Prolonged light exposure time enhances the photosynthetic investment in osmotrophic Ochromonas

Abstract

The photoperiod, as a critical external environmental signal, triggers a cascade of signaling responses in organisms that significantly affect photosynthetic efficiency and photomorphogenesis in autotrophs, while also influencing behavioral patterns and activity rhythms of heterotrophs. Despite its importance, the mechanisms by which mixotrophs respond to photoperiod changes remain largely unexplored. It is crucial for understanding metabolic plasticity how mixotrophs respond to light availability and make optimal decisions during diurnal transitions by regulating their autotrophic and osmotrophic pathways. Therefore, this study focused on Ochromonas gloeopara, a eukaryotic protist capable of both photoautotrophic and osmotrophic growth, aiming to explore the metabolic strategies of mixotrophs in response to changes in photoperiod. The results showed the following. (i) Under autotrophic conditions, the optimal photoperiod for photosynthetic efficiency in Ochromonas was approximately 12 h of light exposure, while prolonged light exposure beyond this duration reduced photosynthetic investment and efficiency, accompanied by an increase in heat dissipation to prevent photodamage. (ii) Under osmotrophic conditions, O. gloeopara adapted to prolonged light exposure by reducing. The reliance on external organic carbon sources and enhancing photosynthetic capacity, thereby shifting towards a more autotrophic metabolic mode. This study systematically elucidates the nutritional strategies of mixotrophic O. gloeopara in response to photoperiod changes at the levels of population dynamics, photosynthetic physiology, and carbon acquisition pathways, deepening our understanding of the response to photoperiodic changes in mixotrophs. These findings provide important theoretical insights for understanding the functional roles of mixotrophs in ecosystems and for accurately predicting changes in global carbon cycles.

Importance: Mixotrophs possess flexible metabolism modes and multiple ecological roles, making them sensitive to environmental changes. Due to their widespread distribution and unique nutritional strategy, they serve as key functional groups in marine and freshwater ecosystems, with significant roles in global biogeochemical cycles. Photoperiod, a critical environmental cue, regulates circadian rhythms and may influence the metabolic strategies of mixotrophs. Therefore, this study focused on how the mixotrophic microorganisms Ochromonas gloeopara adjusted autotrophic and osmotrophic pathways in response to photoperiodic changes. These findings highlight the metabolic flexibility of mixotrophic organisms in response to photoperiodic changes, providing new insight on how mixotrophs regulate the flow of materials and reshape the food web structures. This research offers valuable and innovative perspectives for understanding the functional roles of mixotrophic microorganisms in ecosystems, with important implications for improving the accuracy of global carbon cycle predictions.

Keywords: carbon acquisition; metabolic plasticity; osmotrophy; photoperiod; photosynthesis.

Fig 1

Population dynamics of O. gloeopara of different nutritional modes under different photoperiods. (a) Autotrophic O. gloeopara, (b) osmotrophic O. gloeopara, (c) heterotrophic O. gloeopara, and (d) the time for O. gloeopara to reach the maximum density.

Fig 2

Growth performances of O. gloeopara cultured at different metabolic modes under different photoperiods. (a) Population growth rates, (b) predicted slope of population growth rate with light exposure time, (c) dynamics of maximum population abundance with light exposure time, and (d) maximum values of maximum population of autotrophic and osmotrophic O. gloeopara and its corresponding light exposure time.

Fig 3

Morphology-related characteristics of O. gloeopara under different metabolic modes and photoperiods. (a) Chlorophyll content per cell, (b) cell volume, (c) micrographs of cell morphology, and (d) correlation analysis among photoperiods, chlorophyll content per cell, and cell volume.

Fig 4

Photosynthetic efficiency of O. gloeopara under different metabolic modes (a, c, e, and g) and the effect size of photoperiod on these indicators (b, d, f, and h).

Fig 5

Correlation among photoperiod (LT), nutritional modes (NM), photosynthetic efficiency, and population indicators of O. gloeopara.

Fig 6

Carbon utilization strategies of O. gloeopara under different photoperiod (time unit: h). Carbon acquisition rates of autotrophic and osmotrophic O. gloeopara under different light exposure time (a) and the change rate in carbon acquisition rates with light exposure time (b). AP, potential photosynthetic carbon fixation rate under autotrophic conditions; MP, potential photosynthetic carbon fixation rate under osmotrophic conditions of mixotrophs; MG, carbon acquired through phagotrophy of mixotrophs; MO, carbon acquired through osmotrophy of mixotrophs.

Fig 7

Carbon utilization strategies of O. gloeopara under different photoperiod (time unit: days). Carbon acquisition rates of autotrophic and osmotrophic O. gloeopara under different light exposure time (a) and the ratio of potential photosynthetic carbon fixation to total carbon acquisition (b). PC, potential carbon fixation rates by photosynthesis; TC, total of potential photosynthetic carbon fixation and carbon acquired through osmotrophy.