Abstract
Phycobilisomes are light-harvesting antenna complexes of cyanobacteria and red algae that are comprised of chromoproteins called phycobiliproteins. PBS core structures are made up of allophycocyanin subunits. Halomicronema hongdechloris (H. hongdechloris) is one of the cyanobacteria that produce chlorophyll f (Chl f) under far-red light and is regulated by the Far-Red Light Photoacclimation gene cluster. There are five genes encoding APC in this specific gene cluster, and they are responsible for assembling the red-shifted PBS in H. hongdechloris grown under far-red light. In this study, the five apc genes located in the FaRLiP gene cluster were heterologously expressed in an Escherichia coli reconstitution system. The canonical APC-encoding genes were also constructed in the same system for comparison. Additionally, five annotated phycobiliprotein lyase-encoding genes (cpcS) from the H. hongdechloris genome were phylogenetically classified and experimentally tested for their catalytic properties including their contribution to the shifted absorption of PBS. Through analysis of recombinant proteins, we determined that the heterodimer of CpcS-I and CpcU are able to ligate a chromophore to the APC-α/APC-β subunits. We discuss some hypotheses towards understanding the roles of the specialised APC and contributions of PBP lyases.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- Aa:
-
Amino acid(s)
- AP-B(ApcD):
-
Allophycocyanin B
- APC:
-
Allophycocyanin
- APCx:
-
Represents all APC subunits studied in this work
- Amp :
-
Ampicillin
- Chlorm :
-
Chloramphenicol
- Chl f :
-
Chlorophyll f
- ChlF:
-
The gene encoding the Chl f synthase
- CpcS:
-
S-type phycobilin lyase
- FaRLiP:
-
Far-Red Light Photoacclimation
- H. Hongdechloris :
-
Halomicronema hongdechloris
- IPTG:
-
Isopropyl β-D-thiogalactoside
- JTT:
-
Jones-Thornton-Taylor
- LCM (ApcE):
-
Core-membrane linker
- PBPs:
-
Phycobiliproteins
- PBS:
-
Phycobilisomes
- PCB:
-
Phycocyanobilin
- pCD-Sx:
-
PCDFDuet-single-cpcS
- pCDSxSy:
-
PCDFDuet-two-cpcS genes
- Spec :
-
Spectinomycin
References
Berkelman TR, Lagarias JC (1986) Visualization of bilin-linked peptides and proteins in polyacrylamide gels. Anal Biochem 156:194–201. https://doi.org/10.1016/0003-2697(86)90173-9
Bryant DA, Canniffe DP (2018) How nature designs light-harvesting antenna systems: design principles and functional realization in chlorophototrophic prokaryotes. J Phys b: at Mol Opt Phys 51:033001. https://doi.org/10.1088/1361-6455/aa9c3c
Chen M, Hernandez-Prieto MA, Loughlin PC, Li Y, Willows RD (2019) Genome and proteome of the chlorophyll f-producing cyanobacterium Halomicronema hongdechloris: adaptative proteomic shifts under different light conditions. BMC Genomics 20:207. https://doi.org/10.1186/s12864-019-5587-3
Chen M, Li Y, Birch D, Willows RD (2012) A cyanobacterium that contains chlorophyll f-a red-absorbing photopigment. FEBS Lett 586:3249–3254. https://doi.org/10.1016/j.febslet.2012.06.045
Chen M, Schliep M, Willows RD, Cai ZL, Neilan BA, Scheer H (2010) A red-shifted chlorophyll. Science 329:1318–1319. https://doi.org/10.1126/science.1191127
Gan F, Bryant DA (2015) Adaptive and acclimative responses of cyanobacteria to far-red light. Environ Microbiol 17:3450–3465. https://doi.org/10.1111/1462-2920.12992
Gan F, Shen G, Bryant DA (2014) Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria. Life 5:4–24. https://doi.org/10.3390/life5010004
Glazer AN (1989) Light guides: directional energy transfer in a photosynthetic antenna. J Biol Chem 264:1–4
Grossman AR (2003) A molecular understanding of complementary chromatic adaptation. Photosynth Res 76:207–215. https://doi.org/10.1023/A:1024907330878
Herrera-Salgado P, Leyva-Castillo LE, Rios-Castro E, Gomez-Lojero C (2018) Complementary chromatic and far-red photoacclimations in Synechococcus ATCC 29403 (PCC 7335). I: the phycobilisomes, a proteomic approach. Photosynth Res 138:39–56. https://doi.org/10.1007/s11120-018-0536-6
Ho MY, Gan F, She G, Zhao C, Bryant DA (2017) Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335: I. Regulation of FaRLiP gene expression. Photosynth Res 131:173–186. https://doi.org/10.1007/s11120-016-0309-z
Kronfel CM, Kuzin AP, Forouhar F, Biswas A, Su M, Lew S, Seetharaman J, Xiao R, Everett JK, Ma LC, Acton TB (2013) Structural and biochemical characterization of the bilin lyase CpcS from Thermosynechococcus Elongatus. Biochemistry 52:8663–8676. https://doi.org/10.1021/bi401192z
Kupka M, Zhang J, Fu WL, Tu JM, Böhm S, Su P, Chen Y, Zhou M, Scheer H, Zhao KH (2009) Catalytic mechanism of s-type phycobiliprotein lyase: chaperone-like action and functional amino acid residues. J Biol Chem 284:36405–36414. https://doi.org/10.1074/jbc.M109.056382
Li Y, Lin Y, Garvey CJ, Birch D, Corkery RW, Loughlin PC, Scheer H, Willows RD, Chen M (2016) Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. Biochim Biophys Acta 1857:107–114. https://doi.org/10.1016/j.bbabio.2015.10.009
