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Award Abstract # 1542555
Dimensions: Links Between Spectral Irradiance and Cryptophyte Biodiversity in Environments from Ponds to Oceans

NSF Org: DEB
Division Of Environmental Biology
Recipient: UNIVERSITY OF SOUTH CAROLINA
Initial Amendment Date: September 1, 2015
Latest Amendment Date: January 28, 2016
Award Number: 1542555
Award Instrument: Standard Grant
Program Manager: Michael Sieracki
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: September 1, 2015
End Date: August 31, 2021 (Estimated)
Total Intended Award Amount: $1,956,478.00
Total Awarded Amount to Date: $1,960,535.00
Funds Obligated to Date: FY 2015 = $1,956,478.00
FY 2016 = $4,057.00
History of Investigator:
  • Tammi Richardson (Principal Investigator)
    richardson@biol.sc.edu
  • Jeffry Dudycha (Co-Principal Investigator)
Recipient Sponsored Research Office: University of South Carolina at Columbia
1600 HAMPTON ST
COLUMBIA
SC  US  29208-3403
(803)777-7093
Sponsor Congressional District: 06
Primary Place of Performance: University of South Carolina at Columbia
Columbia
SC  US  29208-0001
Primary Place of Performance
Congressional District:
06
Unique Entity Identifier (UEI): J22LNTMEDP73
Parent UEI: Q93ZDA59ZAR5
NSF Program(s): Dimensions of Biodiversity
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
01001617DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1097, 1650, 9117, 9150
Program Element Code(s): 796800
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

In aquatic environments, microscopic algae known as phytoplankton are important primary producers. Through photosynthesis, these organisms fix carbon dioxide into the organic carbon molecules that fuel life in ponds, rivers, lakes and oceans. The color of light available for photosynthesis varies among environments, e.g., the deep blue ocean vs. a black water river. In order to live in a particular environment, phytoplankton must have photosynthetic pigments that are tuned to absorbing the colors of light available. This project focuses on the cryptophytes, a relatively uncharacterized group of phytoplankton, that are abundant in a wide range of aquatic habitats ranging from small ponds to oceans. Cryptophytes use phycobilin pigments to capture light energy; these pigments allow cryptophytes to photosynthesize in light environments that are poorly exploited by other types of algae. The project goals are: (1) to characterize the ecological distribution and taxonomic diversification of cryptophyte species, (2) to determine the effectiveness of their light capture in different light environments, and (3) to characterize the molecular evolutionary pathways of critical light capture genes. Understanding these links is important to predicting how changes in land-use (like deforestation and urbanization, both of which impact the color of light in downstream watersheds) will affect aquatic productivity. This project will provide training for a post-doc, 2-4 graduate students, and 10 undergraduates. Through a partnership with Morris College and other University of South Carolina programs, underrepresented minorities will be recruited into summer fellowships. Novel cryptophyte strains will be deposited in living culture collections for use by other researchers.

