Cyanophages from a less virulent clade dominate over their sister clade in global oceans

Maidanik, Ilia; Kirzner, Shay; Pekarski, Irena; Arsenieff, Laure; Tahan, Ran; Carlson, Michael C. G.; Shitrit, Dror; Baran, Nava; Goldin, Svetlana; Weitz, Joshua S.; Lindell, Debbie

doi:10.1038/s41396-022-01259-y

Cited by 8 publications

(11 citation statements)

References 60 publications

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“…To compare the infection kinetics of cyanopodoviruses under identical conditions, we used Prochlorococcus MED4 as the host, which can be infected by both the MPP-C and MPP-B phages. Two MPP-B phages P-SSP7 and P-GSP1 showed similar one step infection dynamics with latent periods of 6–8 h, which are consistent with previous studies of these two phages [ 51 , 62 , 63 ]. Following the latent period, the amounts of extracellular phage DNA for P-SSP7 and P-GSP1 increased exponentially until the plateaus were reached at ~16 hours after infection (Fig.…”

Section: Resultssupporting

confidence: 90%

Abundant and cosmopolitan lineage of cyanopodoviruses lacking a DNA polymerase gene

et al. 2022

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Cyanopodoviruses affect the mortality and population dynamics of the unicellular picocyanobacteria Prochlorococcus and Synechococcus, the dominant primary producers in the oceans. Known cyanopodoviruses all contain the DNA polymerase gene (DNA pol) that is important for phage DNA replication and widely used in field quantification and diversity studies. However, we isolated 18 cyanopodoviruses without identifiable DNA pol. They form a new MPP-C clade that was separated from the existing MPP-A, MPP-B, and P-RSP2 clades. The MPP-C phages have the smallest genomes (37.3–37.9 kb) among sequenced cyanophages, and show longer latent periods than the MPP-B phages. Metagenomic reads of both clades are highly abundant in surface waters, but the MPP-C phages show higher relative abundance in surface waters than in deeper waters, while MPP-B phages have higher relative abundance in deeper waters. Our study reveals that cyanophages with distinct genomic contents and infection kinetics can exhibit different depth profiles in the oceans.

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Section: Resultssupporting

confidence: 90%

Abundant and cosmopolitan lineage of cyanopodoviruses lacking a DNA polymerase gene

et al. 2022

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“…There are few studies of decay rates among marine phage isolates [ 67 ]. However, a recent study found that strains within two major lineages of cyanopodoviruses (clade A and B) did not differ significantly in their decay rates, despite these clades having clear differences in host range and lifestyle strategies [ 70 ]. Because phage decay is an important factor in the dynamics of community composition, more analysis of decay rate variation within a phylogenetic framework, especially for cyanomyoviruses, is warranted.…”

Section: Discussionmentioning

confidence: 99%

Diverse Marine T4-like Cyanophage Communities Are Primarily Comprised of Low-Abundance Species Including Species with Distinct Seasonal, Persistent, Occasional, or Sporadic Dynamics

Dart

Fuhrman

Ahlgren

2023

Viruses

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Cyanophages exert important top-down controls on their cyanobacteria hosts; however, concurrent analysis of both phage and host populations is needed to better assess phage–host interaction models. We analyzed picocyanobacteria Prochlorococcus and Synechococcus and T4-like cyanophage communities in Pacific Ocean surface waters using five years of monthly viral and cellular fraction metagenomes. Cyanophage communities contained thousands of mostly low-abundance (<2% relative abundance) species with varying temporal dynamics, categorized as seasonally recurring or non-seasonal and occurring persistently, occasionally, or sporadically (detected in ≥85%, 15-85%, or <15% of samples, respectively). Viromes contained mostly seasonal and persistent phages (~40% each), while cellular fraction metagenomes had mostly sporadic species (~50%), reflecting that these sample sets capture different steps of the infection cycle—virions from prior infections or within currently infected cells, respectively. Two groups of seasonal phages correlated to Synechococcus or Prochlorococcus were abundant in spring/summer or fall/winter, respectively. Cyanophages likely have a strong influence on the host community structure, as their communities explained up to 32% of host community variation. These results support how both seasonally recurrent and apparent stochastic processes, likely determined by host availability and different host-range strategies among phages, are critical to phage–host interactions and dynamics, consistent with both the Kill-the-Winner and the Bank models.

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“…Using the polony method, we quantified TIM5-like cyanophages over the annual cycle in the Red Sea at 20 m depth in 4 years between 2013 and 2016 (Figure 3). During this period, the water column exhibited typical seasonal dynamics for the Red Sea (Carlson et al, 2014;Lindell & Post, 1995;Maidanik et al, 2022). In the winter, the upper layers of the water column were colder (Figure 3A), which drove deep convective mixing and the influx of nutrients into the photic zone that stimulated phytoplankton productivity observed in increased chlorophyll concentrations (Figure 3B).…”

Section: Seasonal Distribution Patterns Of Tim5-like Cyanophages In T...mentioning

confidence: 97%

“…As the water column warmed from spring to early autumn (Figure 3A), the water column stratified. This is generally associated with succession of the phototrophic community from picoeukaryotes in winter, Synechococcus in early spring and Prochlorococcus in summer (Lindell & Post, 1995;Maidanik et al, 2022) and is reflected in the decreasing chlorophyll-a concentrations (Figure 3B). Maximum Synechococcus abundances, observed with monthly resolution, occurred in March following the onset of stratification after convective mixing.…”

Section: Seasonal Distribution Patterns Of Tim5-like Cyanophages In T...mentioning

confidence: 97%

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Widespread yet persistent low abundance of TIM5‐like cyanophages in the oceans

Baran

Carlson

Sabehi

et al. 2022

Environmental Microbiology

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Ocean ecosystems are inhabited by a diverse set of viruses that impact microbial mortality and evolution. However, the distribution and abundances of specific viral lineages, particularly those from the large bank of rare viruses, remains largely unknown. Here, we assessed the diversity and abundance of the TIM5-like cyanophages. The sequencing of three new TIM5-like cyanophage genomes and environmental amplicons of a signature gene from the Red Sea revealed highly conserved gene content and sequence similarity. We adapted the polony method, a solid-phase polymerase chain reaction assay, to quantify TIM5-like cyanophages during three 2000 km expeditions in the Pacific Ocean and four annual cycles in the Red Sea. TIM5-like cyanophages were widespread, detected at all latitudes and seasons surveyed throughout the photic zone. Yet they were generally rare, ranging between <100 and 4000 virusesÁml À1 . Occasional peaks in abundance of 10-to 100-fold were observed, reaching 71,000 virusesÁml À1 . These peaks were ephemeral and seasonally variable in the Red Sea. Infection levels, quantified during one such peak, were very low. These characteristics of low diversity and abundance, as well as variable outbreaks, distinguishes the TIM5-like lineage from other major cyanophage lineages and illuminates that rare virus lineages can be persistent and widespread in the oceans.

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Cyanophages from a less virulent clade dominate over their sister clade in global oceans

Cited by 8 publications

References 60 publications

Abundant and cosmopolitan lineage of cyanopodoviruses lacking a DNA polymerase gene

Abundant and cosmopolitan lineage of cyanopodoviruses lacking a DNA polymerase gene

Diverse Marine T4-like Cyanophage Communities Are Primarily Comprised of Low-Abundance Species Including Species with Distinct Seasonal, Persistent, Occasional, or Sporadic Dynamics

Widespread yet persistent low abundance of TIM5‐like cyanophages in the oceans

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