1. Gene Expression Patterns during Light and Dark Infection of Prochlorococcus by Cyanophage
- Author
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Luke R. Thompson, Sallie W. Chisholm, Qinglu Zeng, Massachusetts Institute of Technology. Department of Biology, Massachusetts Institute of Technology. Department of Civil and Environmental Engineering, Thompson, Luke Richard, Zeng, Qinglu, and Chisholm, Sallie W
- Subjects
0301 basic medicine ,lcsh:Medicine ,Gene Expression ,Plant Science ,Virus Replication ,Plastid terminal oxidase ,Biochemistry ,Bacteriophages ,Photosynthesis ,lcsh:Science ,Photosystem ,Prochlorococcus ,Viral Genomics ,Multidisciplinary ,biology ,Plant Biochemistry ,Organic Compounds ,Monosaccharides ,Genomics ,Darkness ,3. Good health ,Chemistry ,Viruses ,Physical Sciences ,Transcriptome Analysis ,Research Article ,Pentoses ,Carbohydrates ,Photophosphorylation ,Microbial Genomics ,Pentose phosphate pathway ,Biosynthesis ,Cyanobacteria ,Microbiology ,Phosphates ,Electron Transport ,03 medical and health sciences ,Virology ,Botany ,Genetics ,lcsh:R ,Organic Chemistry ,Organisms ,Chemical Compounds ,Biology and Life Sciences ,Computational Biology ,Cyanophage ,biology.organism_classification ,Genome Analysis ,030104 developmental biology ,lcsh:Q ,Photosynthetic membrane ,Transcriptome - 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[superscript +] reductase (FNR), which uses the electron acceptor NADP[superscript +] 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., Gordon and Betty Moore Foundation (GBMF495), National Science Foundation (U.S.) (OCE-1153588 and DBI-0424599), National Institutes of Health (U.S.) (Pre-Doctoral Training Grant T32GM007287)
- Published
- 2016