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Combined pigment and metatranscriptomic analysis reveals highly synchronized diel patterns of phenotypic light response across domains in the open oligotrophic ocean

Abstract

Sunlight is the most important environmental control on diel fluctuations in phytoplankton activity, and understanding diel microbial processes is essential to the study of oceanic biogeochemical cycles. Yet, little is known about the in situ temporal dynamics of phytoplankton metabolic activities and their coordination across different populations. We investigated diel orchestration of phytoplankton activity in photosynthesis, photoacclimation, and photoprotection by analyzing pigment and quinone distributions in combination with metatranscriptomes in surface waters of the North Pacific Subtropical Gyre (NPSG). We found diel cycles in pigment abundances resulting from the balance of their synthesis and consumption. These dynamics suggest that night represents a metabolic recovery phase, refilling cellular pigment stores, while photosystems are remodeled towards photoprotection during daytime. Transcript levels of genes involved in photosynthesis and pigment metabolism had synchronized diel expression patterns among all taxa, reflecting the driving force light imparts upon photosynthetic organisms in the ocean, while other environmental factors drive niche differentiation. For instance, observed decoupling of diel oscillations in transcripts and related pigments indicates that pigment abundances are modulated by environmental factors extending beyond gene expression/regulation reinforcing the need to combine metatranscriptomics with proteomics and metabolomics to fully understand the timing of these critical processes in situ.

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Fig. 1: Schematic representation of the structure of photosystem II in photosynthetic membranes.
Fig. 2: Diel oscillations of pigments and pigment-related transcripts.
Fig. 3: Relationship between periodic pigment-associated gene expression in phytoplankton transcripts and actual pigment abundances.
Fig. 4: Conceptualized temporal separation of phytoplankton pigment, plastoquinone and transcript abundances during the dark–light cycle in surface waters (15 m) at station ALOHA.

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Acknowledgements

We are grateful to the officers and crew of the R/V Kilo Moana cruise KM1513 (HOE Legacy II). We thank Helen F. Fredricks for help with lipidomics analysis, Daniel J. Repeta for help with onboard sample collection, and two anonymous reviewers for constructive criticism. This work was funded by a grant from the Simons Foundation (SCOPE, Award # 329108, BASVM, STD, EFD, JSW), and Gordon and Betty Moore Foundation (grant #3777, EFD). KWB was further supported by the Postdoctoral Scholarship Program at Woods Hole Oceanographic Institution & U.S. Geological Survey.

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BASVM, STD, EFD. conceived the study. KWB, MJH, and DRM conducted and analyzed lipidomic, eukaryotic metatranscriptomic and prokaryote transcriptomic studies, respectively. JSW and DM supported data analysis. KWB and MJH wrote the paper with contributions from all authors.

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Correspondence to Kevin W. Becker.

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Becker, K.W., Harke, M.J., Mende, D.R. et al. Combined pigment and metatranscriptomic analysis reveals highly synchronized diel patterns of phenotypic light response across domains in the open oligotrophic ocean. ISME J 15, 520–533 (2021). https://doi.org/10.1038/s41396-020-00793-x

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