Cyanobacterial viruses exhibit diurnal rhythms during infection

Abstract

As an adaptation to the daily light–dark (diel) cycle, cyanobacteria exhibit diurnal rhythms of gene expression and cell cycle. The light–dark cycle also affects the life cycle of viruses (cyanophages) that infect the unicellular picocyanobacteriaProchlorococcusandSynechococcus, which are the major primary producers in the oceans. For example, the adsorption of some cyanophages to the host cells depends on light, and the burst sizes of cyanophages are positively correlated to the length of light exposure during infection. Recent metatranscriptomic studies revealed transcriptional rhythms of field cyanophage populations. However, the underlying mechanism remains to be determined, as cyanophage laboratory cultures have not been shown to exhibit diurnal transcriptional rhythms. Here, we studied variation in infection patterns and gene expression ofProchlorococcusphages in laboratory culture conditions as a function of light. We found three distinct diel-dependent life history traits in dark conditions (diel traits): no adsorption (cyanophage P-HM2), adsorption but no replication (cyanophage P-SSM2), and replication (cyanophage P-SSP7). Under light–dark cycles, each cyanophage exhibited rhythmic transcript abundance, and cyanophages P-HM2 and P-SSM2 also exhibited rhythmic adsorption patterns. Finally, we show evidence to link the diurnal transcriptional rhythm of cyanophages to the photosynthetic activity of the host, thus providing a mechanistic explanation for the field observations of cyanophage transcriptional rhythms. Our study identifies that cultured viruses can exhibit diurnal rhythms during infection, which might impact cyanophage population-level dynamics in the oceans.

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

“…In contrast, P-SSP7 dynamics were better explained by light-driven host growth rate. Our results corroborate the observations of [37], adding mechanistic evidences of light-driven Prochlorococcus infection dynamics. The failure of P-HM2 to adsorb to MED4 in the dark indicates that adsorption could be directly modulated by light, as suggested by [36].…”

“…As in [37]: "Axenic Prochlorococcus strains were grown in Port Shelter (Hong Kong) seawater-based Pro99 medium [57]. Batch cultures were incubated at 23 • C in continuous light (25 µmol quanta m −2 s −1 ) or a 14h light:10h dark cycle (35 µmol quanta m −2 s −1 in the light period).…”

“…Some studies suggested a possible dependence of viral production on the host cell cycle in different phytoplankton lineages [31][32][33][34] whereas the intracellular production of some viruses may be decoupled from host cell cycle and light levels [35,36]. A recent paper on the diel infection pattern of cyanophage infecting Prochlorococcus [37] suggests that the adsorption rhythm, as well as the transcription rhythm of cyanophage, may be related to the light-dark cycle and not to the host cell cycle. Analyzing light impacts on cyanophage-cyanobacteria dynamics requires some elaboration of the cyanophage life cycle.…”

Prochlorococcusphage ferredoxin: structural characterization and electron transfer to cyanobacterial sulfite reductases

“…However, it is unclear how the temporal expression of phage Fd changes the flux of nutrients during the cyclical lifecycle of cyanobacteria. Recent studies have revealed that cyanophage gene expression and replication is diurnally linked to host replication, with both processes occurring during the afternoonevening period when light intensity is high (18,78,79). Additionally, phage transcripts drop at night and when photosystem is compromised (18).…”

“…Recent studies have revealed that cyanophage gene expression and replication is diurnally linked to host replication, with both processes occurring during the afternoonevening period when light intensity is high (18,78,79). Additionally, phage transcripts drop at night and when photosystem is compromised (18). Despite these advances, we don't know what feedback loops govern expression of phage genes in infected cells, especially photosynthesis-related genes derived from host homologs.…”