Characterizing the Status of Energetic Metabolism of Dinoflagellate Resting Cysts Under Mock Conditions of Marine Sediments Via Physiological and Transcriptional Measurements

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2022 Dec 11

PMID 36499364

Authors

Fengting Li

Caixia Yue

Yunyan Deng

Ying Zhong Tang

Affiliations

Soon will be listed here.

Abstract

Similar to the seeds of higher plants, resting cysts, a non-motile, benthic, and dormant stage in the life history of many dinoflagellate species, play vital roles via germination in the seasonal dynamics and particularly the initiation of harmful algal blooms (HABs) of dinoflagellates. It is thus crucial for resting cysts to balance between the energetic catabolism for viability maintenance and the energy preservation for germination during their dormancy. Despite this importance, studies on how resting cysts of dinoflagellates accomplish energetic metabolism in marine sediment have been virtually absent. In this study, using the cosmopolitan HABs-causing species as a representative, we measured the transcriptional activity of the most efficient pathway of the energy catabolism tricarboxylic acid (TCA) cycle, cell viability (via neutral red staining), and the cellular ATP content of resting cysts under a set of mock conditions in marine sediments (e.g., 4 °C, darkness, and anoxia) for a maximum period of one year. Based on the correlation analyses among the expression levels of genes, cyst viability, and ATP content, we revealed that the TCA cycle was still a crucial pathway of energetic catabolism for resting cysts under aerobic conditions, and its expression was elevated at higher temperatures, light irradiation, and the early stage of dormancy. Under anaerobic conditions, however, the TCA cycle pathway ceased expression in resting cysts, as also supported by ATP measurements. Our results have laid a cornerstone for the comprehensive revelation of the energetic metabolism and biochemical processes of dormancy of resting cysts in marine sediments.

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References

Lemaitre T, Urbanczyk-Wochniak E, Flesch V, Bismuth E, Fernie A, Hodges M . NAD-dependent isocitrate dehydrogenase mutants of Arabidopsis suggest the enzyme is not limiting for nitrogen assimilation. Plant Physiol. 2007; 144(3):1546-58. PMC: 1914144. DOI: 10.1104/pp.107.100677. View

Akram M . Citric acid cycle and role of its intermediates in metabolism. Cell Biochem Biophys. 2013; 68(3):475-8. DOI: 10.1007/s12013-013-9750-1. View

Su J, Yang X, Zheng T, Hong H . An efficient method to obtain axenic cultures of Alexandrium tamarense--a PSP-producing dinoflagellate. J Microbiol Methods. 2007; 69(3):425-30. DOI: 10.1016/j.mimet.2006.07.005. View

DeBerardinis R, Mancuso A, Daikhin E, Nissim I, Yudkoff M, Wehrli S . Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci U S A. 2007; 104(49):19345-50. PMC: 2148292. DOI: 10.1073/pnas.0709747104. View

Yue C, Chai Z, Hu Z, Shang L, Deng Y, Tang Y . Deficiency of nitrogen but not phosphorus triggers the life cycle transition of the dinoflagellate Scrippsiella acuminata from vegetative growth to resting cyst formation. Harmful Algae. 2022; 118:102312. DOI: 10.1016/j.hal.2022.102312. View

Pietrocola F, Galluzzi L, Bravo-San Pedro J, Madeo F, Kroemer G . Acetyl coenzyme A: a central metabolite and second messenger. Cell Metab. 2015; 21(6):805-21. DOI: 10.1016/j.cmet.2015.05.014. View

Jeong H, Kang H, Lim A, Jang S, Lee K, Lee S . Feeding diverse prey as an excellent strategy of mixotrophic dinoflagellates for global dominance. Sci Adv. 2021; 7(2). PMC: 7793574. DOI: 10.1126/sciadv.abe4214. View

