Osmotrophy of dissolved organic compounds by coccolithophore populations: Fixation into particulate organic and inorganic carbon

Abstract

Coccolithophores are typically thought of as photoautotrophs, yet a few genera inhabit sub-euphotic environments with insufficient light for photosynthesis, suggesting that other carbon acquisition strategies are likely. Field experiments were performed in the northwest Atlantic (a region with potentially abundant coccolithophores). Phytoplankton populations were incubated with 14 C-labeled dissolved organic carbon (DOC) compounds, acetate, mannitol, and glycerol. Coccolithophores were sorted from these populations 24 hours later using flow cytometry, and DOC uptake was measured. DOC uptake rates were as high as 10 −15 moles cell −1 day −1 , slow relative to photosynthesis rates (10 −12 moles cell −1 day −1 ). Growth rates on the organic compounds were low, suggesting that osmotrophy plays more of a survival strategy in low-light situations. Assimilated DOC was found in both particulate organic carbon and calcite coccoliths (particulate inorganic carbon), suggesting that osmotrophic uptake of DOC into coccolithophore calcite is a small but notable part of the biological carbon pump and alkalinity pump paradigms.

Phagocytosis in Marine Coccolithophore Gephyrocapsa huxleyi: Comparison between Calcified and Non-Calcified Strains

“…Furthermore, our flow cytometry results indicate that darkness could significantly affect the phagocytosis capability of the haploid non-calcified phase (Figure 4). It is believed that coccolithophores are able to survive in low light or even dark conditions through osmotrophy [40,65] and phagotrophy [38]. Our research further supported the potential of phagocytosis as a nutritional source for G. huxleyi, especially in the dark.…”

“…In contrast to the calcified strain, the non-calcified strain, lacking coccoliths and possessing two flagella [28][29][30], does not participate in the carbonate counter pump with much less contribution to the carbon pump into depth. However, in the deeper twilight zone, the phagotrophic nutritional pathway observed in the present study in addition to the previously reported osmotrophic pathway [40,65], may together benefit coccolithophore survival under energy-limited low light and dark conditions. [77,78].…”

“…the calcified strain (125,952) than in the non-calcified strain (65,225), with the calcified strain exhibiting DNA content approximately twice that of the non-calcified strain (Figure 2b).…”

“…In our investigation, the particle organic carbon can be phagocytosed to a higher percentage in the non-calcified phase than the calcified phase in the dark as compared to the light condition. Dissolved organic carbon (DOC) has been reported to be utilized by coccolithophores with osmotrophy in low light [39,65]. The physiological differences in terms of growth rate, cell diameter, cellular POC, cellular protein, and sinking rate are also listed (The relative font size indicates the relative magnitude of each physiological metric between the two phases) [32].…”

Role of Syndiniales parasites in depth-specific networks and carbon flux in the oligotrophic ocean

“…Spores may survive without their preferred hosts by widening their host range, becoming dormant inside host cysts [ 69 ], or acquiring alternative energy sources (e.g., uptake of DOM). Osmotrophy of DOM has been shown in haptophytes [ 77 ], which warrants its investigation in other protist groups such as Syndiniales that may possibly utilize DOM to survive under host-limited conditions. Lastly, Syndiniales may reach deep waters through convective mixing [ 42 , 78 ], either directly or on particles.…”