Ma J, You X, Sun S, Wang X, Qin S, Sui SF (2020) Structural basis of energy transfer in porphyridium purpureum phycobilisome. Nature 579:146–151
Miao D, Ding WL, Zhao BQ, Lu L, Xu QZ, Scheer H, Zhao KH (2016) Adapting photosynthesis to the near-infrared: non-covalent binding of phycocyanobilin provides an extreme spectral red-shift to phycobilisome core-membrane linker from Synechococcus sp. PCC 7335. Biochim Biophys Acta 1857:688–694
Peng PP, Dong LL, Sun YF, Zeng XL, Ding WL, Scheer H, Yang X, Zhao KH (2014) The structure of allophycocyanin B from Synechocystis PCC 6803 reveals the structural basis for the extreme redshift of the terminal emitter in phycobilisomes. Acta Crystallogr D Biol Crystallogr 70:2558–2569. https://doi.org/10.1107/S1399004714015776
Saunee NA, Williams SR, Bryant DA, Schluchter WM (2008) Biogenesis of phycobiliproteins: II. CpcS-I and CpcU comprise the heterodimeric bilin lyase that attaches phycocyanobilin to CYS-82 of β-phycocyanin and CYS-81 of allophycocyanin subunits in Synechococcus sp. PCC 7002. J Biol Chem 283:7513–7522. https://doi.org/10.1074/jbc.M708165200
Scheer H, Zhao KH (2008) Biliprotein maturation: the chromophore attachment. Mol Microbiol 68:263–276. https://doi.org/10.1111/j.1365-2958.2008.06160.x
Shen G, Saunee NA Williams SR, Gallo EF, Schluchter WM, Bryant DA (2006) Identification and characterization of a new class of bilin lyase: the cpcT gene encodes a bilin lyase responsible for attachment of phycocyanobilin to Cys-153 on the β-subunit of phycocyanin in Synechococcus sp. PCC 7002. J Biol Chem 281:17768–17778. https://doi.org/10.1074/jbc.M602563200.
Shen G, Schluchter WM, Bryant DA (2008) Biogenesis of phycobiliproteins: I. cpcS-I and cpcU mutants of the cyanobacterium Synechococcus sp. PCC 7002 define a heterodimeric phyococyanobilin lyase specific for β-phycocyanin and allophycocyanin subunits.J Biol Chem 283:7503–7512. https://doi.org/10.1074/jbc.M708164200.
Singh NK, Sonani RR, Rastogi RP, Madamwar D (2015) The Phycobilisomes: an early requisite for efficient photosynthesis in cyanobacteria. EXCLI J 14:268–89. https://doi.org/10.17179/excli2014-723.
Soulier N, Laremore TN, Bryant DA (2020) Characterization of cyanobacterial allophycocyanins absorbing far-red light. Photosynth Res 145:189–207. https://doi.org/10.1007/s11120-020-00775-2
Sui SF (2021) Structure of phycobilisomes. Annu Rev Biophys 50:53–72. https://doi.org/10.1146/annurev-biophys-062920-063657
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) Mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Zhao KH, Deng MG, Zheng M, Zhou M, Parbel A, Storf M, Meyer M, Strohmann B, Scheer H (2000) Novel activity of a phycobiliprotein lyase: both the attachment of phycocyanobilin and the isomerization to phycoviolobilin are catalyzed by the proteins PecE and PecF encoded by the phycoerythrocyanin operon. FEBS Lett 469:9–13. https://doi.org/10.1016/s0014-5793(00)01245-x
Zhao KH, Su P, Li J, Tu JM, Zhou M, Bubenzer C, Scheer H (2006) Chromophore attachment to phycobiliprotein β-subunits: Phycocyanobilin: cysteine-β84 phycobiliprotein lyase activity of CpeS-like protein from Anabaena Sp. PCC7120. J Biol Chem 281:8573–8581. https://doi.org/10.1074/jbc.M513796200
Zhao KH, Zhang J, Tu JM, Bohm S, Ploscher M, Eichacker L, Bubenzer C et al (2007) Lyase activities of CpcS-and CpcT-like proteins from Nostoc PCC7120 and sequential reconstitution of binding sites of phycoerythrocyanin and phycocyanin β-subunits. J Biol Chem 282:34093–34103. https://doi.org/10.1074/jbc.M703038200
Zhou J, Gasparich GE, Stirewalt VL, de Lorimier R, Bryant DA (1992) The cpcE and cpcF genes of Synechococcus sp. PCC 7002. Construction and phenotypic characterization of interposon mutants. J Biol Chem 267:16138–16145 . https://doi.org/10.1016/S0021-9258(18)41978-3
Acknowledgements
This work is supported by ARC Projects CE140100015 and DP210102187. Authors thanks Dr. Tendo Mukasa Mugerwa, Dr. Amanda Huen from University of Sydney and Professor Robert Willows from Macquarie University for generous help and discussion in the Escherichia coli System reconstitution experimental process.
Funding
This study was supported by ARC Centre of Excellence for Translational Photosynthesis (CE140100015) and Discovery Project (DP210102187).
Author information
Authors and Affiliations
Contributions
MC initiated the main ideas. YL formalised the detail method and executed the experiments. MC conducted phylogenetic analysis. MC and YL contributed to data analysis and the writing of the paper.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Data availability
Not applicable.
Code availability
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Li, Y., Chen, M. The specificity of the bilin lyase CpcS for chromophore attachment to allophycocyanin in the chlorophyll f-containing cyanobacterium Halomicronima hongdechloris. Photosynth Res 151, 213–223 (2022). https://doi.org/10.1007/s11120-021-00878-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-021-00878-4