: 10.1111/1462-2920.13104. View

Roitman S, Hornung E, Flores-Uribe J, Sharon I, Feussner I, Beja O . Cyanophage-encoded lipid desaturases: oceanic distribution, diversity and function. ISME J. 2017; 12(2):343-355. PMC: 5776448. DOI: 10.1038/ismej.2017.159. View

Kamiya H, Kasai H . 2-Hydroxy-dATP is incorporated opposite G by Escherichia coli DNA polymerase III resulting in high mutagenicity. Nucleic Acids Res. 2000; 28(7):1640-6. PMC: 102799. DOI: 10.1093/nar/28.7.1640. View

Zeidner G, Bielawski J, Shmoish M, Scanlan D, Sabehi G, Beja O . Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ Microbiol. 2005; 7(10):1505-13. DOI: 10.1111/j.1462-2920.2005.00833.x. View

Corrigan R, Bellows L, Wood A, Grundling A . ppGpp negatively impacts ribosome assembly affecting growth and antimicrobial tolerance in Gram-positive bacteria. Proc Natl Acad Sci U S A. 2016; 113(12):E1710-9. PMC: 4812758. DOI: 10.1073/pnas.1522179113. View

Millard A, Zwirglmaier K, Downey M, Mann N, Scanlan D . Comparative genomics of marine cyanomyoviruses reveals the widespread occurrence of Synechococcus host genes localized to a hyperplastic region: implications for mechanisms of cyanophage evolution. Environ Microbiol. 2009; 11(9):2370-87. DOI: 10.1111/j.1462-2920.2009.01966.x. View

Borbely G, Kaki C, Gulyas A, Farkas G . Bacteriophage infection interferes with guanosine 3'-diphosphate-5'-diphosphate accumulation induced by energy and nitrogen starvation in the cyanobacterium Anacystis nidulans. J Bacteriol. 1980; 144(3):859-64. PMC: 294745. DOI: 10.1128/jb.144.3.859-864.1980. View

Jones P, Binns D, Chang H, Fraser M, Li W, McAnulla C . InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014; 30(9):1236-40. PMC: 3998142. DOI: 10.1093/bioinformatics/btu031. View

Bryan M, Burroughs N, Spence E, Clokie M, Mann N, Bryan S . Evidence for the intense exchange of MazG in marine cyanophages by horizontal gene transfer. PLoS One. 2008; 3(4):e2048. PMC: 2297514. DOI: 10.1371/journal.pone.0002048. View

10.

Lindell D, Sullivan M, Johnson Z, Tolonen A, Rohwer F, Chisholm S . Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci U S A. 2004; 101(30):11013-8. PMC: 503735. DOI: 10.1073/pnas.0401526101. View

11.

Baran N, Goldin S, Maidanik I, Lindell D . Quantification of diverse virus populations in the environment using the polony method. Nat Microbiol. 2017; 3(1):62-72. PMC: 5739286. DOI: 10.1038/s41564-017-0045-y. View

12.

Doron S, Fedida A, Hernandez-Prieto M, Sabehi G, Karunker I, Stazic D . Transcriptome dynamics of a broad host-range cyanophage and its hosts. ISME J. 2015; 10(6):1437-55. PMC: 5029184. DOI: 10.1038/ismej.2015.210. View

13.

Enav H, Mandel-Gutfreund Y, Beja O . Comparative metagenomic analyses reveal viral-induced shifts of host metabolism towards nucleotide biosynthesis. Microbiome. 2014; 2(1):9. PMC: 4022391. DOI: 10.1186/2049-2618-2-9. View

14.

Sullivan M, Coleman M, Weigele P, Rohwer F, Chisholm S . Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol. 2005; 3(5):e144. PMC: 1079782. DOI: 10.1371/journal.pbio.0030144. View

15.

Sullivan M, Huang K, Ignacio-Espinoza J, Berlin A, Kelly L, Weigele P . Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol. 2010; 12(11):3035-56. PMC: 3037559. DOI: 10.1111/j.1462-2920.2010.02280.x. View

16.

Gross M, Marianovsky I, Glaser G . MazG -- a regulator of programmed cell death in Escherichia coli. Mol Microbiol. 2006; 59(2):590-601. DOI: 10.1111/j.1365-2958.2005.04956.x. View

17.

Moroz O, Murzin A, Makarova K, Koonin E, Wilson K, Galperin M . Dimeric dUTPases, HisE, and MazG belong to a new superfamily of all-alpha NTP pyrophosphohydrolases with potential "house-cleaning" functions. J Mol Biol. 2005; 347(2):243-55. DOI: 10.1016/j.jmb.2005.01.030. View

18.

Fridman S, Flores-Uribe J, Larom S, Alalouf O, Liran O, Yacoby I . A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected Prochlorococcus cells. Nat Microbiol. 2017; 2(10):1350-1357. DOI: 10.1038/s41564-017-0002-9. View

19.

Lindell D, Jaffe J, Johnson Z, Church G, Chisholm S . Photosynthesis genes in marine viruses yield proteins during host infection. Nature. 2005; 438(7064):86-9. DOI: 10.1038/nature04111. View

20.

Galperin M, Moroz O, Wilson K, Murzin A . House cleaning, a part of good housekeeping. Mol Microbiol. 2005; 59(1):5-19. DOI: 10.1111/j.1365-2958.2005.04950.x. View