Blue light reduces photosynthetic efficiency of cyanobacteria through an imbalance between photosystems I and II

Luimstra, Veerle M.; Schuurmans, J. Merijn; Verschoor, Antonie M.; Hellingwerf, Klaas J.; Huisman, Jef; Matthijs, H.C.P.

doi:10.1007/s11120-018-0561-5

Cited by 123 publications

(127 citation statements)

References 76 publications

(116 reference statements)

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“…That was not the case, however, because PBS‐containing cyanobacteria use blue light very inefficiently. This is commonly attributed to the low absorbance of blue light ≤450 nm by the PBS, which leads to an excitation imbalance between the photosystems PSI and PSII (Solhaug et al , Luimstra et al , ; Fig. ).…”

Section: Discussionmentioning

confidence: 99%

“…(D) The green alga Chlorella (green diamonds) has higher specific growth rates in blue light, whereas (E) the cyanobacterium Synechocystis (blue triangles) has higher specific growth rates in red light. Data in panels D and E are averages of three biological replicates AE SD, from experiments of Luimstra et al (2018). absorption of different wavelengths by phytoplankton, water, dissolved organic matter (gilvin), and suspended particles (tripton).…”

Section: The Modelmentioning

confidence: 99%

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Changes in water color shift competition between phytoplankton species with contrasting light‐harvesting strategies

Luimstra

Verspagen

et al. 2020

Ecology

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The color of many lakes and seas is changing, which is likely to affect the species composition of freshwater and marine phytoplankton communities. For example, cyanobacteria with phycobilisomes as light‐harvesting antennae can effectively utilize green or orange‐red light. However, recent studies show that they use blue light much less efficiently than phytoplankton species with chlorophyll‐based light‐harvesting complexes, even though both phytoplankton groups may absorb blue light to a similar extent. Can we advance ecological theory to predict how these differences in light‐harvesting strategy affect competition between phytoplankton species? Here, we develop a new resource competition model in which the absorption and utilization efficiency of different colors of light are varied independently. The model was parameterized using monoculture experiments with a freshwater cyanobacterium and green alga, as representatives of phytoplankton with phycobilisome‐based vs. chlorophyll‐based light‐harvesting antennae. The parameterized model was subsequently tested in a series of competition experiments. In agreement with the model predictions, the green alga won the competition in blue light whereas the cyanobacterium won in red light, irrespective of the initial relative abundances of the species. These results are in line with observed changes in phytoplankton community structure in response to lake brownification. Similarly, in marine waters, the model predicts dominance of Prochlorococcus with chlorophyll‐based light‐harvesting complexes in blue light but dominance of Synechococcus with phycobilisomes in green light, with a broad range of coexistence in between. These predictions agree well with the known biogeographical distributions of these two highly abundant marine taxa. Our results offer a novel trait‐based approach to understand and predict competition between phytoplankton species with different photosynthetic pigments and light‐harvesting strategies.

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Section: Discussionmentioning

confidence: 99%

Section: The Modelmentioning

confidence: 99%

Changes in water color shift competition between phytoplankton species with contrasting light‐harvesting strategies

Luimstra

Verspagen

et al. 2020

Ecology

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“…Hence, cyanobacteria absorb blue light ≤450 nm. Yet, contrary to green algae and plants, PBS‐containing cyanobacteria have much lower rates of photosynthesis and growth in blue light than in the other light colors absorbed by their photosynthetic pigments (Lemasson et al , Pulich and van Baalen , Wyman and Fay , Jørgensen et al , Wilde et al , Tyystjärvi et al , Wang et al , Singh et al , Chen et al , Choi et al , Bland and Angenent , Luimstra et al ). As a consequence, PBS‐containing cyanobacteria can be strong competitors in cyan, green or orange light absorbed by their PBS, but they are very poor competitors in blue light ≤450 nm in comparison to photosynthetic organisms with chlorophyll‐based light‐harvesting complexes (Luimstra et al ).…”

Section: Introductionmentioning

confidence: 99%

“…In contrast to green algae and plants, PBS‐containing cyanobacteria invest much more of their Chl a in PSI than in PSII (e.g. Myers et al , Fujita , Luimstra et al ). As a consequence, PSI will absorb more blue light than PSII.…”

Section: Introductionmentioning

confidence: 99%

Blue light induces major changes in the gene expression profile of the cyanobacterium Synechocystis sp. PCC 6803

