Temperature-dependent growth and photophysiology of prokaryotic and eukaryotic oceanic picophytoplankton

Kulk, Gemma; Vries, Pablo de; Poll, Willem H. van de; Visser, Ronald J. W.; Buma, Anita G. J.

doi:10.3354/meps09898

Cited by 40 publications

(51 citation statements)

References 59 publications

(88 reference statements)

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“…In the study strain of Prochlorococcus we found a modest increase in measured YNPQ under high excitation pressure (Figure 3A), coinciding with the accumulation of significant predicted photoinactivation in the cultures (Table 3). Some strains of Prochlorococcus (Bailey et al, 2005;Kulk et al, 2012Kulk et al, , 2013 have shown nonphotochemical quenching phases whose induction and relaxation show temperature responses consistent with a dependence upon enzyme kinetics or membrane fluidity, which is not expected for a non-photochemical quenching response based upon photoinactivation of PSII.…”

Section: Resultsmentioning

confidence: 89%

“…There is a long history of treating "q I " or inhibitory quenching (Horton et al, 1996) as a component of non-photochemical quenching, in the broadest sense. Photoinactivation of PSII causes changes in PSII fluorescence emission variables, particularly increases in F 0 and F 0 ′ (Oxborough and Baker, 1997;Ware et al, 2015) that could overlap or interfere with changes provoked by induction of YNPQ (Kulk et al, 2012(Kulk et al, , 2013. Although neither F 0 nor F 0 ′ are explicitly included in calculation of YNPQ nor YNO, underlying changes in F 0 ′ could shift the level of steady state fluorescence under illumination, F S , which is part of the YNPQ and YNO parameters.…”

Section: Methodsmentioning

confidence: 99%

“…This magnitude of YNPQ was sufficient to cause a detectable down-regulation of σ PSII ′ in Ostreococcus and Thalassiosira (Figures 4C,D), but in Prochlorococcus we found no significant down-regulation of σ PSII ′ with light induction of YNPQ even when the actinic light reached as high as 1,600 µmol photons m −2 s −1 . Therefore, whatever the underlying mechanism(s) (Bailey et al, 2005;Kulk et al, 2012Kulk et al, , 2013, we find that changes in measured YNPQ were ineffective in altering σ PSII ′ in our studied strain of Prochlorococcus, measured with light absorbed through divinyl chl a. Indeed the relatively stable light and low nutrient regimes typical for Prochlorococcus strains argue against a large, rapidly regulated capacity for changes in excitation dissipation (Bailey et al, 2005) since it is more economical, in terms of N resource, to slowly regulate the content of antenna complexes to tune σ PSII to a prevailing stable light regime, through changes in gene expression within a strain or changes in genomic encoded capacities among ecotypes (Rocap et al, 2003).…”

Section: Figure 4 Presents the Responses Of σ Psiimentioning

confidence: 99%

“…Non-photochemical quenching reflects changes in the dissipation of absorbed excitation as heat. There is a large literature across species and growth conditions (Ruban et al, 2004;Bailey et al, 2005;Lavaud et al, 2007;Kulk et al, 2012Kulk et al, , 2013Holzwarth et al, 2013;Lavaud and Lepetit, 2013;Giovagnetti and Ruban, 2016) reporting the patterns and responses of the unbounded Stern-Volmer parameterization, NPQ:…”

Section: Introductionmentioning

confidence: 99%

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Phytoplankton σPSII and Excitation Dissipation; Implications for Estimates of Primary Productivity

Lavaud

Perkins

et al. 2018

Front. Mar. Sci.

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The effective absorption cross section for photochemistry of Photosystem II in the light (σ PSII ′ ) comprises the probability of light capture by Photosystem II and the quantum yield for subsequent photochemistry. σ PSII ′ is used to model photosynthesis and aquatic productivity, and phytoplankters regulate σ PSII ′ to mitigate over-or under-excitation of Photosystem II. We used diverse phytoplankton taxa to compare short and long term changes in σ PSII ′ with the induction of the yield of non-photochemical quenching (YNPQ) of chlorophyll fluorescence, a measure of regulated excitation dissipation. In two picocyanobacteria σ PSII ′ showed no decline upon induction of moderate YNPQ, above light levels sufficient for saturation of electron transport. In the eukaryotic chl a/b Ostreococcus and the chl a/c diatom Thalassiosira, induction of non-photochemical quenching was stronger after growth under saturating light, an acclimation attributable to increased xanthophyll cycle pigment content. Across short and longer-term light histories to induce or relax regulatory processes Ostreococcus and Thalassiosira showed proportional variations between the level of YNPQ and the down regulation of σ PSII ′ . The proportional down regulation of σ PSII ′ was, however, significantly smaller than the amplitude of YNPQ induction. For the eukaryotes we can predict changes in σ PSII ′ , useful for modeling electron transport, productivity and acclimation, from measures of YNPQ, which are accessible from fluorescence yield measures that do not include σ PSII ′ . This useful relation, however, does not extend to the tested prokaryotes, possibly as a result of differential violations of the rate constant assumptions that underlie the calculated YNPQ parameter.

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Section: Resultsmentioning

confidence: 89%

Section: Methodsmentioning

confidence: 99%

Section: Figure 4 Presents the Responses Of σ Psiimentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Phytoplankton σPSII and Excitation Dissipation; Implications for Estimates of Primary Productivity

Lavaud

Perkins

et al. 2018

Front. Mar. Sci.

