Function, expression, specificity, diversity and incompatibility of actinobacteriophage <i>parABS</i> systems

Dedrick, Rebekah M.; Mavrich, Travis N.; Ng, Wei Lun; Reyes, Juan C. Cervantes; Olm, Matthew R.; Rush, Rachael E.; Jacobs-Sera, Deborah; Russell, Daniel A.; Hatfull, Graham F.

doi:10.1111/mmi.13414

Cited by 32 publications

(55 citation statements)

References 71 publications

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“…Efficient DNA sequencing methods are yielding numerous complete phage genomes that allow robust approaches to comparative genomics and mechanistic studies of specific phage proteins and pathways (31,32). Phage T4 provided a beautiful model for laying the foundations of molecular biology and for unraveling the biochemical processes directed by T4-type phages during lytic infections (reviewed in reference 33).…”

Section: Figmentioning

confidence: 99%

Vibrio Phage KVP40 Encodes a Functional NAD ⁺ Salvage Pathway

Lee

Miller

2017

J Bacteriol

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The genome of T4-type Vibrio bacteriophage KVP40 has five genes predicted to encode proteins of pyridine nucleotide metabolism, of which two, nadV and natV, would suffice for an NAD ϩ salvage pathway. NadV is an apparent nicotinamide phosphoribosyltransferase (NAmPRTase), and NatV is an apparent bifunctional nicotinamide mononucleotide adenylyltransferase (NMNATase) and nicotinamideadenine dinucleotide pyrophosphatase (Nudix hydrolase). Genes encoding the predicted salvage pathway were cloned and expressed in Escherichia coli, the proteins were purified, and their enzymatic properties were examined. KVP40 NadV NAmPRTase is active in vitro, and a clone complements a Salmonella mutant defective in both the bacterial de novo and salvage pathways. Similar to other NAmPRTases, the KVP40 enzyme displayed ATPase activity indicative of energy coupling in the reaction mechanism. The NatV NMNATase activity was measured in a coupled reaction system demonstrating NAD ϩ biosynthesis from nicotinamide, phosphoribosyl pyrophosphate, and ATP. The NatV Nudix hydrolase domain was also shown to be active, with preferred substrates of ADP-ribose, NAD ϩ , and NADH. Expression analysis using reverse transcriptionquantitative PCR (qRT-PCR) and enzyme assays of infected Vibrio parahaemolyticus cells demonstrated nadV and natV transcription during the early and delayed-early periods of infection when other KVP40 genes of nucleotide precursor metabolism are expressed. The distribution and phylogeny of NadV and NatV proteins among several large double-stranded DNA (dsDNA) myophages, and also those from some very large siphophages, suggest broad relevance of pyridine nucleotide scavenging in virus-infected cells. NAD ϩ biosynthesis presents another important metabolic resource control point by large, rapidly replicating dsDNA bacteriophages.IMPORTANCE T4-type bacteriophages enhance DNA precursor synthesis through reductive reactions that use NADH/NADPH as the electron donor and NAD ϩ for ADPribosylation of proteins involved in transcribing and translating the phage genome. We show here that phage KVP40 encodes a functional pyridine nucleotide scavenging pathway that is expressed during the metabolic period of the infection cycle. The pathway is conserved in other large, dsDNA phages in which the two genes, nadV and natV, share an evolutionary history in their respective phage-host group.

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Section: Figmentioning

confidence: 99%

Vibrio Phage KVP40 Encodes a Functional NAD ⁺ Salvage Pathway

Lee

Miller

2017

J Bacteriol

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“…Over a dozen different attB sites are predicted to be used for prophage integration (22). Interestingly, some phages – predominantly members of Cluster A – do not have an integration cassette and instead code for a parABS partitioning system (57, 58). In lysogeny, these phages replicate extrachromosomally at low copy number, although the replication functions have yet to be determined (58).…”

Section: Mycobacteriophage Genome Organization and Expressionmentioning

confidence: 99%

“…Curiously, in the Cluster A phages that have been transcriptionally characterized (L5, D29, StarStuff, RedRock, Kampe, SWU1), a non-coding region near the right genome end is transcribed extremely high very early in lytic growth (54, 58, 60, 61). There may be several small transcripts made, but their functions are not known.…”

Section: Mycobacteriophage Genome Organization and Expressionmentioning

confidence: 99%

“…Lysogenic gene expression has been explored in a few mycobacteriophages, primarily those in Clusters A, F, Q, and N (58, 59, 62, 63). Not unexpectedly, the repressor is typically expressed, and the lytic genes are switched off.…”

Section: Mycobacteriophage Genome Organization and Expressionmentioning

confidence: 99%

“…A subset of temperate mycobacteriophages do not have integration systems, but instead encode parABS systems similar to those used by plasmids to promote segregation into daughter cells at division (57, 58). These phages – all of which group in Cluster A but span 10 different subclusters – replicate extrachromosomally at low copy number, and as such are subject to incompatibility mediated potentially by both prophage replication system, and the partitioning systems themselves.…”

Section: Drivers Of Mycobacterial and Mycobacteriophage Dynamicsmentioning

confidence: 99%

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Mycobacteriophages

Hatfull

2018

Microbiol Spectr

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Mycobacteriophages are viruses that infect mycobacterial hosts. A large number of mycobacteriophages have been isolated and genomically characterized, providing insights into viral diversity and evolution, as well as fueling development of tools for mycobacterial genetics. Mycobacteriophages have intimate relationships with their hosts, and provide insights into the genetics and physiology of the mycobacteria, and tools for potential clinical applications such as drug development, diagnosis, vaccines, and potentially therapy.

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