Light-driven synchrony of Prochlorococcus growth and mortality in the subtropical Pacific gyre

Abstract

Theoretical studies predict that competition for limited resources reduces biodiversity to the point of ecological instability, whereas strong predator/prey interactions enhance the number of coexisting species and limit fluctuations in abundances. In open ocean ecosystems, competition for low availability of essential nutrients results in relatively few abundant microbial species. The remarkable stability in overall cell abundance of the dominant photosynthetic cyanobacterium Prochlorococcus is assumed to reflect a simple food web structure strongly controlled by grazers and/or viruses. This hypothesized link between stability and ecological interactions, however, has been difficult to test with open ocean microbes because sampling methods commonly have poor temporal and spatial resolution. Here we use continuous techniques on two different winter-time cruises to show that Prochlorococcus cell production and mortality rates are tightly synchronized to the day/night cycle across the subtropical Pacific Ocean. In warmer waters, we observed harmonic oscillations in cell production and mortality rates, with a peak in mortality rate consistently occurring ∼6 h after the peak in cell production. Essentially no cell mortality was observed during daylight. Our results are best explained as a synchronized two-component trophic interaction with the per-capita rates of Prochlorococcus consumption driven either directly by the day/night cycle or indirectly by Prochlorococcus cell production. Light-driven synchrony of food web dynamics in which most of the newly produced Prochlorococcus cells are consumed each night likely enforces ecosystem stability across vast expanses of the open ocean.cyanobacteria | cell division | mortality | flow cytometry | SeaFlow P otential interdependencies between species diversity and ecosystem stability have gained increased focus due to global changes in species distributions and abundances (1). Strong predator-prey interactions are predicted to enhance the number of coexisting species and limit fluctuations in abundances (2, 3), whereas competition for limited resources is predicted to reduce biodiversity, in some instances, to the point of ecological instability (3, 4). Mechanisms underlying ecosystem stability remain challenging to characterize on relevant temporal and spatial scales, in part because few empirical data are available to test these theories.Our focus is on the microbial communities within surface waters of the vast oligotrophic gyre of the north Pacific Subtropical Ocean. Here, competition for low concentrations of essential nutrients is hypothesized to result in relatively few abundant microbial species, typified by their extremely small cell sizes and streamlined genomes (5). The cyanobacterium Prochlorococcus numerically dominates the photosynthetic community in these regions, with a relatively constant cell abundance close to half a billion cells per liter despite a population doubling time of approximately one day (6). Such constant cell numbers are predicted when both...

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“…Several recent studies suggest a previously underappreciated importance of closely coupled diurnal oscillations as the underlying mechanisms of ecosystem stability in open ocean food webs (Ottesen et al, 2014;Ribalet et al, 2015). Our results show strong diurnal variability in photophysiology and cell metabolism of mixed phytoplankton assemblages.…”

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Diel Infection of Cyanobacteria by Cyanophages

“…Recently, the growth and mortality of Prochlorococcus in the subtropical Pacific gyre was found to be synchronized to the light-dark cycle, with the highest mortality rate at night (Ribalet et al, 2015). This could be explained by light-dark synchronized infection of Prochlorococcus by cyanophages, although synchronized grazing by protists is also possible (Ribalet et al, 2015).…”