This project's central question is deceptively simple: How do functional, genetic, and phylogenetic diversity interact in the ecological diversification of cryptophytes with respect to light environment? The researchers will conduct an integrative research program on the biodiversity of cryptophytes to understand how environmental variation in spectral irradiance is associated with the physiological diversity of light capture in cryptophytes in the context of their historical diversification. This work integrates several components: (1) Field sampling in water bodies ranging from small ponds to oceans to identify the specific light environments in which strains live, to determine the pigments that cryptophytes produce in those habitats, and to identify novel species; (2) Phenotypic studies to determine how variation in spectral irradiance (light color) influences light capture, photosynthesis, and growth of diverse taxa. These will also determine spectral absorption of phycobilins in strains throughout the cryptophyta; (3) Construction of a well-supported phylogeny based on sequencing nucleomorph genomes of ~200 strains; (4) Analyses of molecular evolution of key light capture genes, in particular those that encode the alpha and beta subunits of the cryptophyte phycobiliproteins, and those involved in the phycobilin synthesis pathway; (5) Experimental evolution to test the ability of diverse strains of cryptophytes to evolve into new light niches; (6) Experimental transcriptomics to identify the functional responses of diverse strains to variation in spectral irradiance; and (7) Phylogenetically-informed tests of the associations between habitat, molecular evolution, organismal performance, and spectral absorbance. Ultimately, this work should be a transformative contribution to our understanding of the diversification of photosynthesis and the role of that diversification in the ecological distribution of cryptophytes.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Cunningham, B.R., M.J. Greenwold, E.M. Lachenmyer, K.M. Heidenreich, A.C. Davis, J.L. Dudycha and T.L. Richardson "Light capture and pigment diversity in marine and freshwater cryptophytes." Journal of Phycology , v.55 , 2019 doi:10.111/jpy.12816
Cunningham, B.R., M.J. Greenwold, E.M. Lachenmyer, K.M. Heidenreich*, A.C. Davis, J.L. Dudycha and T.L. Richardson "Light capture and pigment diversity in marine and freshwater cryptophytes." Journal of Phycology , v.55 , 2018 , p.552-564
Faulkner, S.T., C.M. Rekully, E.M. Lachenmyer, E. Kara, T.L. Richardson, T.J. Shaw, and M.L. Myrick. "Single-cell and bulk fluorescence excitation signatures of seven phytoplankton species during nitrogen depletion and resupply" Applied Spectroscopy , v.73 , 2018 doi: 10.1177/0003702818812090
Greenwold, MJ, B.R. Cunningham, E.M. Lachenmyer, J.M. Pullman, T.L. Richardson and J.L. Dudycha "Diversification of light capture ability was accompanied by the evolution of phycobiliproteins in cryptophyte algae" Proceedings of the Royal Society Bdoi.org/10.1098/rspb.2019.0655 , 2019
Greenwold, M.J., B.R. Cunningham, E.M. Lachenmyer, J. Pullman, T.L. Richardson and J.L. Dudycha "Diversification of light capture ability was accompanied by the evolution of phycobiliproteins in cryptophyte algae" Proceedings of the Royal Society B , v.286 , 2019 http://dx.doi.org/10.1098/rspb.2019.0655
Heidenreich, K.M. and T.L. Richardson "PHOTOPIGMENT, ABSORPTION, AND GROWTH RESPONSES OF MARINECRYPTOPHYTES TO VARYING SPECTRAL IRRADIANCE" Journal of Phycology , v.56 , 2020 , p.507 DOI: 10.1111/jpy.12962
K. Heidenreich and T. Richardson "Photopigment, absorption, and growth responses of marine cryptophytes to varying spectral irradiance" Journal of Phycology , 2020 DOI: 10.1111/jpy.12962
Matthew J. Greenwold, Brady R. Cunningham, Eric M. Lachenmyer,John Michael Pullman, Tammi L. Richardson and Jeffry L. Dudycha "Diversification of light capture abilitywas accompanied by the evolution ofphycobiliproteins in cryptophyte algae" Proceedings of the Royal Society B , v.286 , 2019 http://dx.doi.org/10.1098/rspb.2019.0655

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Since 2015, through funding from the NSF?s Dimensions of Biodiversity program, we have been studying a fascinating group of microalgae known as cryptophytes. As the name implies, cryptophytes are ?cryptic?. They are relatively understudied compared to other phytoplankton taxa, yet they are ubiquitous and can be found in environments ranging from tea-colored ponds to the blue-water open ocean. Our Dimensions grant explored the genetic, phylogenetic, and functional diversity of cryptophytes as related to their diversification into differently-colored light environments. We were particularly interested in the role of specialized pigments contained in cryptophytes, called phycobiliproteins (PBPs).

