Transcriptomic-Guided Phosphonate Utilization Analysis Unveils Evidence of Clathrin-Mediated Endocytosis and Phospholipid Synthesis in the Model Diatom,
            <i>Phaeodactylum tricornutum</i>

Shu, Huilin; You, Yunxiang; Wang, Hongwei; Wang, Jingtian; Li, Ling; Ma, Jian; Lin, Xin

doi:10.1128/msystems.00563-22

Cited by 8 publications

(8 citation statements)

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“…The other organic matters can also be an alternative nutrient supply, especially for mixotrophic dinoflagellates which is able to digest the intact cell of the prey (Zhang et al, 2011; Jeong et al, 2021;). Our previous work revealed clathrin-mediated endocytosis in the uptake and utilization of DOP by Phaeodactylum tricornutum (Shu et al, 2022), and this mechanism was also recently reported in Symbiodiniacean species (Dinophyta) (Li et al, 2023). Besides organic nitrogen and phosphorus, dissolved metal ions (such as bioactive iron and copper), vitamins, and growth-promoting factors are accessible to dinoflagellates as well (Laglera and Berg, 2009; wells et al, 2015; Amin et al, 2015; Seymour et al, 2017).…”

Section: Discussionsupporting

confidence: 73%

StimulatedProrocentrum donghaiensecell growth byin-situmariculture dissolved organic matter

Wang,

Wu,

et al. 2024

Preprint

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Mixotrophic dinoflagellates frequently cause harmful algal blooms (HAB) in eutrophic mariculture waters that contain diverse excreted dissolved organic matter (DOM). The phagotrophy and the utilization of single organic small molecules have been extensively investigated in the bloom-forming mixotrophic dinoflagellates. However, their ability to utilize thein-situDOM via absorbtrophy still remains unexplored. Here we examined the growth promotion effect of thein-situmariculture DOM onProrocentrum donghaiense, a representative HAB-forming species in coastal waters. Our results showed that the cell growth and photosynthesis ofP. donghaiensewere significantly promoted underin-situDOM culture conditions. Additionally, parallel cultures were set up to disclose the potential role of the bacterioplankton in the free-living community (helper), where they aid in the remineralization of thein-situDOM, and the phycosphere community (competitor), where they compete against the algal host to acquire nutrients from thein-situDOM. Meanwhile, we determined the cellular stoichiometry under different culture conditions, showing that mariculture DOM can shape cellular stoichiometry significantly. Elevated cellular N (84.96%) and P (48.3%) were observed in spring DOM groups compared with the control groups. For the first time, this study quantifies the efficient utilization of thein-situDOM via absorbtrophy, indicating the vital role in the outbreak and maintenance of HAB events.

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Section: Discussionsupporting

confidence: 73%

StimulatedProrocentrum donghaiensecell growth byin-situmariculture dissolved organic matter

Wang,

Wu,

et al. 2024

Preprint

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“…In C. goreaui , the clathrin‐mediated endocytosis was upregulated during PA utilization (Figure 5b). Recently, clathrin‐mediated endocytosis has been reported to perform the phosphonate uptake in the diatom P. tricornutum (Shu et al, 2022), suggesting that endocytosis might also be employed to transport PA into C. goreaui cells. Given that endocytosis has an energy cost, the upregulation of glycolysis and TCA cycle in the PA‐grown cells might provide the energy needed (Figure 4a).…”

Section: Discussionmentioning

confidence: 99%

Phosphorus nutrition strategies in a Symbiodiniacean species: Implications in coral‐alga symbiosis facing increasing phosphorus deficiency in future warmer oceans

Li,

Zhang,

et al. 2023

Global Change Biology

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Coral reefs thrive in the oligotrophic ocean and rely on symbiotic algae to acquire nutrients. Global warming is projected to intensify surface ocean nutrient deficiency and anthropogenic discharge of wastes with high nitrogen (N): phosphorus (P) ratios can exacerbate P nutrient limitation. However, our understanding on how symbiotic algae cope with P deficiency is limited. Here, we investigated the responses of a coral symbiotic species of Symbiodiniaceae, Cladocopium goreaui, to P‐limitation by examining its physiological performance and transcriptomic profile. Under P stress, C. goreaui exhibited decreases in algal growth, photosynthetic efficiency, and cellular P content but enhancement in carbon fixation, N assimilation, N:P ratio, and energy metabolism, with downregulated expression of carbohydrate exporter genes. Besides, C. goreaui showed flexible mechanisms of utilizing different dissolved organic phosphorus to relieve P deficiency. When provided glycerol phosphate, C. goreaui hydrolyzed it extracellularly to produce phosphate for uptake. When grown on phytate, in contrast, C. goreaui upregulated the endocytosis pathway while no dissolved inorganic phosphorus was released into the medium, suggesting that phytate was transported into the cell, potentially via the endocytosis pathway. This study sheds light on the survival strategies of C. goreaui and potential weakening of its role as an organic carbon supplier in P‐limited environments, underscoring the importance of more systematic investigation on future projections of such effects.

