Dataset Information

Temporal transcriptional patterns of cyanophage genes suggest synchronized infection of cyanobacteria in the oceans.

ABSTRACT:

Background

Based on the peak expression times during infection, early, middle, and late genes have been characterized in viruses (cyanophages) that infect the unicellular cyanobacterium Prochlorococcus. Laboratory experiments show that some cyanophages can only replicate in the light and thus exhibit diurnal infection rhythms under light-dark cycles. Field evidence also suggests synchronized infection of Prochlorococcus by cyanophages in the oceans, which should result in progressive expression of cyanophage early, middle, and late genes. However, distinct temporal expression patterns have not been observed in cyanophage field populations.

Results

In this study, we reanalyzed a previous metatranscriptomic dataset collected in the North Pacific Subtropical Gyre. In this dataset, it was previously shown that aggregate transcripts from cyanophage scaffolds display diurnal transcriptional rhythms with transcript abundances decreasing at night. By mapping metatranscriptomic reads to individual viral genes, we identified periodically expressed genes from putative viruses infecting the cyanobacteria Prochlorococcus and Synechococcus, heterotrophic bacteria, and algae. Of the 41 cyanophage genes, 35 were from cyanomyoviruses. We grouped the periodically expressed cyanomyovirus genes into early, middle, and late genes based on the conserved temporal expression patterns of their orthologs in cyanomyovirus laboratory cultures. We found that the peak expression times of late genes in cyanophage field populations were significantly later than those of early and middle genes, which were similar to the temporal expression patterns of synchronized cyanophage laboratory cultures.

Conclusions

The significantly later peak expression times of late genes in cyanomyovirus field populations suggest that cyanophage infection of Prochlorococcus is synchronized in the North Pacific Subtropical Gyre. The night-time peak expression of late genes also suggests synchronized lysis of Prochlorococcus at night, which might result in synchronized release of dissolved organic matter to the marine food web. Video abstract.

SUBMITTER: Chen Y

PROVIDER: S-EPMC7238727 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Publications

Temporal transcriptional patterns of cyanophage genes suggest synchronized infection of cyanobacteria in the oceans.

Chen Yue Y Zeng Qinglu Q

Microbiome 20200519 1

<h4>Background</h4>Based on the peak expression times during infection, early, middle, and late genes have been characterized in viruses (cyanophages) that infect the unicellular cyanobacterium Prochlorococcus. Laboratory experiments show that some cyanophages can only replicate in the light and thus exhibit diurnal infection rhythms under light-dark cycles. Field evidence also suggests synchronized infection of Prochlorococcus by cyanophages in the oceans, which should result in progressive exp ...[more]

PMID: 32430017

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Project description: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.

Project description:In cyanobacteria, alkanes are synthesized from a fatty acyl-ACP by two enzymes, acyl-acyl carrier protein reductase and aldehyde deformylating oxygenase. Despite the great interest in the exploitation for biofuel production, nothing is known about the transcriptional organization of their genes or the physiological function of alkane synthesis. The comparison of 115 microarray datasets indicates the relatively constitutive expression of aar and ado genes. The analysis of 181 available genomes showed that in 90% of the genomes both genes are present, likely indicating their physiological relevance. In 61% of them they cluster together with genes encoding acetyl-CoA carboxyl transferase and a short-chain dehydrogenase, strengthening the link to fatty acid metabolism and in 76% of the genomes they are located in tandem, suggesting constraints on the gene arrangement. However, contrary to the expectations for an operon, we found in Synechocystis sp. PCC 6803 specific promoters for the two genes, sll0208 (ado) and sll0209 (aar), which give rise to monocistronic transcripts. Moreover, the upstream located ado gene is driven by a proximal as well as a second, distal, promoter, from which a third transcript, the ~160 nt sRNA SyR9 is transcribed. Thus, the transcriptional organization of the alkane biosynthesis genes in Synechocystis sp. PCC 6803 is of substantial complexity. We verified all three promoters to function independently from each other and show a similar promoter arrangement also in the more distant Nodularia spumigena, Trichodesmium erythraeum, Anabaena sp. PCC 7120, Prochlorococcus MIT9313, and MED4. The presence of separate regulatory elements and the dominance of monocistronic mRNAs suggest the possible autonomous regulation of ado and aar. The complex transcriptional organization of the alkane synthesis gene cluster has possible metabolic implications and should be considered when manipulating the expression of these genes in cyanobacteria.

Dataset Information

Temporal transcriptional patterns of cyanophage genes suggest synchronized infection of cyanobacteria in the oceans.

Background

Results

Conclusions

Publications

Temporal transcriptional patterns of cyanophage genes suggest synchronized infection of cyanobacteria in the oceans.

Similar Datasets

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