skip to main content


Title: Interplay between differentially expressed enzymes contributes to light color acclimation in marine Synechococcus

MarineSynechococcus, a globally important group of cyanobacteria, thrives in various light niches in part due to its varied photosynthetic light-harvesting pigments. ManySynechococcusstrains use a process known as chromatic acclimation to optimize the ratio of two chromophores, green-light–absorbing phycoerythrobilin (PEB) and blue-light–absorbing phycourobilin (PUB), within their light-harvesting complexes. A full mechanistic understanding of howSynechococcuscells tune their PEB to PUB ratio during chromatic acclimation has not yet been obtained. Here, we show that interplay between two enzymes named MpeY and MpeZ controls differential PEB and PUB covalent attachment to the same cysteine residue. MpeY attaches PEB to the light-harvesting protein MpeA in green light, while MpeZ attaches PUB to MpeA in blue light. We demonstrate that the ratio ofmpeYtompeZmRNA determines if PEB or PUB is attached. Additionally, strains encoding only MpeY or MpeZ do not acclimate. Examination of strains ofSynechococcusisolated from across the globe indicates that the interplay between MpeY and MpeZ uncovered here is a critical feature of chromatic acclimation for marineSynechococcusworldwide.

 
more » « less
Award ID(s):
1818187
NSF-PAR ID:
10087655
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Publisher / Repository:
Proceedings of the National Academy of Sciences
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
116
Issue:
13
ISSN:
0027-8424
Page Range / eLocation ID:
p. 6457-6462
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. MarineSynechococcuscyanobacteria owe their ubiquity in part to the wide pigment diversity of their light-harvesting complexes. In open ocean waters, cells predominantly possess sophisticated antennae with rods composed of phycocyanin and two types of phycoerythrins (PEI and PEII). Some strains are specialized for harvesting either green or blue light, while others can dynamically modify their light absorption spectrum to match the dominant ambient color. This process, called type IV chromatic acclimation (CA4), has been linked to the presence of a small genomic island occurring in two configurations (CA4-A and CA4-B). While the CA4-A process has been partially characterized, the CA4-B process has remained an enigma. Here we characterize the function of two members of the phycobilin lyase E/F clan, MpeW and MpeQ, inSynechococcussp. strain A15-62 and demonstrate their critical role in CA4-B. While MpeW, encoded in the CA4-B island and up-regulated in green light, attaches the green light-absorbing chromophore phycoerythrobilin to cysteine-83 of the PEII α-subunit in green light, MpeQ binds phycoerythrobilin and isomerizes it into the blue light-absorbing phycourobilin at the same site in blue light, reversing the relationship of MpeZ and MpeY in the CA4-A strain RS9916. Our data thus reveal key molecular differences between the two types of chromatic acclimaters, both highly abundant but occupying distinct complementary ecological niches in the ocean. They also support an evolutionary scenario whereby CA4-B island acquisition allowed former blue light specialists to become chromatic acclimaters, while former green light specialists would have acquired this capacity by gaining a CA4-A island.

     
    more » « less
  2. Benefits and trade-offs of blue/green chromatic acclimation (CA4) have received limited study. We investigated the energetic costs associated with executing chromatic acclimation using a fluorescence-based calculation of light use efficiency. Using laboratory cultures and artificial light environments, we show that the delayed response to acclimation known to occur in marine Synechococcus acclimating strains (generalists) in green light do not reduce light use efficiency in green light, but that only one generalist, RCC307, with a much smaller range of acclimation, had higher light use efficiency than blue and green light specialist strains. Generalists with a wider acclimation range either had the same or >30% lower light use efficiencies in blue and green light environments. From this work, we propose that advantages from CA4 may not be geared at direct competition with other Synechococcus specialists with fixed pigment types, but may serve to expand the ecological range of Synechococcus in spectral competition with other genera. As all eight Synechococcus strains tested had higher light use efficiency in green light, regardless of a fixed or flexible light harvesting strategy, we add evidence to the suitability of the Synechococcus genus to greener ocean niches, whether stable, or variable. 
    more » « less
  3. Abstract

