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T4 genes in the marine ecosystem: studies of the T4-like cyanophages and their role in marine ecology.

Clokie MR, Millard AD, Mann NH - Virol. J. (2010)

Bottom Line: Other host-derived genes encode enzymes involved in carbon metabolism, phosphate acquisition and ppGpp metabolism.The impact of these host-derived genes on phage fitness has still largely to be assessed and represents one of the most important topics in the study of this group of T4-like phages in the laboratory.However, these phages are also of considerable environmental significance by virtue of their impact on key contributors to oceanic primary production and the true extent and nature of this impact has still to be accurately assessed.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences, University of Warwick, Coventry, CV4 7AL, UK.

ABSTRACT
From genomic sequencing it has become apparent that the marine cyanomyoviruses capable of infecting strains of unicellular cyanobacteria assigned to the genera Synechococcus and Prochlorococcus are not only morphologically similar to T4, but are also genetically related, typically sharing some 40-48 genes. The large majority of these common genes are the same in all marine cyanomyoviruses so far characterized. Given the fundamental physiological differences between marine unicellular cyanobacteria and heterotrophic hosts of T4-like phages it is not surprising that the study of cyanomyoviruses has revealed novel and fascinating facets of the phage-host relationship. One of the most interesting features of the marine cyanomyoviruses is their possession of a number of genes that are clearly of host origin such as those involved in photosynthesis, like the psbA gene that encodes a core component of the photosystem II reaction centre. Other host-derived genes encode enzymes involved in carbon metabolism, phosphate acquisition and ppGpp metabolism. The impact of these host-derived genes on phage fitness has still largely to be assessed and represents one of the most important topics in the study of this group of T4-like phages in the laboratory. However, these phages are also of considerable environmental significance by virtue of their impact on key contributors to oceanic primary production and the true extent and nature of this impact has still to be accurately assessed.

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Related in: MedlinePlus

Cryoelectron micrographs of purified S-PM2 phage particles. (A) Showing one phage particle in the extended form and one in the contracted form both still have DNA in their heads and (B) Two phage particles with contracted tail sheaths, the particle on the left has ejected its DNA. The lack of collar structure is particularly visible in (B). The diameter of the head is 65 nm. Pictures were taken at the University of Warwick with the kind assistance of Dr Svetla Stoilova-McPhie.
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Figure 1: Cryoelectron micrographs of purified S-PM2 phage particles. (A) Showing one phage particle in the extended form and one in the contracted form both still have DNA in their heads and (B) Two phage particles with contracted tail sheaths, the particle on the left has ejected its DNA. The lack of collar structure is particularly visible in (B). The diameter of the head is 65 nm. Pictures were taken at the University of Warwick with the kind assistance of Dr Svetla Stoilova-McPhie.

Mentions: In their review on the interplay between bacterial host and T4 phage physiology, Kutter et al [1] stated that "efforts to understand the infection process and evolutionary pressures in the natural habitat(s) of T-even phages need to take into account bacterial metabolism and intracellular environments under such conditions". This statement was made around the time that the first cyanophages infecting marine cyanobacteria were being isolated and characterized and the majority of which exhibited a T4-like morphology (Figure 1) and [2-4]. Obviously, the metabolic properties and intracellular environments of obligately photoautotrophic marine cyanobacteria are very different to those of the heterotrophic bacteria that had been studied as the experimental hosts of T4-like phages and no less significant are the differences between the environments in which they are naturally found. It is not surprising, therefore, that the study of these phages has led to the recognition of remarkable new features of the phage-host relationship and this is reflected by the fact that they have been referred to as "photosynthetic phages" [5,6]. These T4-like phages of cyanobacteria have extensively been referred to as cyanomyoviruses and this is the term we have used throughout this review. Without doubt the most exciting advances have been associated with an analysis of their ecological significance, particularly with respect to their role in determining the structure of marine cyanobacterial populations and diverting fixed carbon away from higher trophic levels and into the microbial loop. Associated with this have been the extraordinary developments in our understanding of marine viral communities obtained through metagenomic approaches e.g. [7-9] and these are inextricably linked to the revelations from genomic analyses that these phages carry a significant number of genes of clearly host origin such as those involved in photosynthesis, which raises important questions regarding the metabolic function of these genes and their contribution to phage fitness. Obviously, this has major implications for horizontal gene transfer between phages, but also between hosts. Finally, from genomic sequencing it has also become apparent that the cyanomyoviruses are not only morphologically similar to T4, but are also genetically interrelated. It is still too early for these key areas, which form the major substance of this review, to have been extensively reviewed, but aspects of these topics have been covered [10-12].


