Representative Diatom and Coccolithophore Species Exhibit Divergent Responses throughout Simulated Upwelling Cycles

ABSTRACT Wind-driven upwelling followed by relaxation results in cycles of cold nutrient-rich water fueling intense phytoplankton blooms followed by nutrient depletion, bloom decline, and sinking of cells. Surviving cells at depth can then be vertically transported back to the surface with upwelled...

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Autores principales: Robert H. Lampe, Gustavo Hernandez, Yuan Yu Lin, Adrian Marchetti
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Publicado: American Society for Microbiology 2021
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spelling oai:doaj.org-article:ef52d9c9a0134fe08348f00b14f975642021-12-02T19:22:27ZRepresentative Diatom and Coccolithophore Species Exhibit Divergent Responses throughout Simulated Upwelling Cycles10.1128/mSystems.00188-212379-5077https://doaj.org/article/ef52d9c9a0134fe08348f00b14f975642021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00188-21https://doaj.org/toc/2379-5077ABSTRACT Wind-driven upwelling followed by relaxation results in cycles of cold nutrient-rich water fueling intense phytoplankton blooms followed by nutrient depletion, bloom decline, and sinking of cells. Surviving cells at depth can then be vertically transported back to the surface with upwelled waters to seed another bloom. As a result of these cycles, phytoplankton communities in upwelling regions are transported through a wide range of light and nutrient conditions. Diatoms appear to be well suited for these cycles, but their responses to them remain understudied. To investigate the bases for diatoms’ ecological success in upwelling environments, we employed laboratory simulations of a complete upwelling cycle with a common diatom, Chaetoceros decipiens, and coccolithophore, Emiliania huxleyi. We show that while both organisms exhibited physiological and transcriptomic plasticity, the diatom displayed a distinct response enabling it to rapidly shift-up growth rates and nitrate assimilation when returned to light and available nutrients following dark nutrient-deplete conditions. As observed in natural diatom communities, C. decipiens highly expresses before upwelling, or frontloads, key transcriptional and nitrate assimilation genes, coordinating its rapid response to upwelling conditions. Low-iron simulations showed that C. decipiens is capable of maintaining this response when iron is limiting to growth, whereas E. huxleyi is not. Differential expression between iron treatments further revealed specific genes used by each organism under low iron availability. Overall, these results highlight the responses of two dominant phytoplankton groups to upwelling cycles, providing insight into the mechanisms fueling diatom blooms during upwelling events. IMPORTANCE Coastal upwelling regions are among the most biologically productive ecosystems. During upwelling events, nutrient-rich water is delivered from depth resulting in intense phytoplankton blooms typically dominated by diatoms. Along with nutrients, phytoplankton may also be transported from depth to seed these blooms then return to depth as upwelling subsides creating a cycle with varied conditions. To investigate diatoms’ success in upwelling regions, we compare the responses of a common diatom and coccolithophore throughout simulated upwelling cycles under iron-replete and iron-limiting conditions. The diatom exhibited a distinct rapid response to upwelling irrespective of iron status, whereas the coccolithophore’s response was either delayed or suppressed depending on iron availability. Concurrently, the diatom highly expresses, or frontloads, nitrate assimilation genes prior to upwelling, potentially enabling this rapid response. These results provide insight into the molecular mechanisms underlying diatom blooms and ecological success in upwelling regions.Robert H. LampeGustavo HernandezYuan Yu LinAdrian MarchettiAmerican Society for Microbiologyarticlephytoplanktonshift upnitrogen metabolismiron limitationtranscriptomicsMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution DOAJ
collection DOAJ
language EN
topic phytoplankton
shift up
nitrogen metabolism
iron limitation
transcriptomics
Microbiology
QR1-502
spellingShingle phytoplankton
shift up
nitrogen metabolism
iron limitation
transcriptomics
Microbiology
QR1-502
Robert H. Lampe
Gustavo Hernandez
Yuan Yu Lin
Adrian Marchetti
Representative Diatom and Coccolithophore Species Exhibit Divergent Responses throughout Simulated Upwelling Cycles
description ABSTRACT Wind-driven upwelling followed by relaxation results in cycles of cold nutrient-rich water fueling intense phytoplankton blooms followed by nutrient depletion, bloom decline, and sinking of cells. Surviving cells at depth can then be vertically transported back to the surface with upwelled waters to seed another bloom. As a result of these cycles, phytoplankton communities in upwelling regions are transported through a wide range of light and nutrient conditions. Diatoms appear to be well suited for these cycles, but their responses to them remain understudied. To investigate the bases for diatoms’ ecological success in upwelling environments, we employed laboratory simulations of a complete upwelling cycle with a common diatom, Chaetoceros decipiens, and coccolithophore, Emiliania huxleyi. We show that while both organisms exhibited physiological and transcriptomic plasticity, the diatom displayed a distinct response enabling it to rapidly shift-up growth rates and nitrate assimilation when returned to light and available nutrients following dark nutrient-deplete conditions. As observed in natural diatom communities, C. decipiens highly expresses before upwelling, or frontloads, key transcriptional and nitrate assimilation genes, coordinating its rapid response to upwelling conditions. Low-iron simulations showed that C. decipiens is capable of maintaining this response when iron is limiting to growth, whereas E. huxleyi is not. Differential expression between iron treatments further revealed specific genes used by each organism under low iron availability. Overall, these results highlight the responses of two dominant phytoplankton groups to upwelling cycles, providing insight into the mechanisms fueling diatom blooms during upwelling events. IMPORTANCE Coastal upwelling regions are among the most biologically productive ecosystems. During upwelling events, nutrient-rich water is delivered from depth resulting in intense phytoplankton blooms typically dominated by diatoms. Along with nutrients, phytoplankton may also be transported from depth to seed these blooms then return to depth as upwelling subsides creating a cycle with varied conditions. To investigate diatoms’ success in upwelling regions, we compare the responses of a common diatom and coccolithophore throughout simulated upwelling cycles under iron-replete and iron-limiting conditions. The diatom exhibited a distinct rapid response to upwelling irrespective of iron status, whereas the coccolithophore’s response was either delayed or suppressed depending on iron availability. Concurrently, the diatom highly expresses, or frontloads, nitrate assimilation genes prior to upwelling, potentially enabling this rapid response. These results provide insight into the molecular mechanisms underlying diatom blooms and ecological success in upwelling regions.
format article
author Robert H. Lampe
Gustavo Hernandez
Yuan Yu Lin
Adrian Marchetti
author_facet Robert H. Lampe
Gustavo Hernandez
Yuan Yu Lin
Adrian Marchetti
author_sort Robert H. Lampe
title Representative Diatom and Coccolithophore Species Exhibit Divergent Responses throughout Simulated Upwelling Cycles
title_short Representative Diatom and Coccolithophore Species Exhibit Divergent Responses throughout Simulated Upwelling Cycles
title_full Representative Diatom and Coccolithophore Species Exhibit Divergent Responses throughout Simulated Upwelling Cycles
title_fullStr Representative Diatom and Coccolithophore Species Exhibit Divergent Responses throughout Simulated Upwelling Cycles
title_full_unstemmed Representative Diatom and Coccolithophore Species Exhibit Divergent Responses throughout Simulated Upwelling Cycles
title_sort representative diatom and coccolithophore species exhibit divergent responses throughout simulated upwelling cycles
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/ef52d9c9a0134fe08348f00b14f97564
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