The first step of our investigation was to produce a molecular phylogeny (a family tree) using 99 strains of cryptophytes, and a database of phenotypic characteristics (cell size, pigment composition, light absorption characteristics, etc.). These allowed us to reclassify one species to a different genus, to update PBP diversity within the genus Hemiselmis, to classify a previously unidentified strain CCMP 2293 into the genus Falcomonas, and a previously unidentified strain CCMP 3175 into a clade with Chroomonas species. We also produced a statistical model using PBP type, cellular concentration, and cryptophyte habitat; these factors together correctly predicted 70.6% of clade composition. We found that the non-PBP pigments (chl-a, chl-c2, a-carotene and alloxanthin) did not contribute significantly to clade classification (i.e., they played no role in determining which species were related to one another). Further work showed that the evolutionary path of different cryptophyte species was determined by which PBP pigments they contained. In particular, we found that part of the PBP molecule, the beta subunit, has been modified over evolutionary time through mechanisms like gene loss and gene duplication, that results in the variety of PBP pigments we see in cryptophytes today.

Our study of functional diversity in the cryptophytes explored phenotypic plasticity (flexibility) in cryptophytes, specifically their potential for ?complementary chromatic adaptation?. The theory posits that pigments in a photosynthetic organism should be optimally tuned to absorbing the available wavelengths of light and, if moved to a new environment, the organism will alter its pigmentation to match its new surroundings. When shifted to a new spectral environment of equal light intensity, we found significant changes in pigment composition of 8 cryptophytes we studied, but not always in ways that would be considered ?complementary?. When Storeatula sp. was shifted from a full spectrum to a green light environment it significantly increased its concentration of (green-light-absorbing) Cr-PE 545, which would be considered a ?complementary? chromatic acclimation response.  However, both Storeatula sp. and Rhodomonas salina significantly reduced their cellular concentrations of Cr-PE 545, chl-a, and chl-c2 when shifted from full spectrum to blue light -presumably because there was sufficient energy to fuel photosynthesis and growth when all available photons were blue. Results of this study also showed that cryptophytes may have the ability to tune their PBPs to the available wavelengths of light, which would give them a great ecological advantage if their habitat changed color due to deforestation, urbanization, or other anthropogenic disturbance.

Our most recent work has focused on gene expression in a cryptophyte called Rhodomonas salina, and how expression changed when cultures were exposed to different colors of light. We found that pigment-related gene expression did not vary with light color, suggesting that any regulation may occur post-transcriptionally. We did find that the expression of non-photosynthetic physiological processes, like glycolysis (respiration) and sexual reproduction, may be in some way controlled by the color of light in the cryptophyte environment. 

Finally, we examined the potential for evolutionary tradeoffs in the photosynthetic physiology of cryptophytes. Elucidating potential trade-offs among photosynthetic traits provides information on different ecological and physiological strategies for light capture. We investigated potential trade-offs by measuring photosynthetic traits for 15 species of cryptophytes. We constructed photosynthesis vs. irradiance (P-E) curves and rapid light curves (RLC) to estimate  traits that characterize photosynthetic performance and electron transport rate. Testing the gleaner-opportunist framework for resource acquisition  tradeoffs, we found no evidence for trade-offs between maximum rate of photosynthesis and the sensitivity of photosynthesis to light limitation, nor between maximum relative electron transport rate and the sensitivity of electron transport to light limitation. We also found no evidence of a power-efficiency tradeoff among photosynthetic parameters in cryptophytes. Contrary to predicted negative relationships, we observed a positive correlation between the  maximum photosynthetic rate and photosynthetic sensitivity to light intensity. We propose that  trade-offs may exist between photosynthetic traits and other resource acquisition traits, or that  the emergence of photosynthetic trade-offs may be context-dependent. 

This project has contributed to the training and professional development of the next generation of scientists. In sum, we have trained 2 postdocs (both of whom have permanent employment now), 3 graduate students, and at least 16 undergraduate students in the general field of phytoplankton ecology and evolutionary biology.


Last Modified: 01/13/2022
Modified by: Tammi L Richardson

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