    Light penetration through the ocean creates underwater light color niches and photosynthetic organisms use specific strategies to capture light in these niches. The selection pressure for some cyanobacteria strains in the genusSynechococcusthat change color to absorb either blue or green light (chromatic acclimaters, or generalists) is not well understood. Here, we tested the hypothesis that changes in ocean spectra brought about by mixing preferentially selects for generalists within aSynechococcuspopulation. We investigated ocean conditions that led to high proportions ofSynechococcusgeneralists versus specialists in a model ocean column, and compared simulations with in situ metagenomic and physical oceanographic data from major Bio‐GO‐SHIP cruises, supplemented with GEOTRACES and TARA Oceans, as well as the GOOS Argo Program and sea surface height from AVISO. We found that greater mixed layer depths selected for generalists in simulatedSynechococcuspopulations, but did not account for much of the variance in the partitioning of light‐harvesting strategies in situ. Rather, oceanographic signatures for upwelling areas and ocean fronts explained more of the variation betweenSynechococcusgeneralists and specialists in the ocean. Our results motivate further study of the in situ light environments of upwelling zones and ocean fronts, which are currently understudied as potential light‐driven niche habitats.

     
    more » « less
  4. Marine Synechococcus efficiently harvest available light for photosynthesis using complex antenna systems, called phycobilisomes, composed of an allophycocyanin core surrounded by rods, which in the open ocean are always constituted of phycocyanin and two phycoerythrin (PE) types: PEI and PEII. These cyanobacteria display a wide pigment diversity primarily resulting from differences in the ratio of the two chromophores bound to PEs, the green-light absorbing phycoerythrobilin and the blue-light absorbing phycourobilin. Prior to phycobiliprotein assembly, bilin lyases post-translationally catalyze the ligation of phycoerythrobilin to conserved cysteine residues on α- or β-subunits, whereas the closely related lyase-isomerases isomerize phycoerythrobilin to phycourobilin during the attachment reaction. MpeV was recently shown in Synechococcus sp. RS9916 to be a lyase-isomerase which doubly links phycourobilin to two cysteine residues (C50 and C61; hereafter C50, 61) on the β-subunit of both PEI and PEII. Here we show that Synechococcus sp. WH8020, which belongs to the same pigment type as RS9916, contains MpeV that demonstrates lyase-isomerase activity on the PEII β-subunit but only lyase activity on the PEI β-subunit. We also demonstrate that occurrence of a histidine at position 141 of the PEI β-subunit from WH8020, instead of a leucine in its counterpart from RS9916, prevents the isomerization activity by WH8020 MpeV, showing for the first time that both the substrate and the enzyme play a role in the isomerization reaction. We propose a structural-based mechanism for the role of H141 in blocking isomerization. More generally, the knowledge of the amino acid present at position 141 of the β-subunits may be used to predict which phycobilin is bound at C50, 61 of both PEI and PEII from marine Synechococcus strains. 
    more » « less
  5. The underwater light field of lakes, estuaries, and oceans may vary greatly in spectral composition. Phytoplankton in these environments must contain pigments that absorb the available colors of light. If spectral quality changes, acclimation to the new spectral environment would confer an ecological advantage in terms of photosynthesis and growth. Here, we explored the capacity of eight marine cryptophytes to adjust pigmentation in response to changes in spectral irradiance and related effects on light absorption, photosynthetically useable radiation (PUR), and growth rate. The pigment composition of all species changed in some way in response to shifts in spectral irradiance, but not all pigment changes could be considered advantageous in the context of chromatic acclimation. For most species, absorption by chl‐aand chl‐c2resulted in highest absorption in the blue region, highestPURvalues for blue‐light grown cells, and highest growth rates in blue light. The exception wasChroomonas mesostigmatica(CCMP1168), which contains a high percentage of Cryptophyte‐Phycocyanin (Cr‐PC) 645, absorbs strongly in the orange‐to‐red region of the spectrum, and grew fastest under red light. The position and magnitude of the maximum and secondary absorption peak of Cr‐PC569, the phycobiliprotein pigment ofHemiselmis cryptochromatica, varied with spectral irradiance. The underlying cause remains unknown, but may represent a mechanism by which cryptophytes optimize photon capture.

     
    more » « less