A minimal mathematical model of nonphotochemical quenching of chlorophyll fluorescence

Copyright © 2010 Elsevier Ireland Ltd. All rights reserved.Peer reviewedPreprin

Excitation quenching in chlorophyll-carotenoid antenna systems: 'coherent' or 'incoherent'

Plants possess an essential ability to rapidly down-regulate light-harvesting in response to high light. This photoprotective process involves the formation of energy-quenching interactions between the chlorophyll and carotenoid pigments within the antenna of Photosystem II (PSII). The nature of these interactions is currently debated, with, among others, ‘incoherent’ or ‘coherent’ quenching models (or a combination of the two) suggested by a range of time-resolved spectroscopic measurements. In ‘incoherent quenching’, energy is transferred from a chlorophyll to a carotenoid and is dissipated due to the intrinsically short excitation lifetime of the latter. ‘Coherent quenching’ would arise from the quantum mechanical mixing of chlorophyll and carotenoid excited state properties, leading to a reduction in chlorophyll excitation lifetime. The key parameters are the energy gap, Δ=Car−Chl, Δ ε = ε C a r − ε C h l , and the resonance coupling, J, between the two excited states. Coherent quenching will be the dominant process when −<Δ<, − J < Δ ε < J , i.e., when the two molecules are resonant, while the quenching will be largely incoherent when Chl>(Car+). ε C h l > ( ε C a r + J ) . One would expect quenching to be energetically unfavorable for Chl<(Car−). ε C h l < ( ε C a r − J ) . The actual dynamics of quenching lie somewhere between these limiting regimes and have non-trivial dependencies of both J and Δ. Δ ε . Using the Hierarchical Equation of Motion (HEOM) formalism we present a detailed theoretical examination of these excitation dynamics and their dependence on slow variations in J and Δ. Δ ε . We first consider an isolated chlorophyll–carotenoid dimer before embedding it within a PSII antenna sub-unit (LHCII). We show that neither energy transfer, nor the mixing of excited state lifetimes represent unique or necessary pathways for quenching and in fact discussing them as distinct quenching mechanisms is misleading. However, we do show that quenching cannot be switched ‘on’ and ‘off’ by fine tuning of Δ Δ ε around the resonance point, Δ=0. Δ ε = 0. Due to the large reorganization energy of the carotenoid excited state, we find that the presence (or absence) of coherent interactions have almost no impact of the dynamics of quenching. Counter-intuitively significant quenching is present even when the carotenoid excited state lies above that of the chlorophyll. We also show that, above a rather small threshold value of >10cm−1 J > 10 c m − 1 quenching becomes less and less sensitive to J (since in the window −<Δ< − J < Δ ε < J the overall lifetime is independent of it). The requirement for quenching appear to be only that >0. J > 0. Although the coherent/incoherent character of the quenching can vary, the overall kinetics are likely robust with respect to fluctuations in J and Δ. Δ ε . This may be the basis for previous observations of NPQ with both coherent and incoherent features

Satellite-derived fluorescence quantum yields as indicators of phytoplankton photophysiology

Understanding and quantifying phytoplankton physiological variability is essential for analyses of biogeochemical cycling, climate change and ecosystem processes. Satellite measurements of chlorophyll indicate phytoplankton biomass but hold minimal direct information about the organisms\u27 photosynthetic capabilities: however, remote sensing-derived fluorescence quantum yields have the potential for monitoring phytoplankton photophysiological states on a global scale. Recent research has demonstrated the effects of both nutrient stress and photoacclimation on fluorescence yield. Here, a novel satellite product comprising seven years of fluorescence quantum yields, derived from MODIS/Aqua normalized fluorescence line heights and corrected for pigment packaging effects, is evaluated and explored. Fluorescence yields are highest during winter, decline to mid-summer minima and increase again during autumn; winter-spring and summer-autumn transitions exhibit different slopes at most locations. Seasonal patterns respond primarily to changes in growth irradiance, forming a closed annual cycle. Monthly climatologies show spatial patterns associated with the annual cycle and the timing of seasonal transitions are modulated by latitude. Across the northwest and northeast Atlantic shelf sea regions, fluorescence yields are lower throughout the year than in the open ocean. Interannual variability is greatest during late autumn and winter months, aligned with times of dynamic water column mixing. An empirical orthogonal function analysis of the seven year time series finds strong seasonally-variable influences with a high degree of geographic complexity. Beyond large spatial and temporal patterns, this new satellite product effectively captures short-term photoacclimation events. Increases in fluorescence quantum yield coincident with the sharp increase in water column stratification but prior to the spring chlorophyll peak were ubiquitous throughout the northern North Atlantic. During such events, phytoplankton are first acclimating to increased growth irradiance before the population bloom. At all scales, fluorescence yield trends compare well with an established conceptual model and are most strongly associated with growth irradiance dynamics rather than other forcing factors (i.e., macro- and micro-nutrient stress and phytoplankton community composition). This thesis provides the first synoptic quantification of seasonal and interannual phytoplankton photophysiological variability in the northern North Atlantic and demonstrates the potential of this new product for global investigations

