Phosphorus Deficiency Inhibits Cell Division But Not Growth in the Dinoflagellate Amphidinium carterae.

Meizhen Li,Chentao Guo,Xinguo Shi,Senjie Lin

doi:10.3389/fmicb.2016.00826

Meizhen Li, Chentao Guo + Show 2 more

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https://doi.org/10.3389/fmicb.2016.00826

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Abstract

Phosphorus (P) is an essential nutrient element for the growth of phytoplankton. How P deficiency affects population growth and the cell division cycle in dinoflagellates has only been studied in some species, and how it affects photosynthesis and cell growth remains poorly understood. In the present study, we investigated the impact of P deficiency on the cell division cycle, the abundance of the carbon-fixing enzyme Rubisco, and other cellular characteristics in the Gymnodiniales peridinin-plastid species Amphidinium carterae. We found that under P-replete condition, the cell cycle actively progressed in the culture in a 24-h diel cycle with daily growth rates markedly higher than the P-deficient cultures, in which cells were arrested in the G1 phase and cell size significantly enlarged. The results suggest that, as in previously studied dinoflagellates, P deficiency likely disenables A. carterae to complete DNA duplication or check-point protein phosphorylation. We further found that under P-deficient condition, overall photosystem II quantum efficiency (Fv/Fm ratio) and Rubisco abundance decreased but not significantly, while cellular contents of carbon, nitrogen, and proteins increased significantly. These observations indicated that under P-deficiency, this dinoflagellate was able to continue photosynthesis and carbon fixation, such that proteins and photosynthetically fixed carbon could accumulate resulting in continued cell growth in the absence of division. This is likely an adaptive strategy thereby P-limited cells can be ready to resume the cell division cycle upon resupply of phosphorus.

Highlights

Phosphorus (P) plays an essential role in cellular structure and function of living organisms because it is required in vital molecules such as nucleic acids (DNA, RNA), phospholipids, inositol triphosphate, reduced nicotinamide adenine dinucleotide (NADH) and its phosphorylated form (NADPH; both reducing equivalents), and adenosine triphosphate (ATP; energy currency)
The field population of K. brevis was shown to commence DNA synthesis in the light period and complete mitosis at the end of the dark period both in 16:8 and 12:12 light/dark cycles (Van Dolah and Leighfield, 1999). Different from these species, A. carterae cultures grown under the P-replete condition and 14:10 light/dark cycle in the present study exhibited the most active DNA synthesis in the middle of the light period following cell size increase, mitosis at dusk, and cytokinesis in the mid dark period
We found a circadian rhythm in Rubisco abundance in the P-replete A. carterae cultures despite the large within-treatment-group variations

Summary

Introduction

Phosphorus (P) plays an essential role in cellular structure and function of living organisms because it is required in vital molecules such as nucleic acids (DNA, RNA), phospholipids (membrane constituents), inositol triphosphate (signaling molecule), reduced nicotinamide adenine dinucleotide (NADH) and its phosphorylated form (NADPH; both reducing equivalents), and adenosine triphosphate (ATP; energy currency). Phytoplankton have evolved adaptive mechanisms to cope with the shortage of DIP (Lin et al, 2015), e.g., enhancing ability to take up low-abundance DIP by means of high affinity phosphate transporters (Orchard et al, 2009), scavenging P from dissolved organic phosphorus via the action of alkaline phosphatase and other hydrolytic enzymes (Benitez-Nelson and Buesseler, 1999; Reynolds et al, 2014), and decreasing phosphorus demand by substituting phospholipids with sulfolipids (Van Mooy et al, 2006, 2009) or accelerating phospholipid turnover to provide short term P supply (Martin et al, 2011)

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