Diversity and evolutionary relationships of <scp>T</scp>7‐like podoviruses infecting marine cyanobacteria

Dekel-Bird, Naama P.; Avrani, Sarit; Sabehi, Gazalah; Pekarsky, Irina; Marston, Marcia F.; Kirzner, Shay; Lindell, Debbie

doi:10.1111/1462-2920.12103

Cited by 61 publications

(93 citation statements)

References 79 publications

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“…% Cyanophage Sequences a broader range of hosts, whereas podo-and siphoviruses are specialists, infecting a narrow range of host species (20)(21)(22)(23)(24). To date no genetic marker has been clearly associated with phage morphological groups.…”

Section: Discussionmentioning

confidence: 99%

Ribonucleotide reductases reveal novel viral diversity and predict biological and ecological features of unknown marine viruses

Sakowski¹,

Munsell²,

Hyatt³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Virioplankton play a crucial role in aquatic ecosystems as topdown regulators of bacterial populations and agents of horizontal gene transfer and nutrient cycling. However, the biology and ecology of virioplankton populations in the environment remain poorly understood. Ribonucleotide reductases (RNRs) are ancient enzymes that reduce ribonucleotides to deoxyribonucleotides and thus prime DNA synthesis. Composed of three classes according to O 2 reactivity, RNRs can be predictive of the physiological conditions surrounding DNA synthesis. RNRs are universal among cellular life, common within viral genomes and virioplankton shotgun metagenomes (viromes), and estimated to occur within >90% of the dsDNA virioplankton sampled in this study. RNRs occur across diverse viral groups, including all three morphological families of tailed phages, making these genes attractive for studies of viral diversity. Differing patterns in virioplankton diversity were clear from RNRs sampled across a broad oceanic transect. The most abundant RNRs belonged to novel lineages of podoviruses infecting α-proteobacteria, a bacterial class critical to oceanic carbon cycling. RNR class was predictive of phage morphology among cyanophages and RNR distribution frequencies among cyanophages were largely consistent with the predictions of the "kill the winner-cost of resistance" model. RNRs were also identified for the first time to our knowledge within ssDNA viromes. These data indicate that RNR polymorphism provides a means of connecting the biological and ecological features of virioplankton populations. viral ecology | viral evolution | phage replication

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Section: Discussionmentioning

confidence: 99%

Ribonucleotide reductases reveal novel viral diversity and predict biological and ecological features of unknown marine viruses

Sakowski¹,

Munsell²,

Hyatt³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Resistant Prochlorococcus substrains used in this study (Table S1) were initially selected for resistance to one of the following T7-like cyanopodoviruses: P-SSP7, P-TIP2, or P-GSP1 for MED4-derived strains, P-SSP2 for MIT9312-derived strains, and P-SSP1 or P-RSP1 for MIT9215-derived strains, as described by Avrani et al (14). These and the following additional T7-like cyanopodoviruses were used in the present study to assess resistance range and host population decline: P-TIP1 and P-TIP38 for MED4 strains, P-SSP3b for MIT9312-derived strains, and P-TIP39 for MIT9215-derived strains (14,74). The susceptible control cultures used in this study were isolated at the same time as the initial resistance substrains and were derived from the same ancestral colonies as their respective resistant substrains (Fig.…”

Section: Methodsmentioning

confidence: 99%

Convergent evolution toward an improved growth rate and a reduced resistance range inProchlorococcusstrains resistant to phage

Avrani

Lindell

2015

Proc. Natl. Acad. Sci. U.S.A.

