Diel Infection of Cyanobacteria by Cyanophages

Ni, Tianchi; Zeng, Qinglu

doi:10.3389/fmars.2015.00123

Cited by 25 publications

(22 citation statements)

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“…Prochlorococcus cyanobacteria are distributed across temperature and light gradients in the ocean environment (3,(20)(21)(22). They are specialized into high-light (HL)-and low-light (LL)-adapted ecotypes (23)(24)(25).…”

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confidence: 99%

“…In contrast, HL ecotypes grow faster at medium light intensities, have a low concentration of divinyl chlorophyll a and b, and have only constitutive photosystem II light-harvesting complexes (23)(24)(25). Prochlorococcus cells do not have a circadian rhythm; rather, they have a diurnal rhythm that can be synchronized under light-dark cycles (21,26,27). This diurnal rhythm is divided predominantly into photosynthesis during the light phase and cell division associated with energy consumption during the dark phase (22,28).…”

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confidence: 99%

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Linking Light-Dependent Life History Traits with Population Dynamics for Prochlorococcus and Cyanophage

et al. 2020

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Prochlorococcus cyanobacteria grow in diurnal rhythms driven by diel cycles. Their ecology depends on light, nutrients, and top-down mortality processes, including lysis by viruses. Cyanophage, viruses that infect cyanobacteria, are also impacted by light. For example, the extracellular viability and intracellular infection kinetics of some cyanophage vary between light and dark conditions. Nonetheless, it remains unclear whether light-dependent viral life history traits scale up to influence population-level dynamics. Here, we examined the impact of diel forcing on both cellular- and population-scale dynamics in multiple Prochlorococcus-phage systems. To do so, we developed a light-driven population model, including both cellular growth and viral infection dynamics. We then tested the model against measurements of experimental infection dynamics with diel forcing to examine the extent to which population level changes in both viral and host abundances could be explained by light-dependent life history traits. Model-data integration reveals that light-dependent adsorption can improve fits to population dynamics for some virus-host pairs. However, light-dependent variation alone does not fully explain realized host and virus population dynamics. Instead, we show evidence consistent with lysis saturation at relatively high virus-to-cell ratios. Altogether, our study represents a quantitative approach to integrate mechanistic models to reconcile Prochlorococcus-virus dynamics spanning cellular-to-population scales. IMPORTANCE The cyanobacterium Prochlorococcus is an essential member of global ocean ecosystems. Light rhythms drive Prochlorococcus photosynthesis, ecology, and interactions with potentially lethal viruses. At present, the impact of light on Prochlorococcus-virus interactions is not well understood. Here, we analyzed Prochlorococcus and virus population dynamics with a light-driven population model and compared our results with experimental data. Our approach revealed that light profoundly drives both cellular- and population-level dynamics for some host-virus systems. However, we also found that additional mechanisms, including lysis saturation, are required to explain observed host-virus dynamics at the population scale. This study provides the basis for future work to understand the intertwined fates of Prochlorococcus and associated viruses in the surface ocean.

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Linking Light-Dependent Life History Traits with Population Dynamics for Prochlorococcus and Cyanophage

et al. 2020

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“…Support of this model will require biochemical understanding of its individual elements, such as protein complexes with FNR and CP12, and changes in the flow of electrons as infection proceeds. Investigations into the intrinsic role of light will eventually need to incorporate the host’s light–dark cycle and cell cycle [62], which are confounding but ultimately essential aspects of this phage–host metabolic parasitism in the wild.…”

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confidence: 99%

Gene Expression Patterns during Light and Dark Infection of Prochlorococcus by Cyanophage

