Divergence of photosynthetic strategies amongst marine diatoms.

Marine phytoplankton, and in particular diatoms, are responsible for almost half of all primary production on Earth. Diatom species thrive from polar to tropical waters and across light environments that are highly complex to relatively benign, and so have evolved highly divergent strategies for reg...

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Main Authors: Nerissa L Fisher, Douglas A Campbell, David J Hughes, Unnikrishnan Kuzhiumparambil, Kimberly H Halsey, Peter J Ralph, David J Suggett
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0244252
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spelling doaj-c478fa2f04ca4c13968463a8741d70862021-03-12T05:30:57ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-011512e024425210.1371/journal.pone.0244252Divergence of photosynthetic strategies amongst marine diatoms.Nerissa L FisherDouglas A CampbellDavid J HughesUnnikrishnan KuzhiumparambilKimberly H HalseyPeter J RalphDavid J SuggettMarine phytoplankton, and in particular diatoms, are responsible for almost half of all primary production on Earth. Diatom species thrive from polar to tropical waters and across light environments that are highly complex to relatively benign, and so have evolved highly divergent strategies for regulating light capture and utilization. It is increasingly well established that diatoms have achieved such successful ecosystem dominance by regulating excitation energy available for generating photosynthetic energy via highly flexible light harvesting strategies. However, how different light harvesting strategies and downstream pathways for oxygen production and consumption interact to balance excitation pressure remains unknown. We therefore examined the responses of three diatom taxa adapted to inherently different light climates (estuarine Thalassioisira weissflogii, coastal Thalassiosira pseudonana and oceanic Thalassiosira oceanica) during transient shifts from a moderate to high growth irradiance (85 to 1200 μmol photons m-2 s-1). Transient high light exposure caused T. weissflogii to rapidly downregulate PSII with substantial nonphotochemical quenching, protecting PSII from inactivation or damage, and obviating the need for induction of O2 consuming (light-dependent respiration, LDR) pathways. In contrast, T. oceanica retained high excitation pressure on PSII, but with little change in RCII photochemical turnover, thereby requiring moderate repair activity and greater reliance on LDR. T. pseudonana exhibited an intermediate response compared to the other two diatom species, exhibiting some downregulation and inactivation of PSII, but high repair of PSII and induction of reversible PSII nonphotochemical quenching, with some LDR. Together, these data demonstrate a range of strategies for balancing light harvesting and utilization across diatom species, which reflect their adaptation to sustain photosynthesis under environments with inherently different light regimes.https://doi.org/10.1371/journal.pone.0244252
collection DOAJ
language English
format Article
sources DOAJ
author Nerissa L Fisher
Douglas A Campbell
David J Hughes
Unnikrishnan Kuzhiumparambil
Kimberly H Halsey
Peter J Ralph
David J Suggett
spellingShingle Nerissa L Fisher
Douglas A Campbell
David J Hughes
Unnikrishnan Kuzhiumparambil
Kimberly H Halsey
Peter J Ralph
David J Suggett
Divergence of photosynthetic strategies amongst marine diatoms.
PLoS ONE
author_facet Nerissa L Fisher
Douglas A Campbell
David J Hughes
Unnikrishnan Kuzhiumparambil
Kimberly H Halsey
Peter J Ralph
David J Suggett
author_sort Nerissa L Fisher
title Divergence of photosynthetic strategies amongst marine diatoms.
title_short Divergence of photosynthetic strategies amongst marine diatoms.
title_full Divergence of photosynthetic strategies amongst marine diatoms.
title_fullStr Divergence of photosynthetic strategies amongst marine diatoms.
title_full_unstemmed Divergence of photosynthetic strategies amongst marine diatoms.
title_sort divergence of photosynthetic strategies amongst marine diatoms.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2020-01-01
description Marine phytoplankton, and in particular diatoms, are responsible for almost half of all primary production on Earth. Diatom species thrive from polar to tropical waters and across light environments that are highly complex to relatively benign, and so have evolved highly divergent strategies for regulating light capture and utilization. It is increasingly well established that diatoms have achieved such successful ecosystem dominance by regulating excitation energy available for generating photosynthetic energy via highly flexible light harvesting strategies. However, how different light harvesting strategies and downstream pathways for oxygen production and consumption interact to balance excitation pressure remains unknown. We therefore examined the responses of three diatom taxa adapted to inherently different light climates (estuarine Thalassioisira weissflogii, coastal Thalassiosira pseudonana and oceanic Thalassiosira oceanica) during transient shifts from a moderate to high growth irradiance (85 to 1200 μmol photons m-2 s-1). Transient high light exposure caused T. weissflogii to rapidly downregulate PSII with substantial nonphotochemical quenching, protecting PSII from inactivation or damage, and obviating the need for induction of O2 consuming (light-dependent respiration, LDR) pathways. In contrast, T. oceanica retained high excitation pressure on PSII, but with little change in RCII photochemical turnover, thereby requiring moderate repair activity and greater reliance on LDR. T. pseudonana exhibited an intermediate response compared to the other two diatom species, exhibiting some downregulation and inactivation of PSII, but high repair of PSII and induction of reversible PSII nonphotochemical quenching, with some LDR. Together, these data demonstrate a range of strategies for balancing light harvesting and utilization across diatom species, which reflect their adaptation to sustain photosynthesis under environments with inherently different light regimes.
url https://doi.org/10.1371/journal.pone.0244252
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