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“…However, cells become increasingly larger and pigment-packaging effects seem to counteract any benefits associated with increased pigmentation and absolute rates of primary productivity decline ( Figure 5C). As the efficiency of the Calvin Cycle decreases, alternative electron sinks e.g., cyclic electron transport around PSII, Mehler reaction, terminal oxidase activity, nitrate reduction also become progressively more important with increasing temperature (Hancke et al, 2008;Kulk et al, 2012).…”

Section: Temperature Driven Changes In Fitness and Other Functional Tmentioning

confidence: 99%

Thermal Performance Curves of Functional Traits Aid Understanding of Thermally Induced Changes in Diatom-Mediated Biogeochemical Fluxes

et al. 2016

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How the functional traits (FTs) of phytoplankton change with temperature is important for understanding the impacts of ocean warming on phytoplankton mediated biogeochemical fluxes. This study quantifies the thermal performance curves (TPCs) of FTs in the cosmopolitan model diatom, Thalassiosira pseudonana, to advance understanding of trade-offs between physiological (photoacclimation, carbon fixation, nitrate, phosphate, and silicate uptake) and morphological traits (cell volume and frustule silicification). We show that each FT has substantial phenotypic plasticity and exhibits a unique TPC, varying in both shape and thermal optimum, and diverging from the growth response. The TPC for growth was symmetric with a thermal optimum (T opt ) of 18 • C. In comparison, the TPC for primary productivity was warm-skewed with a T opt around 21 • C, whereas frustule silicification decreased linearly with increasing temperature. Together, this suggests that the optimal temperature for overall fitness is a balance of trade-offs in the underlying functional traits. Moreover, these results demonstrate that growth is not necessarily an accurate estimate of overall biogeochemical performance and that temperature change will likely influence elemental fluxes such as carbon and silicon. Finally, we show that temperature-driven changes in individual traits e.g., photoacclimation, can mimic responses experienced under other environmental stressors (high light) and so a multi-trait assessment is essential for accurate interpretation of the cellular impact of warming. This study also reveals that multi-trait analysis, in the context of TPCs, provides insight into the cellular physiology regulating the whole cell response and has the potential to provide better estimates of how diatom-mediated biogeochemical fluxes are likely to be impacted in the context of ocean warming. Analyzing the response of multiple traits more comprehensively over other environmental gradients may therefore provide a useful framework to advance understanding of how taxon-specific functional traits will respond to multifaceted ocean change.

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Distribution of phytoplankton groups within the deep chlorophyll maximum

Latasa

Cabello

Morán

et al. 2016

Limnology & Oceanography

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The fine vertical distribution of phytoplankton groups within the deep chlorophyll maximum (DCM) was studied in the NE Atlantic during summer stratification. A simple but unconventional sampling strategy allowed examining the vertical structure with ca. 2 m resolution. The distribution of Prochlorococcus, Synechococcus, chlorophytes, pelagophytes, small prymnesiophytes, coccolithophores, diatoms, and dinoflagellates was investigated with a combination of pigment-markers, flow cytometry and optical and FISH microscopy. All groups presented minimum abundances at the surface and a maximum in the DCM layer. The cell distribution was not vertically symmetrical around the DCM peak and cells tended to accumulate in the upper part of the DCM layer. The more symmetrical distribution of chlorophyll than cells around the DCM peak was due to the increase of pigment per cell with depth. We found a vertical alignment of phytoplankton groups within the DCM layer indicating preferences for different ecological niches in a layer with strong gradients of light and nutrients. Prochlorococcus occupied the shallowest and diatoms the deepest layers. Dinoflagellates, Synechococcus and small prymnesiophytes preferred shallow DCM layers, and coccolithophores, chlorophytes and pelagophytes showed a preference for deep layers. Cell size within groups changed with depth in a pattern related to their mean size: the cell volume of the smallest group increased the most with depth while the cell volume of the largest group decreased the most. The vertical alignment of phytoplankton groups confirms that the DCM is not a homogeneous entity and indicates groups' preferences for different ecological niches within this layer.The deep chlorophyll maximum (DCM) is a subsurface layer enriched in chlorophyll (Chl) typical of stratified marine and freshwater bodies. It might be the result of diverse processes and may present different characteristics (Cullen 1982(Cullen , 2015. In temperate areas, the DCM disappears in winter when mixing takes place and reappears after the spring bloom, when stratification is established. The dynamics of this kind of DCM have been described in the literature (Estrada et al. 1993;Mignot et al. 2014). Briefly, winter surface waters replete with nutrients start stratifying after the air-water heat balance becomes negative (Sverdrup 1953;Taylor and Ferrari 2011) producing the spring bloom in temperate areas (although this classical approach has been challenged by Behrenfeld 2010). At this moment, the abundant phytoplankton accumulates very close to the surface, limiting the irradiance immediately below and inducing the synthesis of pigments by the deeper phytoplankton and the formation of a shallow DCM that might not correspond to a biomass maximum. However, this is a very dynamic situation because phytoplankton quickly (days-weeks) consume the nutrients from the well illuminated layers becoming less abundant at surface and concentrating at depth. This process originates a deeper DCM, coinciding with the nutricline ...

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Temperature-dependent growth and photophysiology of prokaryotic and eukaryotic oceanic picophytoplankton

Cited by 40 publications

References 59 publications

Phytoplankton σPSII and Excitation Dissipation; Implications for Estimates of Primary Productivity

Phytoplankton σPSII and Excitation Dissipation; Implications for Estimates of Primary Productivity

Thermal Performance Curves of Functional Traits Aid Understanding of Thermally Induced Changes in Diatom-Mediated Biogeochemical Fluxes

Distribution of phytoplankton groups within the deep chlorophyll maximum

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