Phenotypic Diversity and Plasticity of Photoresponse Across an Environmentally Contrasting Family of Phytoflagellates

Organisms often employ ecophysiological strategies to exploit environmental conditions and ensure bio-energetic success. However, the many complexities involved in the differential expression and flexibility of these strategies are rarely fully understood. Therefore, for the first time, using a thre...

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Main Authors: Mark R. Clegg, Alexander Wacker, Elly Spijkerman
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.707541/full
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author Mark R. Clegg
Alexander Wacker
Alexander Wacker
Elly Spijkerman
author_facet Mark R. Clegg
Alexander Wacker
Alexander Wacker
Elly Spijkerman
author_sort Mark R. Clegg
collection DOAJ
description Organisms often employ ecophysiological strategies to exploit environmental conditions and ensure bio-energetic success. However, the many complexities involved in the differential expression and flexibility of these strategies are rarely fully understood. Therefore, for the first time, using a three-part cross-disciplinary laboratory experimental analysis, we investigated the diversity and plasticity of photoresponsive traits employed by one family of environmentally contrasting, ecologically important phytoflagellates. The results demonstrated an extensive inter-species phenotypic diversity of behavioural, physiological, and compositional photoresponse across the Chlamydomonadaceae, and a multifaceted intra-species phenotypic plasticity, involving a broad range of beneficial photoacclimation strategies, often attributable to environmental predisposition and phylogenetic differentiation. Deceptively diverse and sophisticated strong (population and individual cell) behavioural photoresponses were observed, with divergence from a general preference for low light (and flexibility) dictated by intra-familial differences in typical habitat (salinity and trophy) and phylogeny. Notably, contrasting lower, narrow, and flexible compared with higher, broad, and stable preferences were observed in freshwater vs. brackish and marine species. Complex diversity and plasticity in physiological and compositional photoresponses were also discovered. Metabolic characteristics (such as growth rates, respiratory costs and photosynthetic capacity, efficiency, compensation and saturation points) varied elaborately with species, typical habitat (often varying more in eutrophic species, such as Chlamydomonas reinhardtii), and culture irradiance (adjusting to optimise energy acquisition and suggesting some propensity for low light). Considerable variations in intracellular pigment and biochemical composition were also recorded. Photosynthetic and accessory pigments (such as chlorophyll a, xanthophyll-cycle components, chlorophyll a:b and chlorophyll a:carotenoid ratios, fatty acid content and saturation ratios) varied with phylogeny and typical habitat (to attune photosystem ratios in different trophic conditions and to optimise shade adaptation, photoprotection, and thylakoid architecture, particularly in freshwater environments), and changed with irradiance (as reaction and harvesting centres adjusted to modulate absorption and quantum yield). The complex, concomitant nature of the results also advocated an integrative approach in future investigations. Overall, these nuanced, diverse, and flexible photoresponsive traits will greatly contribute to the functional ecology of these organisms, addressing environmental heterogeneity and potentially shaping individual fitness, spatial and temporal distribution, prevalence, and ecosystem dynamics.
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spelling doaj.art-507c2fe6313042caa7acf8d8dee7e2502022-12-21T22:33:55ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-08-011210.3389/fpls.2021.707541707541Phenotypic Diversity and Plasticity of Photoresponse Across an Environmentally Contrasting Family of PhytoflagellatesMark R. Clegg0Alexander Wacker1Alexander Wacker2Elly Spijkerman3Department of Ecology and Ecosystem Modelling, Institute of Biochemistry and Biology, University of Potsdam, Potsdam, GermanyDepartment of Theoretical Aquatic Ecology and Ecophysiology, Institute of Biochemistry and Biology, University of Potsdam, Potsdam, GermanyAnimal Ecology Group, Zoological Institute and Museum, University of Greifswald, Greifswald, GermanyDepartment of Ecology and Ecosystem Modelling, Institute of Biochemistry and Biology, University of Potsdam, Potsdam, GermanyOrganisms often employ ecophysiological strategies to exploit environmental conditions and ensure bio-energetic success. However, the many complexities involved in the differential expression and flexibility of these strategies are rarely fully understood. Therefore, for the first time, using a three-part cross-disciplinary laboratory experimental analysis, we investigated the diversity and plasticity of photoresponsive traits employed by one family of environmentally contrasting, ecologically important phytoflagellates. The results demonstrated an extensive inter-species phenotypic diversity of behavioural, physiological, and compositional photoresponse across the Chlamydomonadaceae, and a multifaceted intra-species phenotypic plasticity, involving a broad range of beneficial photoacclimation strategies, often attributable to environmental predisposition and phylogenetic differentiation. Deceptively diverse and sophisticated strong (population and individual cell) behavioural photoresponses were observed, with divergence from a general preference for low light (and flexibility) dictated by intra-familial differences in typical habitat (salinity and trophy) and phylogeny. Notably, contrasting lower, narrow, and flexible compared with higher, broad, and stable preferences were observed in freshwater vs. brackish and marine species. Complex diversity and plasticity in physiological and compositional photoresponses were also discovered. Metabolic characteristics (such as growth rates, respiratory costs and photosynthetic capacity, efficiency, compensation and saturation points) varied elaborately with species, typical habitat (often varying more in eutrophic species, such as Chlamydomonas reinhardtii), and culture irradiance (adjusting to optimise energy acquisition and suggesting some propensity for low light). Considerable variations in intracellular pigment and biochemical composition were also recorded. Photosynthetic and accessory pigments (such as chlorophyll a, xanthophyll-cycle components, chlorophyll a:b and chlorophyll a:carotenoid ratios, fatty acid content and saturation ratios) varied with phylogeny and typical habitat (to attune photosystem ratios in different trophic conditions and to optimise shade adaptation, photoprotection, and thylakoid architecture, particularly in freshwater environments), and changed with irradiance (as reaction and harvesting centres adjusted to modulate absorption and quantum yield). The complex, concomitant nature of the results also advocated an integrative approach in future investigations. Overall, these nuanced, diverse, and flexible photoresponsive traits will greatly contribute to the functional ecology of these organisms, addressing environmental heterogeneity and potentially shaping individual fitness, spatial and temporal distribution, prevalence, and ecosystem dynamics.https://www.frontiersin.org/articles/10.3389/fpls.2021.707541/fullphotoresponsebehaviourphysiologycompositionphotosynthesisacclimation
spellingShingle Mark R. Clegg
Alexander Wacker
Alexander Wacker
Elly Spijkerman
Phenotypic Diversity and Plasticity of Photoresponse Across an Environmentally Contrasting Family of Phytoflagellates
Frontiers in Plant Science
photoresponse
behaviour
physiology
composition
photosynthesis
acclimation
title Phenotypic Diversity and Plasticity of Photoresponse Across an Environmentally Contrasting Family of Phytoflagellates
title_full Phenotypic Diversity and Plasticity of Photoresponse Across an Environmentally Contrasting Family of Phytoflagellates
title_fullStr Phenotypic Diversity and Plasticity of Photoresponse Across an Environmentally Contrasting Family of Phytoflagellates
title_full_unstemmed Phenotypic Diversity and Plasticity of Photoresponse Across an Environmentally Contrasting Family of Phytoflagellates
title_short Phenotypic Diversity and Plasticity of Photoresponse Across an Environmentally Contrasting Family of Phytoflagellates
title_sort phenotypic diversity and plasticity of photoresponse across an environmentally contrasting family of phytoflagellates
topic photoresponse
behaviour
physiology
composition
photosynthesis
acclimation
url https://www.frontiersin.org/articles/10.3389/fpls.2021.707541/full
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