Thompson

Zeng

2016

PLoS ONE

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Cyanophage infecting the marine cyanobacteria Prochlorococcus and Synechococcus require light and host photosystem activity for optimal reproduction. Many cyanophages encode multiple photosynthetic electron transport (PET) proteins, which are presumed to maintain electron flow and produce ATP and NADPH for nucleotide biosynthesis and phage genome replication. However, evidence suggests phage augment NADPH production via the pentose phosphate pathway (PPP), thus calling into question the need for NADPH production by PET. Genes implicated in cyclic PET have since been identified in cyanophage genomes. It remains an open question which mode of PET, cyclic or linear, predominates in infected cyanobacteria, and thus whether the balance is towards producing ATP or NADPH. We sequenced transcriptomes of a cyanophage (P-HM2) and its host (Prochlorococcus MED4) throughout infection in the light or in the dark, and analyzed these data in the context of phage replication and metabolite measurements. Infection was robust in the light, but phage were not produced in the dark. Host gene transcripts encoding high-light inducible proteins and two terminal oxidases (plastoquinol terminal oxidase and cytochrome c oxidase)—implicated in protecting the photosynthetic membrane from light stress—were the most enriched in light but not dark infection. Among the most diminished transcripts in both light and dark infection was ferredoxin–NADP+ reductase (FNR), which uses the electron acceptor NADP+ to generate NADPH in linear photosynthesis. The phage gene for CP12, which putatively inhibits the Calvin cycle enzyme that receives NADPH from FNR, was highly expressed in light infection. Therefore, both PET production of NADPH and its consumption by carbon fixation are putatively repressed during phage infection in light. Transcriptomic evidence is thus consistent with cyclic photophosphorylation using oxygen as the terminal electron acceptor as the dominant mode of PET under infection, with ATP from PET and NADPH from the PPP producing the energy and reducing equivalents for phage nucleotide biosynthesis and replication.

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“…Prochlorococcus are distributed across temperature and light gradients in the ocean environment [3,[20][21][22]. They are specialized into High-Light (HL), and Low-Light (LL) adapted ecotypes [23][24][25].…”

Section: Introductionmentioning

confidence: 99%

“…chlorophyll a and b, and have only constitutive photosystem II light-harvesting complexes [23][24][25]. Prochlorococcus cells do not have a circadian rhythm but rather a diurnal rhythm that persists and can be synchronized under light-dark cycles [22,26,27]. This diurnal rhythm is divided into photosynthesis during the light phase and cell division associated with energy consumption during the dark phase [21,28].…”

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confidence: 99%

Linking light-dependent life history traits with population dynamics forProchlorococcusand cyanophage

Demory

Liu

Chen

et al. 2019

Preprint

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Prochlorococcus grow in diurnal rhythms driven by diel cycles. Their ecology depends on light, nutrients, and top-down mortality processes including lysis by viruses. Cyanophage, viruses that infect cyanobacteria, are also impacted by light. For example, extracellular viability and intracell infection kinetics of some cyanophage vary between light and dark conditions. Nonetheless, it remains unclear if light-dependent viral life history traits scale-up to influence population-level dynamics. Here we examined the impact of diel-forcing on both cellular-and population-scale dynamics in multiple Prochlorococcus-phage systems. To do so, we developed a light-driven population model including both cellular growth and viral infection dynamics. We then tested the model against measurements of experimental infection dynamics with diel forcing to examine the extent to which population level changes in both viral and host abundances could be explained by light-dependent life history traits. Model-data integration reveals that light-dependent adsorption can improve fits to population dynamics for some virus-host pairs. However, light-dependent variation alone does not fully explain realized host and virus population dynamics. Instead, we show evidence of a previously unrecognized lysis saturation at relatively high virus to cell ratios. Altogether, our study represents a quantitative approach to integrate mechanistic models to reconcile Prochlorococcus-virus dynamics spanning cellular to population scales. chlorophyll a and b, and have only constitutive photosystem II light-harvesting complexes [23][24][25]. Prochlorococcus cells do not have a circadian rhythm but rather a diurnal rhythm that persists and can be synchronized under light-dark cycles [22,26,27]. This diurnal rhytm is divided into photosynthesis during the light phase and cell division associated with energy consuption during the dark phase [21,28].

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Diel Infection of Cyanobacteria by Cyanophages

Cited by 25 publications

References 74 publications

Linking Light-Dependent Life History Traits with Population Dynamics for Prochlorococcus and Cyanophage

Linking Light-Dependent Life History Traits with Population Dynamics for Prochlorococcus and Cyanophage

Gene Expression Patterns during Light and Dark Infection of Prochlorococcus by Cyanophage

Linking light-dependent life history traits with population dynamics forProchlorococcusand cyanophage

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