Luimstra

Schuurmans

Hellingwerf

et al. 2020

Physiologia Plantarum

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Although cyanobacteria absorb blue light, they use it less efficiently for photosynthesis than other colors absorbed by their photosynthetic pigments. A plausible explanation for this enigmatic phenomenon is that blue light is not absorbed by phycobilisomes and, hence, causes an excitation shortage at photosystem II (PSII). This hypothesis is supported by recent physiological studies, but a comprehensive understanding of the underlying changes in gene expression is still lacking. In this study, we investigate how a switch from artificial white light to blue, orange or red light affects the transcriptome of the cyanobacterium Synechocystis sp. PCC 6803. In total, 145 genes were significantly regulated in response to blue light, whereas only a few genes responded to orange and red light. In particular, genes encoding the D1 and D2 proteins of PSII, the PSII chlorophyllbinding protein CP47 and genes involved in PSII repair were upregulated in blue light, whereas none of the photosystem I (PSI) genes responded to blue light. These changes were accompanied by a decreasing PSI:PSII ratio. Furthermore, many genes involved in gene transcription and translation and several ATP synthase genes were transiently downregulated, concurrent with a temporarily decreased growth rate in blue light. After 6-7 days, when cell densities had strongly declined, the growth rate recovered and the expression of these growth-related genes returned to initial levels. Hence, blue light induces major changes in the transcriptome of cyanobacteria, in an attempt to increase the photosynthetic activity of PSII and cope with the adverse growth conditions imposed by blue light.

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“…5). Also, although the absorption spectra of Nannochloropsis and Cyanobium overlap in the blue part of the spectrum (400-470 nm range), recent work shows that species with chlorophyll-based light-harvesting complexes such as Nannochloropsis use absorbed blue light much more efficiently than cyanobacteria with phycobilisomes as lightharvesting antennae such as Cyanobium (Luimstra et al 2018(Luimstra et al , 2019. Hence, in total, Cyanobium is more effective in the utilization of orange light (600-650 nm), whereas Nannochloropsis is more effective in the utilization of blue (400-470 nm) and red light (660-700 nm).…”

Section: Mechanisms Of Coexistencementioning

confidence: 99%

Stable Coexistence of Equivalent Nutrient Competitors Through Niche Differentiation in the Light Spectrum

Burson¹,

Stomp²,

Mekkes³

et al. 2020

Bulletin Ecologic Soc America

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Niche-based theories and the neutral theory of biodiversity differ in their predictions of how the species composition of natural communities will respond to changes in nutrient availability. This is an issue of major environmental relevance, as many ecosystems have experienced changes in nitrogen (N) and phosphorus (P) due to anthropogenic manipulation of nutrient loading. To understand how changes in N and P limitation may impact community structure, we conducted laboratory competition experiments using a multispecies phytoplankton community sampled from the North Sea. Results showed that picocyanobacteria (Cyanobium sp.) won the competition under N limitation, while picocyanobacteria and nonmotile nanophytoplankton (Nannochloropsis sp.) coexisted at equal abundances under P limitation. Additional experiments using isolated monocultures confirmed that Cyanobium sp. depleted N to lower levels than Nannochloropsis sp., but that both species had nearly identical P requirements, suggesting a potential for neutral coexistence under P-limited conditions. Pairwise competition experiments with the two isolates seemed to support the consistency of these results, but P limitation resulted in stable species coexistence irrespective of the initial conditions rather than the random drift of species abundances predicted by neutral theory. Comparison of the light absorption spectra indicates that coexistence of the two species was stabilized through differential use of the underwater light spectrum. Our results provide an interesting experimental example of modern coexistence theory, where species were equal competitors in one niche dimension but their competitive traits differed in other niche dimensions, thus enabling stable species coexistence on a single limiting nutrient through niche differentiation in the light spectrum.

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Blue light reduces photosynthetic efficiency of cyanobacteria through an imbalance between photosystems I and II

Cited by 123 publications

References 76 publications

Changes in water color shift competition between phytoplankton species with contrasting light‐harvesting strategies

Changes in water color shift competition between phytoplankton species with contrasting light‐harvesting strategies

Blue light induces major changes in the gene expression profile of the cyanobacterium Synechocystis sp. PCC 6803

Stable Coexistence of Equivalent Nutrient Competitors Through Niche Differentiation in the Light Spectrum

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