The role of zinc in the adaptive evolution of polar phytoplankton

Ye, Naihao; Han, Wentao; Toseland, Andrew; Wang, Ying; Fan, Xiao Nan; Xu, De-Xiang; Oosterhout, Cock van; Aslam, Shazia; Barry, Kerrie; Beszteri, Bánk; Brussaard, Corina P. D.; Clum, Alicia; Copeland, Alex; Daum, Chris; Duncan, Anthony; Eloe‐Fadrosh, Emiley A.; Fong, Allison A.; Foster, Brian; Foster, Bryce; Ginzburg, Michael; Ivanova, Natalia; Kyrpides, Nikos; Martin, Kara; Moulton, Vincent; Mukherjee, Supratim; Palaniappan, Krishnaveni; Reddy, T. B. K.; Roux, Simon; Schmidt, Katrin; Strauss, Jan; Timmermans, Klaas R.; Tringe, Susannah G.; Underwood, Graham J. C.; Valentin, Klaus; Poll, Willem H. van de; Varghese, Neha; Grigoriev, Igor V.; Tagliabue, Alessandro; Zhang, Jian; Zhang, Yan; Ma, Jian; Qiu, Huan; Li, Youxun; Zhang, Xiaowen; Möck, Thomas

doi:10.1038/s41559-022-01750-x

Cited by 21 publications

(13 citation statements)

References 67 publications

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“…Furthermore, functional insights based on the identification of protein families (Pfams) in prokaryotic MAGs revealed that the central Arctic Ocean is a treasure trove for discovering novel biology which likely has evolved because of adaptive processes required to thrive in this harsh environment ( Fig 2C ). Previous work corroborates the idea that life in polar oceans is characterised by unifying biological principles that are polar specific [ 11 ]. However, their discovery is still in its infancy.…”

Section: Resources and Tools For Revealing The Life Of Biological Com...supporting

confidence: 79%

Multiomics in the central Arctic Ocean for benchmarking biodiversity change

Möck

Boulton²,

Balmonte³

et al. 2022

PLoS Biol

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Section: Resources and Tools For Revealing The Life Of Biological Com...supporting

confidence: 79%

Multiomics in the central Arctic Ocean for benchmarking biodiversity change

Möck

Boulton²,

Balmonte³

et al. 2022

PLoS Biol

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“…Each of these behaviors have been observed in the open ocean diatom T. oceanica (Sunda & Huntsman, 1983 , 1986 , 2000 ). Corresponding experiments have not been performed for Antarctic species thus far, but polar lineages may have a greater ability to store and utilize intracellular Zn (Ye et al., 2022 ). As a result, R Zn is set equal to one in the standard version of the model, which indicates no downregulation of Mn uptake in response to high Q Zn .…”

Section: Methodsmentioning

confidence: 99%

Manganese Limitation of Phytoplankton Physiology and Productivity in the Southern Ocean

Hawco

Tagliabue

Twining

2022

Global Biogeochemical Cycles

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Although iron and light are understood to regulate the Southern Ocean biological carbon pump, observations have also indicated a possible role for manganese. Low concentrations in Southern Ocean surface waters suggest manganese limitation is possible, but its spatial extent remains poorly constrained and direct manganese limitation of the marine carbon cycle has been neglected by ocean models. Here, using available observations, we develop a new global biogeochemical model and find that phytoplankton in over half of the Southern Ocean cannot attain maximal growth rates because of manganese deficiency. Manganese limitation is most extensive in austral spring and depends on phytoplankton traits related to the size of photosynthetic antennae and the inhibition of manganese uptake by high zinc concentrations in Antarctic waters. Importantly, manganese limitation expands under the increased iron supply of past glacial periods, reducing the response of the biological carbon pump. Overall, these model experiments describe a mosaic of controls on Southern Ocean productivity that emerge from the interplay of light, iron, manganese and zinc, shaping the evolution of Antarctic phytoplankton since the opening of the Drake Passage.

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“…The contributions of diatoms to primary production is even greater in specific oceanic regions, including the nutrient-rich and highly productive waters at high latitudes (i.e., the Arctic and Antarctic Southern Oceans) (27). Diatoms within polar environments are exposed to multiple photo-physiological stressors such as low environmental temperatures, limitations of key nutrients including iron, zinc, and cobalamin, and elongated photoperiods ranging from continuous illumination in the polar summer to continuous darkness in the winter (24, 26, 28, 29). Previous genomic and physiological studies of model diatoms, such as the transformable species Phaeodactylum tricornutum , have identified multiple strategies that allow diatoms to tolerate photo-stress, including extensive capacities for non-photochemical quenching pathways displaying different features than in plants or in primary red algae (30, 31), and complex strategies for the acquisition, storage and recycling of cellular iron (32), which may provide new strategies for metabolic engineering of enhanced photosynthetic activity in plants (33).…”

Section: Introductionmentioning

confidence: 99%

Complementary environmental analysis and functional characterization of a plastid diatom lower glycolytic-gluconeogenesis pathway

Dorrell

Liang

Guéguen

et al. 2022

Preprint

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Organic carbon fixed through the Calvin Cycle can be diverted towards different metabolic fates within and beyond the plastids of photosynthetic eukaryotes. These include export to the cytoplasm and mitochondrial respiration; gluconeogenesis of storage compounds; and the anabolic synthesis of lipids, amino acids and cofactors via the plastidial pyruvate hub. In plants, pyruvate is principally synthesised via the lower half of glycolysis-gluconeogenesis in the cytoplasm, although a secondary plastid-targeted pathway in non-photosynthetic tissue directly links glyceraldehyde-3-phosphate to the pyruvate hub. Here, we characterize a complete plastidial lower half glycolytic-gluconeogenic pathway in the photosynthetic plastids of diatoms, obligately photosynthetic eukaryotic algae that are important contributors to marine primary production. We show that the two enzymes required to complete plastidial glycolysis-gluconeogenesis, plastidial Enolase and PGAM (bis-phospho-glycerate mutase), originated through recent duplications of mitochondria-targeted respiratory glycolytic isoforms. Through CRISPR-Cas9 mutagenesis and integrative omic analyses in the diatom Phaeodactylum tricornutum, we present evidence that this pathway functions to divert excess plastidial glyceraldehyde-3-phosphate into diverse fates accessed from the pyruvate hub, and may potentially also function in the gluconeogenic direction to permit more efficient management of cellular carbon. Considering meta-genomic data, we show that this pathway is of greater importance in polar and sub-polar oceans, in which diatoms dominate primary production; and considering experimental data, we show that this principally relates to the elongated photoperiods present at high latitudes. Our data provide insights into the functions of a poorly understood yet evolutionarily recurrent plastidial metabolic pathway, and a further explanation for the success of diatoms in the contemporary ocean.

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The role of zinc in the adaptive evolution of polar phytoplankton

Cited by 21 publications

References 67 publications

Multiomics in the central Arctic Ocean for benchmarking biodiversity change

Multiomics in the central Arctic Ocean for benchmarking biodiversity change

Manganese Limitation of Phytoplankton Physiology and Productivity in the Southern Ocean

Complementary environmental analysis and functional characterization of a plastid diatom lower glycolytic-gluconeogenesis pathway

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