T4 genes in the marine ecosystem: studies of the T4-like cyanophages and their role in marine ecology.

Clokie MR, Millard AD, Mann NH - Virol. J. (2010)

Cryoelectron micrographs of purified S-PM2 phage particles. (A) Showing one phage particle in the extended form and one in the contracted form both still have DNA in their heads and (B) Two phage particles with contracted tail sheaths, the particle on the left has ejected its DNA. The lack of collar structure is particularly visible in (B). The diameter of the head is 65 nm. Pictures were taken at the University of Warwick with the kind assistance of Dr Svetla Stoilova-McPhie.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2984593&req=5

Figure 1: Cryoelectron micrographs of purified S-PM2 phage particles. (A) Showing one phage particle in the extended form and one in the contracted form both still have DNA in their heads and (B) Two phage particles with contracted tail sheaths, the particle on the left has ejected its DNA. The lack of collar structure is particularly visible in (B). The diameter of the head is 65 nm. Pictures were taken at the University of Warwick with the kind assistance of Dr Svetla Stoilova-McPhie.
Mentions: In their review on the interplay between bacterial host and T4 phage physiology, Kutter et al [1] stated that "efforts to understand the infection process and evolutionary pressures in the natural habitat(s) of T-even phages need to take into account bacterial metabolism and intracellular environments under such conditions". This statement was made around the time that the first cyanophages infecting marine cyanobacteria were being isolated and characterized and the majority of which exhibited a T4-like morphology (Figure 1) and [2-4]. Obviously, the metabolic properties and intracellular environments of obligately photoautotrophic marine cyanobacteria are very different to those of the heterotrophic bacteria that had been studied as the experimental hosts of T4-like phages and no less significant are the differences between the environments in which they are naturally found. It is not surprising, therefore, that the study of these phages has led to the recognition of remarkable new features of the phage-host relationship and this is reflected by the fact that they have been referred to as "photosynthetic phages" [5,6]. These T4-like phages of cyanobacteria have extensively been referred to as cyanomyoviruses and this is the term we have used throughout this review. Without doubt the most exciting advances have been associated with an analysis of their ecological significance, particularly with respect to their role in determining the structure of marine cyanobacterial populations and diverting fixed carbon away from higher trophic levels and into the microbial loop. Associated with this have been the extraordinary developments in our understanding of marine viral communities obtained through metagenomic approaches e.g. [7-9] and these are inextricably linked to the revelations from genomic analyses that these phages carry a significant number of genes of clearly host origin such as those involved in photosynthesis, which raises important questions regarding the metabolic function of these genes and their contribution to phage fitness. Obviously, this has major implications for horizontal gene transfer between phages, but also between hosts. Finally, from genomic sequencing it has also become apparent that the cyanomyoviruses are not only morphologically similar to T4, but are also genetically interrelated. It is still too early for these key areas, which form the major substance of this review, to have been extensively reviewed, but aspects of these topics have been covered [10-12].

Bottom Line: Other host-derived genes encode enzymes involved in carbon metabolism, phosphate acquisition and ppGpp metabolism.The impact of these host-derived genes on phage fitness has still largely to be assessed and represents one of the most important topics in the study of this group of T4-like phages in the laboratory.However, these phages are also of considerable environmental significance by virtue of their impact on key contributors to oceanic primary production and the true extent and nature of this impact has still to be accurately assessed.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences, University of Warwick, Coventry, CV4 7AL, UK.

ABSTRACT
From genomic sequencing it has become apparent that the marine cyanomyoviruses capable of infecting strains of unicellular cyanobacteria assigned to the genera Synechococcus and Prochlorococcus are not only morphologically similar to T4, but are also genetically related, typically sharing some 40-48 genes. The large majority of these common genes are the same in all marine cyanomyoviruses so far characterized. Given the fundamental physiological differences between marine unicellular cyanobacteria and heterotrophic hosts of T4-like phages it is not surprising that the study of cyanomyoviruses has revealed novel and fascinating facets of the phage-host relationship. One of the most interesting features of the marine cyanomyoviruses is their possession of a number of genes that are clearly of host origin such as those involved in photosynthesis, like the psbA gene that encodes a core component of the photosystem II reaction centre. Other host-derived genes encode enzymes involved in carbon metabolism, phosphate acquisition and ppGpp metabolism. The impact of these host-derived genes on phage fitness has still largely to be assessed and represents one of the most important topics in the study of this group of T4-like phages in the laboratory. However, these phages are also of considerable environmental significance by virtue of their impact on key contributors to oceanic primary production and the true extent and nature of this impact has still to be accurately assessed.

Show MeSH
Related in: MedlinePlus