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Prochlorococcus is an abundant marine cyanobacterium that grows rapidly in the environment and contributes significantly to global primary production. This cyanobacterium coexists with many cyanophages in the oceans, likely aided by resistance to numerous co-occurring phages. Spontaneous resistance occurs frequently in Prochlorococcus and is often accompanied by a pleiotropic fitness cost manifested as either a reduced growth rate or enhanced infection by other phages. Here, we assessed the fate of a number of phage-resistant Prochlorococcus strains, focusing on those with a high fitness cost. We found that phage-resistant strains continued evolving toward an improved growth rate and a narrower resistance range, resulting in lineages with phenotypes intermediate between those of ancestral susceptible wild-type and initial resistant substrains. Changes in growth rate and resistance range often occurred in independent events, leading to a decoupling of the selection pressures acting on these phenotypes. These changes were largely the result of additional, compensatory mutations in noncore genes located in genomic islands, although genetic reversions were also observed. Additionally, a mutator strain was identified. The similarity of the evolutionary pathway followed by multiple independent resistant cultures and clones suggests they undergo a predictable evolutionary pathway. This process serves to increase both genetic diversity and infection permutations in Prochlorococcus populations, further augmenting the complexity of the interaction network between Prochlorococcus and its phages in nature. Last, our findings provide an explanation for the apparent paradox of a multitude of resistant Prochlorococcus cells in nature that are growing close to their maximal intrinsic growth rates.cyanobacteria | cyanophage | resistance | Prochlorococcus | virus

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“…All known marine cyanophages are tailed doublestranded DNA viruses belonging to three well-defined bacteriophage families, Myoviridae, Podoviridae, and Siphoviridae. Cyanomyoviruses tend to infect a broad range of hosts, often across Prochlorococcus and Synechococcus, while cyanopodoviruses and cyanosiphoviruses are generally host specific (5,(8)(9)(10)(11)(12)(13).…”

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confidence: 99%

“…Two discrete marine picocyanobacterial podovirus (MPP) phylogenetic clusters (MPP-A and MPP-B) were recognized based on the viral DNA polymerase gene (12). Recent studies suggested that MPP-B podoviruses are more abundant than MPP-A podoviruses (13,38,39). However, the relative abundances and spatial patterns of specific cyanopodovirus and cyanomyovirus phylogenetic lineages over the global ocean are still broadly unclear.…”

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confidence: 99%

Marine Cyanophages Demonstrate Biogeographic Patterns throughout the Global Ocean

Huang

Zhang

Jiao

et al. 2015

Appl Environ Microbiol

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cMyoviruses and podoviruses that infect cyanobacteria are the two major groups of marine cyanophages, but little is known of how their phylogenetic lineages are distributed in different habitats. In this study, we analyzed the phylogenetic relationships of cyanopodoviruses and cyanomyoviruses based on the existing genomes. The 28 cyanomyoviruses were classified into four clusters (I to IV), and 19 of the 20 cyanopodoviruses were classified into two clusters, MPP-A and MPP-B, with four subclusters within cluster MPP-B. These genomes were used to recruit cyanophage-like fragments from microbial and viral metagenomes to estimate the relative abundances of these cyanophage lineages. Our results showed that cyanopodoviruses and cyanomyoviruses are both abundant in various marine environments and that clusters MPP-B, II and III appear to be the most dominant lineages. Cyanopodoviruses and cluster I and IV cyanomyoviruses exhibited habitat-related variability in their relative levels of abundance, while cluster II and III cyanomyoviruses appeared to be consistently dominant in various habitats. Multivariate analyses showed that reads that mapped to Synechococcus phages and Prochlorococcus phages had distinct distribution patterns that were significantly correlated to those of Synechococcus and Prochlorococcus, respectively. The Mantel test also revealed a strong correlation between the community compositions of cyanophages and picocyanobacteria. Given that cyanomyoviruses tend to have a broad host range and some can cross-infect Synechococcus and Prochlorococcus, while cyanopodoviruses are commonly host specific, the observation that their community compositions both correlated significantly with that of picocyanobacteria was unexpected. Although cyanomyoviruses and cyanopodoviruses differ in host specificity, their biogeographic distributions are likely both constrained by the picocyanobacterial community.

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Diversity and evolutionary relationships of T7‐like podoviruses infecting marine cyanobacteria

Cited by 61 publications

References 79 publications

Ribonucleotide reductases reveal novel viral diversity and predict biological and ecological features of unknown marine viruses

Ribonucleotide reductases reveal novel viral diversity and predict biological and ecological features of unknown marine viruses

Convergent evolution toward an improved growth rate and a reduced resistance range inProchlorococcusstrains resistant to phage

Marine Cyanophages Demonstrate Biogeographic Patterns throughout the Global Ocean

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