Heat stress responses and population genetics of the kelp Laminaria digitata (Phaeophyceae) across latitudes reveal differentiation among North Atlantic populations

To understand the thermal plasticity of a coastal foundation species across its latitudinal distribution, we assess physiological responses to high temperature stress in the kelp Laminaria digitata in combination with population genetic characteristics and relate heat resilience to genetic features and phylogeography. We hypothesize that populations from Arctic and cold-temperate locations are less heat resilient than populations from warm distributional edges. Using meristems of natural L. digitata populations from six locations ranging between Kongsfjorden, Spitsbergen (79°N), and Quiberon, France (47°N), we performed a common-garden heat stress experiment applying 15°C to 23°C over eight days. We assessed growth, photosynthetic quantum yield, carbon and nitrogen storage, and xanthophyll pigment contents as response traits. Population connectivity and genetic diversity were analyzed with microsatellite markers. Results from the heat stress experiment suggest that the upper temperature limit of L. digitata is nearly identical across its distribution range, but subtle differences in growth and stress responses were revealed for three populations from the species' ecological range margins. Two populations at the species' warm distribution limit showed higher temperature tolerance compared to other populations in growth at 19°C and recovery from 21°C (Quiberon, France), and photosynthetic quantum yield and xanthophyll pigment responses at 23°C (Helgoland, Germany). In L. digitata from the northernmost population (Spitsbergen, Norway), quantum yield indicated the highest heat sensitivity. Microsatellite genotyping revealed all sampled populations to be genetically distinct, with a strong hierarchical structure between southern and northern clades. Genetic diversity was lowest in the isolated population of the North Sea island of Helgoland and highest in Roscoff in the English Channel. All together, these results support the hypothesis of moderate local differentiation across L. digitata's European distribution, whereas effects are likely too weak to ameliorate the species' capacity to withstand ocean warming and marine heatwaves at the southern range edge.Foundation for Science and Technology: UIDB/04326/2020/ PTDC/MAR-EST/6053/2014/ Biodiversa/0004/2015info:eu-repo/semantics/publishedVersio

Os estuários como sumidouros decarbono: fotossíntese, fotoinibição e resiliência da produtividade primária pelágica e bêntica