Heisler J, Glibert P, Burkholder J, Anderson D, Cochlan W, Dennison W . Eutrophication and Harmful Algal Blooms: A Scientific Consensus. Harmful Algae. 2017; 8(1):3-13. PMC: 5543702. DOI: 10.1016/j.hal.2008.08.006. View

Nagy B, Polak M, Ozohanics O, Zambo Z, Szabo E, Hubert A . Structure of the dihydrolipoamide succinyltransferase (E2) component of the human alpha-ketoglutarate dehydrogenase complex (hKGDHc) revealed by cryo-EM and cross-linking mass spectrometry: Implications for the overall hKGDHc structure. Biochim Biophys Acta Gen Subj. 2021; 1865(6):129889. DOI: 10.1016/j.bbagen.2021.129889. View

10.

Rudic R, McNamara P, Curtis A, Boston R, Panda S, Hogenesch J . BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol. 2004; 2(11):e377. PMC: 524471. DOI: 10.1371/journal.pbio.0020377. View

11.

Deng Y, Hu Z, Shang L, Chai Z, Tang Y . Transcriptional Responses of the Heat Shock Protein 20 (Hsp20) and 40 (Hsp40) Genes to Temperature Stress and Alteration of Life Cycle Stages in the Harmful Alga (Dinophyceae). Biology (Basel). 2020; 9(11). PMC: 7700488. DOI: 10.3390/biology9110408. View

12.

Lin S . Genomic understanding of dinoflagellates. Res Microbiol. 2011; 162(6):551-69. DOI: 10.1016/j.resmic.2011.04.006. View

13.

Gibson K, Laver W, Neuberger A . Initial stages in the biosynthesis of porphyrins. 2. The formation of delta-aminolaevulic acid from glycine and succinyl-coenzyme A by particles from chicken erythrocytes. Biochem J. 1958; 70(1):71-81. PMC: 1196628. DOI: 10.1042/bj0700071. View

14.

Bravo I, Figueroa R . Towards an Ecological Understanding of Dinoflagellate Cyst Functions. Microorganisms. 2016; 2(1):11-32. PMC: 5029505. DOI: 10.3390/microorganisms2010011. View

15.

Li F, Yang A, Hu Z, Lin S, Deng Y, Tang Y . Probing the Energetic Metabolism of Resting Cysts under Different Conditions from Molecular and Physiological Perspectives in the Harmful Algal Blooms-Forming Dinoflagellate . Int J Mol Sci. 2021; 22(14). PMC: 8307125. DOI: 10.3390/ijms22147325. View

16.

Tang Y, Gu H, Wang Z, Liu D, Wang Y, Lu D . Exploration of resting cysts (stages) and their relevance for possibly HABs-causing species in China. Harmful Algae. 2021; 107:102050. DOI: 10.1016/j.hal.2021.102050. View

17.

Fernie A, Carrari F, Sweetlove L . Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr Opin Plant Biol. 2004; 7(3):254-61. DOI: 10.1016/j.pbi.2004.03.007. View

18.

Wang Z, Xie C, Zhang J, Ji S, Zhao J, Nie X . The responses of Scrippsiella acuminata to the stresses of darkness: antioxidant activities and formation of pellicle cysts. Harmful Algae. 2022; 115:102239. DOI: 10.1016/j.hal.2022.102239. View

19.

Gross S, Cairns R, Minden M, Driggers E, Bittinger M, Jang H . Cancer-associated metabolite 2-hydroxyglutarate accumulates in acute myelogenous leukemia with isocitrate dehydrogenase 1 and 2 mutations. J Exp Med. 2010; 207(2):339-44. PMC: 2822606. DOI: 10.1084/jem.20092506. View

20.

Akimoto H, Kinumi T, Ohmiya Y . Circadian rhythm of a TCA cycle enzyme is apparently regulated at the translational level in the dinoflagellate Lingulodinium polyedrum. J Biol Rhythms. 2005; 20(6):479-89. DOI: 10.1177/0748730405280811. View