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

Abstract

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.

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

“…Similarly, light conditions also modify the cyanophage replication phase. An increase in viral production in light and a reduction in viral production in dark have been reported for Synechococcus (39)(40)(41) and Prochlorococcus (42)(43)(44).…”

Multiple mechanisms drive phage infection efficiency in nearly identical hosts

“…The work presented here invites discussing infection efficiency, as efficiency is a term with relative uses in the literature. Briefly, in phage studies, the term "efficient" is used to describe either infections or phages that lyse the most cells the fastest [28,29], have the shortest LP/best growth rate [104], display better intracellular capabilities (e.g., in DNA replication [105] or gene transcription [37], or are proficient at hijacking host RNAP [37]). In contrast, the eukaryotic viral literature evaluates whether each step of the complex viral infection, from attachment to dispersion, is efficient [106][107][108][109][110][111][112][113].…”

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

“…Similarly, light conditions also modify the virus cycle during the cyanophage replication phase. A positive relationship between light and viral production and reduction at dark have been reported for Synechococcus [39][40][41] and Prochlorococcus [42][43][44]. Some cyanophage also have genes that encode proteins involved in photosynthesis, suggesting that they can maintain the photosynthetic activity of their host during infection [45,46].…”