Estuaries are recognized amongst the most productive ecosystems on Earth. Their high primary productivity is largely due to the photosynthetic carbon fixation by phytoplankton and microphytobenthos, the communities of microalgae and cyanobacteria that inhabit the water column and subtidal or intertidal sediments, respectively. In comparison with the phytoplankton, the microphytobenthos has been much less studied regarding the photophysiological processes affecting primary productivity, and their relative role as contributors to estuarine-level production. One of these processes is photoinhibition, the high light-induced decrease in photosynthetic activity, considered a major limiting factor of growth and primary productivity in the variable and extreme estuarine environment. The detrimental impact of photoinhibition on photosynthesis depends on the balance between the photoinactivation and repair of photosystem II (PSII). By successfully adapting to microphytobenthos a recently-developed methodology based on multi-actinic imaging of chlorophyll fluorescence, this work evaluated their photoacclimation and photoprotective capacity, as measured by the reduction in PSII photoinactivation. PSII photoinactivation and repair was found to vary between different communities, pointing to a trade-off between cellular motility-based and physiological photoprotective mechanisms. Epipelic (motile) species showed a reduced physiological capacity for preventing photodamage, while epipsammic (non-motile) forms appeared less susceptible to photoinactivation and more dependent on physiological photoprotection. This work further investigated an overlooked aspect of microphytobenthos ecology, related to the presence of substantial amounts of microalgal biomass in subsurface sediments. By studying samples from intertidal areas of the Ria de Aveiro (Portugal), this work found that buried cells can quickly regain photosynthetic activity when exposed to surface conditions. Potential viable subsurface (0.5-10 cm) microalgal biomass was found to represent 2-3 times the amount of biomass present at the surface layers (0.0-0.5 cm). These results support the hypothesis that subsurface biomass may play an important ecological role as a source of photosynthetically competent cells capable of ‘reinoculating’ the surface, contributing to the high productivity of intertidal areas. The relative importance of phytoplankton and microphytobenthos as contributors to ecosystem-level primary productivity was evaluated in the Ria de Aveiro, by comparing the spatio-temporal variability of biomass and productivity of different communities. This study made use of a new type of fluorometer allowing the measurement of absolute rates of PSII electron transport rates and the estimation of carbon fixation rates. Biomass-specific productivity rates for phytoplankton and microphytobenthos were found to reach 68.0 and 19.1 mg C mg Chl a-1 d-1, respectively. Annual areal production rates were higher for the microphytobenthos, reaching 105.2 g C m-2 yr-1, as opposed to 49.9 g C m-2 yr-1 for the phytoplankton. The annual rates upscaled for the whole Ria de Aveiro highlight the importance of the intertidal areas as significant carbon sinks and reservoirs of active ‘blue carbon’, and as main sites of primary productivity, found to contribute with more than 60% of the total ecosystem-level budget 12428.3 t C yr-1.Os estuários são reconhecidos como um dos tipos de ecossistemas mais produtivos na Terra. A sua elevada produtividade primária é devida em larga medida à fixação fotossintética de carbono pelo fitoplâncton e microfitobentos, as comunidades de microalgas e cianobactérias que habitam a coluna de àgua e os sedimentos subtidais e intertidais, respetivamente. Em comparação com o fitoplâncton, o microfitobentos tem sido muito menos estudado relativamente aos processos fotofisiológicos que controlam a sua produtividade, bem como à sua contribuição para a produção primária global do estuário. Um destes processos é a fotoinibição, a diminuição da atividade fotossintética causada pela luz, considerada como um importante fator limitante da produtividade primária no ambiente estuarino. O impacto negativo da fotoinibição na fotossíntese depende do balanço entre a fotoinativação e a reparação do fotossistema II (PSII). Baseado num recente método de imagiologia multi-actínica de fluorescência da clorofila, este trabalho avaliou a fotoaclimatação e capacidade de fotoproteção contra a fotoinibição, medida pela redução da fotoinativação do PSII. A fotoinativação e reparação do PSII variou entre diferentes tipos de comunidades, indicando a existência de um balanço entre a fotoproteção baseada na motilidade celular e em mecanismos fisiológicos. Espécies epipélicas (móveis) mostraram uma menor capacidade fisiológica de prevenir danos, enquanto as formas epipsâmicas (imóveis) aparentaram ser menos suscetíveis à fotoinibição e mais dependentes de fotoproteção fisiológica. Este trabalho investigou ainda um aspeto pouco estudado, relacionado com a presença de quantidades substanciais de biomass de microalgas em sedimentos subsuperficias. Pela análise de sedimentos intertidais da Ria de Aveiro (Portugal), foi descoberto que as células enterradas conseguem recuperar rapidamente a sua atividade fotossintética quando expostas a condições da superfície. Foi também concluído que a biomassa subsuperficial (0.5-10 cm) potencialmente viável representa 2-3 vezes a biomassa presente nas camadas superficiais (0.0-0.5 cm). Estes resultados suportam a hipótese de que a biomassa subsuperficial desempenha um papel ecológico importante enquanto fonte de células fotossinteticamente competentes capazes de ‘reinocular’ a superfície, contribuindo para a elevada produtividade das áreas intertidais. A importância relativa da contribuição do fitoplâncton e do microfitobentos para a produtividade primária ao nível do ecossistema foi avaliada para a Ria de Aveiro, comparando a variabilidade espacio-temporal da biomass e produtividade de diferentes comunidades. Este estudo baseou-se na medição de taxas absolutas de transporte de electrões no PSII e a estimação de taxas de fixação de carbono. Por unidade de biomass, estas atingiram 68,0 e 19,1 mg C mg Chl a-1 d-1, para o fitoplâncton e o microfitobentos, respectivamente. Por unidade de área, a produtividade anual foi mais elevada no caso do microfitobentos, atingindo 105,2 g C m-2 yr-1, por oposição a 49,9 g C m-2 yr-1, para o fitoplâncton. Considerando a totalidade da área da Ria de Aveiro, os resultados salientam a importância das áreas intertidais enquanto sumidouros de carbono e reservatórios de “carbono azul”, e locais de elevada produtividade primária, contribuindo com mais de 60% do total anual de 12428,3 t C yr-1.Programa Doutoral em Biologi