A novel roseobacter phage possesses features of podoviruses, siphoviruses, prophages and gene transfer agents

Zhan, Yuanchao; Huang, Sijun; Voget, Sonja; Simon, Meinhard; Chen, Feng

doi:10.1038/srep30372

Cited by 46 publications

(53 citation statements)

References 61 publications

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“…Roseophage SIO1 and DSS3Ф8 also possess the phoH gene [13,26]. Phage-encoded phoH genes have previously been described as apparent parts of a multi-gene family with divergent functions and have played a part in phospholipid metabolism, RNA modification, and fatty acid beta-oxidation [54,61,62].…”

Section: Resultsmentioning

confidence: 99%

A Novel Roseosiphophage Isolated from the Oligotrophic South China Sea

Yang

Cai

et al. 2017

Viruses

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The Roseobacter clade is abundant and widespread in marine environments and plays an important role in oceanic biogeochemical cycling. In this present study, a lytic siphophage (labeled vB_DshS-R5C) infecting the strain type of Dinoroseobacter shibae named DFL12T, which is part of the Roseobacter clade, was isolated from the oligotrophic South China Sea. Phage R5C showed a narrow host range, short latent period and low burst size. The genome length of phage R5C was 77, 874 bp with a G+C content of 61.5%. Genomic comparisons detected no genome matches in the GenBank database and phylogenetic analysis based on DNA polymerase I revealed phylogenetic features that were distinct to other phages, suggesting the novelty of R5C. Several auxiliary metabolic genes (e.g., phoH gene, heat shock protein and queuosine biosynthesis genes) were identified in the R5C genome that may be beneficial to the host and/or offer a competitive advantage for the phage. Among siphophages infecting the Roseobacter clade (roseosiphophages), four gene transfer agent-like genes were commonly located with close proximity to structural genes, suggesting that their function may be related to the tail of siphoviruses. The isolation and characterization of R5C demonstrated the high genomic and physiological diversity of roseophages as well as improved our understanding of host–phage interactions and the ecology of the marine Roseobacter.

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Section: Resultsmentioning

confidence: 99%

A Novel Roseosiphophage Isolated from the Oligotrophic South China Sea

Yang

Cai

et al. 2017

Viruses

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“…All phages with both genes have relatively large dsDNA genomes (from Ruegeria phage DSS3P8 of 146,135 bp to Cronobacter sakazakii phage GAP32 of 358,663 bp). Nearly all of the phages with the two-gene system are Myoviridae phages, with the exception of the Siphoviridae phage DSS3P8 and the large Siphoviridae Caulobacter crescentus phiCbK and phiCbK-like phages (13,14). Clustal Omega alignments and neighbor-joining trees ( Fig.…”

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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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“…However, despite the ecological significance of the Roseobacter clade (Luo & Moran, ), only a small number of roseophages have been isolated and described (Liang et al., ). The few characterized roseophages are assigned to either the Podoviridae or Siphoviridae families, comprising both lytic and temperate phages (Ankrah, Budinoff, Wilson, Wilhelm, & Buchan, ; Liang et al., ; Zhan, Huang, Voget, Simon, & Chen, ) and are considered a key driving force for the genomic diversification of the Roseobacter clade (Zhan et al., ).…”

Section: Discussionmentioning

confidence: 99%

“…The few characterized roseophages are assigned to either the Podoviridae or Siphoviridae families, comprising both lytic and temperate phages (Ankrah, Budinoff, Wilson, Wilhelm, & Buchan, 2014;Liang et al, 2016;Zhan, Huang, Voget, Simon, & Chen, 2016) and are considered a key driving force for the genomic diversification of the Roseobacter clade (Zhan et al, 2016).…”

Section: Atp Synthasementioning

confidence: 99%

Transcriptional response of Nautella italica R11 towards its macroalgal host uncovers new mechanisms of host–pathogen interaction

et al. 2017

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Macroalgae (seaweeds) are essential for the functioning of temperate marine ecosystems, but there is increasing evidence to suggest that their survival is under threat from anthropogenic stressors and disease. Nautella italica R11 is recognized as an aetiological agent of bleaching disease in the red alga, Delisea pulchra. Yet, there is a lack of knowledge surrounding the molecular mechanisms involved in this model host-pathogen interaction. Here we report that mutations in the gene encoding for a LuxR-type quorum sensing transcriptional regulator, RaiR, render N. italica R11 avirulent, suggesting this gene is important for regulating the expression of virulence phenotypes. Using an RNA sequencing approach, we observed a strong transcriptional response of N. italica R11 towards the presence of D. pulchra. In particular, genes involved in oxidative stress resistance, carbohydrate and central metabolism were upregulated in the presence of the host, suggesting a role for these functions in the opportunistic pathogenicity of N. italica R11. Furthermore, we show that RaiR regulates a subset of genes in N. italica R11, including those involved in metabolism and the expression of phage-related proteins. The outcome of this research reveals new functions important for virulence of N. italica R11 and contributes to our greater understanding of the complex factors mitigating microbial diseases in macroalgae.

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A novel roseobacter phage possesses features of podoviruses, siphoviruses, prophages and gene transfer agents

Cited by 46 publications

References 61 publications

A Novel Roseosiphophage Isolated from the Oligotrophic South China Sea

A Novel Roseosiphophage Isolated from the Oligotrophic South China Sea

Vibrio Phage KVP40 Encodes a Functional NAD ⁺ Salvage Pathway

Transcriptional response of Nautella italica R11 towards its macroalgal host uncovers new mechanisms of host–pathogen interaction

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A novel roseobacter phage possesses features of podoviruses, siphoviruses, prophages and gene transfer agents

Cited by 46 publications

References 61 publications

A Novel Roseosiphophage Isolated from the Oligotrophic South China Sea

A Novel Roseosiphophage Isolated from the Oligotrophic South China Sea

Vibrio Phage KVP40 Encodes a Functional NAD + Salvage Pathway

Transcriptional response of Nautella italica R11 towards its macroalgal host uncovers new mechanisms of host–pathogen interaction

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Vibrio Phage KVP40 Encodes a Functional NAD ⁺ Salvage Pathway