Diurnal rhythms are ubiquitous in living organisms as basic adaptations to the light–dark cycles on Earth. They are also exploited as defensive mechanisms in host–parasite interactions, and parasite infestation is known to be enhanced by disruption of the host’s circadian clock. However, to what extent and how the host and parasite influence their opponent’s diurnal rhythms are not well understood. The marine cyanobacterium Prochlorococcus is the smallest but most abundant phototroph on the planet. Previously, we reported on cyanophages that infect Prochlorococcus as the first viral model that exhibits a diurnal rhythm and identified their distinct night-infection strategies. P-SSM2 adopts an intermediate strategy, as it can adsorb to the host in the dark but will not replicate without...[ Read more ]

Diurnal rhythms are ubiquitous in living organisms as basic adaptations to the light–dark cycles on Earth. They are also exploited as defensive mechanisms in host–parasite interactions, and parasite infestation is known to be enhanced by disruption of the host’s circadian clock. However, to what extent and how the host and parasite influence their opponent’s diurnal rhythms are not well understood. The marine cyanobacterium Prochlorococcus is the smallest but most abundant phototroph on the planet. Previously, we reported on cyanophages that infect Prochlorococcus as the first viral model that exhibits a diurnal rhythm and identified their distinct night-infection strategies. P-SSM2 adopts an intermediate strategy, as it can adsorb to the host in the dark but will not replicate without light. In diel cycles, the diurnal rhythm compels most P-SSM2 to infect their hosts at night.

This thesis will first introduce the benefits of cyanophage P-SSM2 night infection in maintaining the transcriptional rhythm of host Prochlorococcus. Although P-SSM2 did not replicate, transcribe, or interfere with host fundamental physiology under dark, phage transcription and replication were enhanced in the following day of night infection. This finding can be explained by the repressed transcriptional activity of the host circadian clock and metabolic pathways in the context of P-SSM2 day infection, while the host transcriptional rhythm was maintained in night infection. The phosphorylation dynamics of the host central circadian clock protein KaiC was also conserved in P-SSM2 night infection. The diurnal rhythm of P-SSM2 drives P-SSM2 to select a night infection strategy, and the maintenance of the host rhythm during night infection underpins the competitiveness and fitness of P-SSM2 in the natural environment.

As the dominant primary producer, Prochlorococcus, as well as its interactions with viral predators, drives the release of substantial amounts of dissolved organic matter (DOM) into the oceans. However, our understanding of the impact of environmental DOM on Prochlorococcus is limited. The last chapter will introduce another project that investigated how Prochlorococcus senses and responds to environmental DOM contributed by its neighboring cyanobacteria. Transcriptomic analysis revealed the genes responsive to foreign matter in cyanobacterial DOM, which include the previously identified coculture-responsive genes. The findings address the largely unexplored chain of reverse feedback from environmental organic matter to the most abundant photoautotrophs, which plays a critical role in the marine biological carbon pump.