Multi-Omics Profiling Reveals Resource Allocation and Acclimation Strategies to Temperature Changes in a Marine Dinoflagellate

Zhang, Hao; Gu, Bowei; Zhou, Youping; Ma, Xiao; Liu, Tianqi; Xu, Hongkai; Xie, Zhang-Xian; Liu, Kailin; Wang, Dazhi; Xia, Xiaomin

doi:10.1128/aem.01213-22

Cited by 10 publications

(22 citation statements)

References 78 publications

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“…Thus, the model predicts a decrease in the concentration of ribosomes with increasing temperatures (fig. S6), in agreement with empirical data (Table 1) (19,27,28) and previous modeling results (28). Our findings build on the modeling work by Toseland et al (28) to show that the decrease in ribosomes is ultimately mediated by the need to invest more in photosystems and repair proteins with warming as a result of energetic imbalances.…”

Section: Shifts In Investment With Increasing Temperaturessupporting

confidence: 91%

“…4A). This hypothesis is supported by proteomic analysis that found nitrogen transporters to be up-regulated with warming even under replete nutrient conditions (Table 1) (19,30).…”

Section: Changes In Cell Size Due To Warmingmentioning

confidence: 76%

“…Thus, as temperatures warm, a cell must increase the relative investment in nutrient transporters, as supported by previous proteomic analyses (19,30), to keep pace with increased metabolic demands. In addition, at higher temperatures, cells switch from unsaturated to saturated lipids (24), requiring a higher relative investment in the synthesis of saturated lipids (18,19,27) to maintain membrane integrity, which also decreases the optimal cell size.…”

Section: Why Do Phytoplankton Acclimate To Warming By Decreasing Cell...mentioning

confidence: 83%

“…Thus, the actual rate of damage v d depends on k d (Eq. 19), on the concentration of photosystems p p , and on the concentration of stored lipids c tag…”

Section: Photosynthesismentioning

confidence: 99%

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Mechanistic constraints on the trade-off between photosynthesis and respiration in response to warming

Leles,

Levine

2023

Sci. Adv.

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Phytoplankton are responsible for half of all oxygen production and drive the ocean carbon cycle. Metabolic theory predicts that increasing global temperatures will cause phytoplankton to become more heterotrophic and smaller. Here, we uncover the metabolic trade-offs between cellular space, energy, and stress management driving phytoplankton thermal acclimation and how these might be overcome through evolutionary adaptation. We show that the observed relationships between traits such as chlorophyll, lipid content, C:N, and size can be predicted on the basis of the metabolic demands of the cell, the thermal dependency of transporters, and changes in membrane lipids. We suggest that many of the observed relationships are not fixed physiological constraints but rather can be altered through adaptation. For example, the evolution of lipid metabolism can favor larger cells with higher lipid content to mitigate oxidative stress. These results have implications for rates of carbon sequestration and export in a warmer ocean.

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Section: Shifts In Investment With Increasing Temperaturessupporting

confidence: 91%

“…4A). This hypothesis is supported by proteomic analysis that found nitrogen transporters to be up-regulated with warming even under replete nutrient conditions (Table 1) (19,30).…”

Section: Changes In Cell Size Due To Warmingmentioning

confidence: 76%

Section: Why Do Phytoplankton Acclimate To Warming By Decreasing Cell...mentioning

confidence: 83%

“…Thus, the actual rate of damage v d depends on k d (Eq. 19), on the concentration of photosystems p p , and on the concentration of stored lipids c tag…”

Section: Photosynthesismentioning

confidence: 99%

See 2 more Smart Citations

Mechanistic constraints on the trade-off between photosynthesis and respiration in response to warming

Leles,

Levine

2023

Sci. Adv.

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“…(b) Cellular nitrogen content (Zhang et al, 2015; Jing et al, 2017; Chen et al, 2019). (c) C/N ratios (Cai et al, 2016; Liu, 2018; Chen et al, 2019; Zhang et al, 2022). (d) C/N ratios in this study and of surface sediments in some bloom areas (Hu et al, 2014; Chao et al, 2017; Wang et al, 2018; Rodil et al, 2020; Wang, 2020b; Likumahua et al, 2021; Xu, 2022; Beltran-Perez et al, 2023).…”

Section: Resultsmentioning

confidence: 99%

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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Differential impacts of temperature increase on prokaryotes across temperature regimes in subtropical coastal waters: insights from field experiments

Gu,

Ma,

Chen

et al. 2024

Limnology & Oceanography

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Prokaryotic communities play a dominant role in driving biogeochemical cycling in marine ecosystems. How short‐term temperature increase impacts prokaryotes in subtropical coastal waters is still largely unknown. Here, 14 field experiments were conducted to investigate the response of prokaryotes in subtropical coastal waters to temperature increases of 3°C and 6°C, encompassing a range of ambient temperatures from 17°C to 31°C. We found that responses of prokaryotic growth, grazing pressure, community, and transcriptomes to increased temperatures were largely affected by ambient temperatures. Increased temperatures enhanced the growth rate and grazing pressure of heterotrophic prokaryotes when ambient temperatures were below 26–28°C. The increased temperatures had greater negative effects on the grazing rate compared to the growth rate; therefore, the abundance of heterotrophic prokaryotes generally increased after temperature increase across all temperature regimes. Metatranscriptomics analysis showed that at an ambient temperature of 30°C, genes involved in the adenosine triphosphate synthase were significantly downregulated by the increased temperature. This could be a major factor contributing to the decreased prokaryotic growth rate. In comparison, autotrophic prokaryotes (Synechococcus) exhibited better performance in response to elevated temperatures, thriving up to 35°C, beyond which their growth rate experienced a dramatic decline. When exposing to extremely high temperatures, genes involved in photosynthesis significantly decreased. These findings highlight the differential ecological impacts of temperature increase on prokaryotic communities, varying across different ambient temperatures and taxa in subtropical coastal waters.

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Multi-Omics Profiling Reveals Resource Allocation and Acclimation Strategies to Temperature Changes in a Marine Dinoflagellate

Abstract: Marine phytoplankton is one of the most important nodes in global biogeochemical cycle. Deciphering temperature-associated marine phytoplankton cell stoichiometric changes and the underlying molecular mechanisms are therefore of great ecological concerns.

Cited by 10 publications

References 78 publications

Mechanistic constraints on the trade-off between photosynthesis and respiration in response to warming

Mechanistic constraints on the trade-off between photosynthesis and respiration in response to warming

StimulatedProrocentrum donghaiensecell growth byin-situmariculture dissolved organic matter

Differential impacts of temperature increase on prokaryotes across temperature regimes in subtropical coastal waters: insights from field experiments

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