P-Limitation Promotes Carbon Accumulation and Sinking of Emiliania huxleyi Through Transcriptomic Reprogramming

Global warming is expected to cause decreases in nutrient availability, photosynthesis, and potentially carbon export in the ocean. But how, and by what molecular mechanisms, nutrient limitation affects biological pump (BP) efficiency of phytoplankton are poorly understood. Here, using transcriptomi...

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Main Authors: Cong Wang, Jingtian Wang, Ling Li, Yujie Wang, Senjie Lin
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2022.860222/full
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author Cong Wang
Cong Wang
Cong Wang
Jingtian Wang
Jingtian Wang
Ling Li
Ling Li
Yujie Wang
Yujie Wang
Senjie Lin
Senjie Lin
Senjie Lin
author_facet Cong Wang
Cong Wang
Cong Wang
Jingtian Wang
Jingtian Wang
Ling Li
Ling Li
Yujie Wang
Yujie Wang
Senjie Lin
Senjie Lin
Senjie Lin
author_sort Cong Wang
collection DOAJ
description Global warming is expected to cause decreases in nutrient availability, photosynthesis, and potentially carbon export in the ocean. But how, and by what molecular mechanisms, nutrient limitation affects biological pump (BP) efficiency of phytoplankton are poorly understood. Here, using transcriptomics, miRNAomics, and physiological measurements, we report that phosphorus (P)-limitation increased cellular carbon and calcium contents and sinking rate of the cosmopolitan phytoplankton Emiliania huxleyi. Under P-limitation, when photosynthesis was depressed, there were substantial increases in cellular organic (3.4-fold) and inorganic (fivefold) carbon contents due to cell division arrest and, as our transcriptomic data suggest, CO2 incorporation into C4 compounds. Furthermore, calcification was increased by 46% through transcriptional and epigenetic regulations. An increase in sinking rate by 37-44% was detected. Although calcification releases equivalent amounts of CO2, the considerable increase in cellular carbon content and sinking rate far outweighed the CO2 release, leading to an elevated efficiency of carbon export by E. huxleyi, which would partially offset the decrease in BP capacity resulting from lower growth rate under P deficiency. However, how the observed sinking rate and its increase under P limitation on the laboratory cultures will translate into BP efficiency still requires further examination using in situ or mesocosm experiments.
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spelling doaj.art-9303672da1c9487bb00ec8c49ae06fff2022-12-22T00:30:20ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452022-05-01910.3389/fmars.2022.860222860222P-Limitation Promotes Carbon Accumulation and Sinking of Emiliania huxleyi Through Transcriptomic ReprogrammingCong Wang0Cong Wang1Cong Wang2Jingtian Wang3Jingtian Wang4Ling Li5Ling Li6Yujie Wang7Yujie Wang8Senjie Lin9Senjie Lin10Senjie Lin11State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, ChinaCollege of the Environment and Ecology, Xiamen University, Xiamen, ChinaCollege of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, ChinaCollege of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, ChinaCollege of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, ChinaCollege of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, ChinaCollege of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaDepartment of Marine Sciences, University of Connecticut, Groton, CT, United StatesGlobal warming is expected to cause decreases in nutrient availability, photosynthesis, and potentially carbon export in the ocean. But how, and by what molecular mechanisms, nutrient limitation affects biological pump (BP) efficiency of phytoplankton are poorly understood. Here, using transcriptomics, miRNAomics, and physiological measurements, we report that phosphorus (P)-limitation increased cellular carbon and calcium contents and sinking rate of the cosmopolitan phytoplankton Emiliania huxleyi. Under P-limitation, when photosynthesis was depressed, there were substantial increases in cellular organic (3.4-fold) and inorganic (fivefold) carbon contents due to cell division arrest and, as our transcriptomic data suggest, CO2 incorporation into C4 compounds. Furthermore, calcification was increased by 46% through transcriptional and epigenetic regulations. An increase in sinking rate by 37-44% was detected. Although calcification releases equivalent amounts of CO2, the considerable increase in cellular carbon content and sinking rate far outweighed the CO2 release, leading to an elevated efficiency of carbon export by E. huxleyi, which would partially offset the decrease in BP capacity resulting from lower growth rate under P deficiency. However, how the observed sinking rate and its increase under P limitation on the laboratory cultures will translate into BP efficiency still requires further examination using in situ or mesocosm experiments.https://www.frontiersin.org/articles/10.3389/fmars.2022.860222/fullglobal warmingphosphorus-limitationEmiliania huxleyibiological pump efficiencymolecular mechanisms
spellingShingle Cong Wang
Cong Wang
Cong Wang
Jingtian Wang
Jingtian Wang
Ling Li
Ling Li
Yujie Wang
Yujie Wang
Senjie Lin
Senjie Lin
Senjie Lin
P-Limitation Promotes Carbon Accumulation and Sinking of Emiliania huxleyi Through Transcriptomic Reprogramming
Frontiers in Marine Science
global warming
phosphorus-limitation
Emiliania huxleyi
biological pump efficiency
molecular mechanisms
title P-Limitation Promotes Carbon Accumulation and Sinking of Emiliania huxleyi Through Transcriptomic Reprogramming
title_full P-Limitation Promotes Carbon Accumulation and Sinking of Emiliania huxleyi Through Transcriptomic Reprogramming
title_fullStr P-Limitation Promotes Carbon Accumulation and Sinking of Emiliania huxleyi Through Transcriptomic Reprogramming
title_full_unstemmed P-Limitation Promotes Carbon Accumulation and Sinking of Emiliania huxleyi Through Transcriptomic Reprogramming
title_short P-Limitation Promotes Carbon Accumulation and Sinking of Emiliania huxleyi Through Transcriptomic Reprogramming
title_sort p limitation promotes carbon accumulation and sinking of emiliania huxleyi through transcriptomic reprogramming
topic global warming
phosphorus-limitation
Emiliania huxleyi
biological pump efficiency
molecular mechanisms
url https://www.frontiersin.org/articles/10.3389/fmars.2022.860222/full
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