Diel oscillations in the feeding activity of heterotrophic and mixotrophic nanoplankton in the North Pacific Subtropical Gyre

Abstract

Daily oscillations in photosynthetically active radiation strongly influence the timing of metabolic processes in picocyanobacteria, but it is less clear how the light-dark cycle affects the activities of their consumers. We investigated the relationship between marine picocyanobacteria and nanoplanktonic consumers throughout the diel cycle to determine whether heterotrophic and mixotrophic protists (algae with phagotrophic ability) display significant periodicity in grazing pressure. Carbon biomass of Prochlorococcus and Synechococcus was estimated continuously from abundances and cell size measurements made by flow cytometry. Picocyanobacterial dynamics were then compared to nanoplankton abundances and ingestion of fluorescently labeled bacteria measured every 4 h during a 4 d survey in the North Pacific Subtropical Gyre. Grazing of the labeled bacteria by heterotrophic nanoplankton was significantly greater at night than during the day. The grazing activity of mixotrophic nanoplankton showed no diel periodicity, suggesting that they may feed continuously, albeit at lower rates than heterotrophic nanoplankton, to alleviate nutrient limitation in this oligotrophic environment. Diel changes in Prochlorococcus biomass indicated that they could support substantial growth of nanoplankton if those grazers are the main source of picocyanobacterial mortality, and that grazers may contribute to temporally stable abundances of picocyanobacteria.

Disentangling top-down drivers of mortality underlying diel population dynamics ofProchlorococcusin the North Pacific Subtropical Gyre

“…We note that the model predicted dynamics of Prochlorococcus , free virus abundance, heterotrophic nanoflagellate abundance, and the percentage of infected cells do not always recapitulate the magnitude of diel oscillations observed. This gap may point to direct light-mediated modulation of life history traits and behavior [16, 17, 18, 19, 20, 21], and/or unaccounted for feedback mechanisms in the model structure. Like our analysis of ECLIP, we find differences in parameter sets between the best fitting generalist and specialist ECLIPSS models that is then recapitulated via analysis of the full suite of coexisting LHS parameter sets (Supplementary Information, Figure S9 and S12-S15) Hence, rather than conclude that a particular parameter set provides the most explanatory power to observed patterns, we seek to identify mechanisms common to those parameter sets that fit the data nearly equally well.…”

“…Slides were stored at -20°C until analysis. Heterotrophic nanoplankton abundances were counted using epifluorescence microscopy from triplicate slides, and differentiated from photo/mixotrophic nanoplankton by the lack of chlorophyll a autofluorescence in plastidic structures when viewed under blue-light excitation [21].…”

“…Cyanobacterial population dynamics are influenced by both nutrients and light availability [2, 3, 4, 5, 6, 7, 8] as well as by density- and size-dependent feedback processes with other components of the community [9, 10, 11, 12, 13, 14, 15]. These interactions lead to diel oscillations, including in grazing rates, viral abundances, viral infection rates, and viral activity [16, 17, 18, 19, 20, 21]. The emergence of diel rhythms in abundances and process rates raises the question: how does light-driven growth of photoautotrophs over day-night cycles influence oscillations of other microbial populations and ecosystem processes?…”

“…Related work from this cruise using the cellular iPolony method estimates that viruses, despite being highly abundant, may contribute to approximately 5% or less of total Prochlorococcus cell losses per day [20]. Congruently, using quota based reasoning, grazing by heterotrophic nanoflagellates could potentially account for the majority of Prochlorococcus cell losses per day [21], but this method cannot rule out the potential for significantly lower rates of grazing. We note that cruise data show clear repeatable periodicity in average Prochlorococcus cell volume, which peaks close to dusk, and cell abundance, which peaks during nighttime.…”

“…We note that cruise data show clear repeatable periodicity in average Prochlorococcus cell volume, which peaks close to dusk, and cell abundance, which peaks during nighttime. Population abundances of heterotrophic nanoflagellates oscillate as does the fraction of cells infected by of T4- and T7-like viruses [20, 21]; suggesting the potential for emergent synchronization.…”