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“…In addition, it is interesting to find that the phagosome pathway was downregulated in both the ATP and G6P groups in our study (Figure 5). Recently, P. tricornutum was reported to be able to utilize 2-aminoethylphosphonate as the sole source of P (Shu et al, 2022). Transcriptomic analysis in that study indicated that the phagosome pathway (specifically, clathrin-mediated endocytosis) was upregulated, suggesting that this phosphonate might be taken up by this alga via endocytosis.…”

Section: Discussionmentioning

confidence: 95%

“…Therefore, P. tricornutum is a good model species for studying the molecular mechanism of DOP utilization in diatoms. Recently, the bioavailability and utilization mechanisms of phytic acid and 2aminoethylphosphonate have been conducted successively in P. tricornutum (Li et al, 2022;Shu et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Transcriptomics and physiological analyses unveil the distinct mechanisms of ATP and glucose-6-phosphate utilization in Phaeodactylum tricornutum

et al. 2023

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Phosphoesters are a dominant component of marine dissolved organic phosphorus (DOP) and an important source of the phosphorus nutrient for phytoplankton, but the molecular mechanisms of their utilization by phytoplankton are divergent and poorly understood. In this study, we used the model diatom Phaeodactylum tricornutum to investigate and compare the utilization mechanisms of two different phosphoesters, adenosine triphosphate (ATP) and glucose-6-phosphate (G6P). We found that ATP and G6P can both be efficiently used to support the growth of P. tricornutum. Cells grown on ATP or G6P showed lower pigment contents and photosynthetic rates but higher cellular lipids relative to those grown on NaH2PO4 (DIP). Surprisingly, in neither the ATP nor the G6P group were significant increases in whole-cell alkaline phosphatase (AP) activity detected, suggesting that utilization of both DOPs was not reliant on extracellular AP. Yet, ATP-grown cultures released DIP into the medium (i.e., ATP hydrolyzed extracellularly) whereas G6P-grown cultures did not. Furthermore, transcriptomic and RT-qPCR results showed that the gene encoding 5’ nucleotidase (5NT) in the ATP group and PhoD in the G6P group was upregulated. These results indicated that different pathways are involved in the use of these two DOPs, with ATP being hydrolyzed extracellularly likely by 5NT (PHATRDRAFT_44177) to release DIP for uptake, and G6P being directly absorbed and hydrolyzed intracellularly likely by PhoD (PHATRDRAFT_45757). Nevertheless, P. tricornutum under ATP and G6P conditions showed more similar transcriptomic profiles to each other than either compared to DIP-grown cultures, indicating similar metabolic functions of these two DOPs. These findings demonstrate that despite the high similarity in transcriptomic response to ATP and G6P conditions, the utilization mechanisms of these phosphoesters in the same species can be totally different, and the lack of AP activity does not necessarily signal the absence of DIP deficiency or the absence of DOP utilization.

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Transcriptomic-Guided Phosphonate Utilization Analysis Unveils Evidence of Clathrin-Mediated Endocytosis and Phospholipid Synthesis in the Model Diatom, Phaeodactylum tricornutum

Abstract: Phosphonates contribute ~25% of total dissolved organic phosphorus in the ocean, and are found to be important for marine phosphorus biogeochemical cycle. As a type of biogenic phosphonate produced by microorganisms, 2-aminoethylphosphonic acid (2-AEP) widely exists in the ocean.

Cited by 8 publications

References 81 publications

StimulatedProrocentrum donghaiensecell growth byin-situmariculture dissolved organic matter

StimulatedProrocentrum donghaiensecell growth byin-situmariculture dissolved organic matter

Phosphorus nutrition strategies in a Symbiodiniacean species: Implications in coral‐alga symbiosis facing increasing phosphorus deficiency in future warmer oceans

Transcriptomics and physiological analyses unveil the distinct mechanisms of ATP and glucose-6-phosphate utilization in Phaeodactylum tricornutum

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