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.

Keywords: SeaFlow; cell division; cyanobacteria; flow cytometry; mortality.

Fig. 1.

Temperature determines the rate of Prochlorococcus cell division in surface waters of the Northeast Pacific Ocean. (A) Daily averaged division rate of Prochlorococcus (division, d⁻¹, color scale), monthly averaged satellite-based sea surface temperature for October (°C, contour line), and Prochlorococcus ecotype composition (pie charts based on percent of each Prochlorococcus ecotype relative to total Prochlorococcus ecotypes represented in 16S rRNA gene amplicons from TAG sequencing; yellow, red, and green for eHLI, eHLII, and eLLI, respectively) during the northward cruise to California (4–9 October 2011) and southward cruise to Hawaii (29 October–2 November 2011). Daily division rates were calculated as the sum of hourly division rates over a 24-h period using a 1-h rolling window. (B) Relationship between daily division rates and surface temperature during the survey. Vertical gray bars represent SDs (n = 24).

Fig. 2.

Synchrony of Prochlorococcus mortality rates at high cell production rates. (A and B) Hourly averaged temperature (°C, gray line) and bulk chlorophyll a concentrations (µg/L, black line), (C and D) hourly averaged cell abundances (10⁶ cells/L, green line) and hourly averaged PAR at 5 m depth (µE/m² per second, gray line), and (E and F) hourly rates of cell production (10⁶ cells/L per hour, blue line) and cell mortality (10⁶ cells/L per hour, purple line) during the northward cruise to California (4–9 October 2011) (Left) and southward cruise to Hawaii (29 October–2 November 2011) (Right). Vertical gray bars represent SDs (n = 20 for temperature, chlorophyll a concentrations, PAR, and cell abundances, n = 24 for cell production and mortality rates). The gray regions indicate night. Horizontal red bars in A represent periods on station. Note that the left panels are shown according to chronology of sampling, as opposed to ascending sea surface temperature in Fig. 1B.

Fig. 3.

Light dependency of Prochlorococcus mortality forces. Modeled Prochlorococcus mortality rate (purple line), production rate (blue line), and cell abundance (green line). (A and C) Stable solution for a virus/host model (23) where the per-capita rates of virus infection (A) remain constant over the day/night cycle or (C) vary according to Prochlorococcus cell division rates. (B and D) Stable solution for a predator–prey model (24) where the per-capita rates of predation (B) remain constant over the day/night cycle or (D) vary according to light intensity. The gray regions indicate night.