Light capture and pigment diversity in marine and freshwater cryptophytes

Cunningham, Brady R.; Greenwold, Matthew J.; Lachenmyer, Eric M.; Heidenreich, Kristin M.; Davis, Abigail C.; Dudycha, Jeffry L.; Richardson, Tammi L.

doi:10.1111/jpy.12816

Cited by 36 publications

(56 citation statements)

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“…Thirty-two are named species, two are different strains of one species (Cryptomonas pyrenoidifera), eight are strains identified to a genus and two are unidentified strains; in total, these strains represent at least 12 genera (electronic supplementary material, table S1). Phenotypic characteristics (whole-cell absorption spectra, cell size measurements, pigment concentrations, phycobiliprotein absorption spectra and PUR values) for 33 of the strains in this study were previously reported in Cunningham et al [14]. Specific characteristics of those strains plus the nine additional strains that we measured are listed in the electronic supplementary material, table S1.…”

Section: (A) Data Collectionmentioning

confidence: 73%

“…Phenotypic measurements were taken during exponential phase as determined by cell counts. Detailed culture conditions, methods for all phenotypic measurements and procedures for DNA extraction, polymerase chain reaction (PCR) amplification and sequencing are listed in the electronic supplementary material, S1 and follow Cunningham et al [14].…”

Section: (A) Data Collectionmentioning

confidence: 99%

“…Molecular sequence data for the 42 strains consisted of the plastid ribulose bisphosphate carboxylase, large subunit (rbcL) and nuclear small subunit (SSU) and partial large subunit (LSU) rDNA nucleotide sequences collected following Johnson et al [35], Marin et al [36], Hoef-Emden [37] and Cunningham et al [14]. Methods for DNA extraction, PCR amplification and sequencing are detailed in the electronic supplementary material, S1.…”

Section: (B) Time-proportional Phylogeniesmentioning

confidence: 99%

“…A reoccurring issue with SSU and LSU cryptophyte phylogenies is that the backbone branches connecting clades 2 -5 are generally short and lack strong support (electronic supplementary material, figure S2; [14,37,48]), potentially reflecting an ancient period of rapid diversification. Our rbcL phylogeny, however, has relatively long backbone branches with moderate to strong support.…”

Section: (D) Ancestral State Estimatesmentioning

confidence: 99%

“…As a consequence, we have a relatively poor overall understanding of the diversification of light capture in comparison to other types of resource acquisition. Recently, we calculated PUR for 33 strains of cryptophyte algae grown under the same light conditions (PAR) in laboratory incubators [14]. We found that PUR varied nearly threefold across the phylum, with substantial variation even within some genera (Cryptomonas, Hemiselmis and Chroomonas).…”

Section: Introductionmentioning

confidence: 96%

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Diversification of light capture ability was accompanied by the evolution of phycobiliproteins in cryptophyte algae

et al. 2019

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Evolutionary biologists have long sought to identify phenotypic traits whose evolution enhances an organism's performance in its environment. Diversification of traits related to resource acquisition can occur owing to spatial or temporal resource heterogeneity. We examined the ability to capture light in the Cryptophyta, a phylum of single-celled eukaryotic algae with diverse photosynthetic pigments, to better understand how acquisition of an abiotic resource may be associated with diversification. Cryptophytes originated through secondary endosymbiosis between an unknown eukaryotic host and a red algal symbiont. This merger resulted in distinctive pigment–protein complexes, the cryptophyte phycobiliproteins, which are the products of genes from both ancestors. These novel complexes may have facilitated diversification across environments where the spectrum of light available for photosynthesis varies widely. We measured light capture and pigments under controlled conditions in a phenotypically and phylogenetically diverse collection of cryptophytes. Using phylogenetic comparative methods, we found that phycobiliprotein characteristics were evolutionarily associated with diversification of light capture in cryptophytes, while non-phycobiliprotein pigments were not. Furthermore, phycobiliproteins were evolutionarily labile with repeated transitions and reversals. Thus, the endosymbiotic origin of cryptophyte phycobiliproteins provided an evolutionary spark that drove diversification of light capture, the resource that is the foundation of photosynthesis.

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Section: (A) Data Collectionmentioning

confidence: 73%

Section: (A) Data Collectionmentioning

confidence: 99%

Section: (B) Time-proportional Phylogeniesmentioning

confidence: 99%

Section: (D) Ancestral State Estimatesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 96%

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Diversification of light capture ability was accompanied by the evolution of phycobiliproteins in cryptophyte algae

et al. 2019

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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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Molecular structures reveal the origin of spectral variation in cryptophyte light harvesting antenna proteins

et al. 2023

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In addition to their membrane‐bound chlorophyll a/c light‐harvesting antenna, the cryptophyte algae have evolved a unique phycobiliprotein antenna system located in the thylakoid lumen. The basic unit of this antenna consists of two copies of an αβ protomer where the α and β subunits scaffold different combinations of a limited number of linear tetrapyrrole chromophores. While the β subunit is highly conserved, encoded by a single plastid gene, the nuclear‐encoded α subunits have evolved diversified multigene families. It is still unclear how this sequence diversity results in the spectral diversity of the mature proteins. By careful examination of three newly determined crystal structures in comparison with three previously obtained, we show how the α subunit amino acid sequences control chromophore conformations and hence spectral properties even when the chromophores are identical. Previously we have shown that α subunits control the quaternary structure of the mature αβ.αβ complex (either open or closed), however, each species appeared to only harbor a single quaternary form. Here we show that species of the Hemiselmis genus contain expressed α subunit genes that encode both distinct quaternary structures. Finally, we have discovered a common single‐copy gene (expressed into protein) consisting of tandem copies of a small α subunit that could potentially scaffold pairs of light harvesting units. Together, our results show how the diversity of the multigene α subunit family produces a range of mature cryptophyte antenna proteins with differing spectral properties, and the potential for minor forms that could contribute to acclimation to varying light regimes.

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Light capture and pigment diversity in marine and freshwater cryptophytes

Cited by 36 publications

References 50 publications

Diversification of light capture ability was accompanied by the evolution of phycobiliproteins in cryptophyte algae

Diversification of light capture ability was accompanied by the evolution of phycobiliproteins in cryptophyte algae

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

Molecular structures reveal the origin of spectral variation in cryptophyte light harvesting antenna proteins

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