A temporal and spatial investigation of cyanophage abundance in the Gulf of Aqaba, Red Sea

Millard, Andrew; Mann, Nicholas H.

doi:10.1017/s0025315406013415

Cited by 31 publications

(48 citation statements)

References 22 publications

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“…The use of Synechococcus strains not generally used for phage isolation may partially explain this. Alternatively, some of the unidentified cyanophages reported previously (37,38,40) may belong to the TIM5-like lineage, but were not sequenced so could not be identified.…”

Section: Discussionmentioning

confidence: 99%

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A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans

Sabehi

Shaulov

Silver

et al. 2012

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

102

128

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Viruses infecting bacteria (phages) are thought to greatly impact microbial population dynamics as well as the genome diversity and evolution of their hosts. Here we report on the discovery of a novel lineage of tailed dsDNA phages belonging to the family Myoviridae and describe its first representative, S-TIM5, that infects the ubiquitous marine cyanobacterium, Synechococcus. The genome of this phage encodes an entirely unique set of structural proteins not found in any currently known phage, indicating that it uses lineage-specific genes for virion morphogenesis and represents a previously unknown lineage of myoviruses. Furthermore, among its distinctive collection of replication and DNA metabolism genes, it carries a mitochondrial-like DNA polymerase gene, providing strong evidence for the bacteriophage origin of the mitochondrial DNA polymerase. S-TIM5 also encodes an array of bacterial-like metabolism genes commonly found in phages infecting cyanobacteria including photosynthesis, carbon metabolism and phosphorus acquisition genes. This suggests a common gene pool and gene swapping of cyanophage-specific genes among different phage lineages despite distinct sets of structural and replication genes. All cytosines following purine nucleotides are methylated in the S-TIM5 genome, constituting a unique methylation pattern that likely protects the genome from nuclease degradation. This phage is abundant in the Red Sea and S-TIM5 gene homologs are widespread in the oceans. This unusual phage type is thus likely to be an important player in the oceans, impacting the population dynamics and evolution of their primary producing cyanobacterial hosts.

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Section: Discussionmentioning

confidence: 99%

“…Strangely, this abundant and widespread phage lineage has not been identified previously even though marine cyanobacteria have been used for two decades to isolate phages (9,30,(37)(38)(39). Indeed, it was previously thought that isolates represent the genetic diversity of cyanophages in nature (3).…”

Section: Discussionmentioning

confidence: 99%

A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans

Sabehi

Shaulov

Silver

et al. 2012

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

102

128

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“…3A) is similar to that of other studies in a variety of marine locations. In particular, the abundances of total viruses and cyanophages tend to be greatest in warmer seasons and/or lowest in the winter (Waterbury & Valois 1993, Jiang & Paul 1994, Suttle & Chan 1994, Cochran & Paul 1998, Marston & Sallee 2003, Millard & Mann 2006, Sandaa & Larsen 2006, Wang et al 2011, Parsons et al 2012. Some of these studies also found that cyanophage abundances co-vary with cyanobacterial abundance and temperature (e.g.…”

Section: Discussionmentioning

confidence: 99%

Diversity and temporal dynamics of Southern California coastal marine cyanophage isolates

Clasen¹,

Hanson²,

Ibrahim³

et al. 2013

Aquat. Microb. Ecol.

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Marine ecosystems contain an immense diversity of phages, many of which infect the cyanobacteria responsible for a portion of oceanic primary productivity. To add to the growing body of research on the dynamics and diversity of these cyanophages, we measured cyanophage abundance, diversity, and community composition monthly for 15 mo at 3 coastal locations in Southern California, USA. We characterized over 900 individual cyanophages, isolated on Synechococcus sp. WH7803, by amplifying and sequencing 2 different genes from each isolate: g20 (the portal protein gene) and psbA (a host-derived gene involved in photosynthesis). The taxonomic composition and diversity of isolated cyanophages were highly variable over time, with little variation across the 3 locations. Particular taxa dominated the community at distinct times of year, with more rapid turnover of dominant types and higher overall abundance and diversity during spring and summer. These temporal patterns as well as taxonomic designations were highly congruent for both genes, based on operational taxonomic units (OTUs) defined at 99% nucleotide similarity, despite a greater level of amino acid conservation within psbA as compared to g20. Overall, this suggests that either gene can serve as a useful marker for cyanophage diversity. However, we detected 1 myovirus taxon (representing about 2.5% of the isolates) of uncertain phylogenetic affiliation that was negative for psbA amplification. Further sampling is necessary to assess whether these temporal dynamics in cyanophage composition, diversity, and abundance are seasonally recurring.

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“…It has been known that there is a tight coupling between picocyanobacterial abundance and cyanophage titer, either temporally or spatially (4,5,7,11,33). A monthly temporal survey at the same sampling site in the Gulf of Aqaba showed that the diversity and abundance of cyanomyoviruses were correlated to those of cooccurring Synechococcus populations (6).…”

Section: ) and Clusters Mpp-a And Mpp-b For Cyanopodovirusesmentioning

confidence: 99%

“…Cyanomyoviruses and cyanopodoviruses appear to be much more abundant than cyanosiphoviruses in the ocean (11,25,33,34), and cyanopodoviruses are likely as abundant as cyanomyoviruses (21). The genetic diversity of marine cyanomyoviruses and cyanopodoviruses has been extensively investigated using molecular markers (see reference 35 for a review).…”

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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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A temporal and spatial investigation of cyanophage abundance in the Gulf of Aqaba, Red Sea

Cited by 31 publications

References 22 publications

A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans

A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans

Diversity and temporal dynamics of Southern California coastal marine cyanophage isolates

Marine Cyanophages Demonstrate Biogeographic Patterns throughout the Global Ocean

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