High-resolution Molecular Structures Illuminate the Evolution of a Novel Light-harvesting Antenna

Beverley Greena, Chang Ying Tenga,b , Stephen Harropc, Krystyna Wilkc, Naoko Onoderad, Kerstin Hoef-Emdene, Roger HillereJohn Archibaldd, Gregory Scholesg, Paul Curmic
a
Botany Dept., University of British Columbia,Vancouver, B.C., Canada V6T 1Z4; bLife Sciences Dept., Ludong University, Yantai, Shandong, China; cSchool of Physics, University of New South Wales, Australia 2052, dDepartment of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada, eBotanical Institute, Universität zu Köln, Köln 50674, Germany; fBiology Dept., Macquarie University, Australia 2109; gChemistry Dept., Princeton, USA.

Cryptophyte algae acquired their plastids from a red alga by secondary endo-symbiosis along with many nuclear-encoded genes for plastid proteins, including the membrane-intrinsic LHC family. However, during the process of integrating the plastid the cryptophytes lost the phycobilisome, the other light-harvesting system of the red alga, and evolved a completely novel antenna system unique to them. Genomic, transcriptomic and proteomic data show that a number of evolutionary mechanisms were involved in the transition between these two bilin-based antennas. Gene loss: all  the phycobilisome proteins except the phycoerythrin b subunit; Gene gain: a small nuclear-encoded protein (“new α” subunit) with no homologs in any other organism. Result: a tetrameric (α1β.α2β) phycobiliprotein unique to cryptophytes, where a subunit interactions play the major role in determining its 3D structure(1). Recombination led to the acquisition of tripartite targeting sequences  resulting in the relocation of assembled tetramers into the thylakoid lumen. Gene duplication/divergence gave families of a subunit genes with a surprising amount of diversity. In the genus Hemiselmis, a single amino acid insertion in the α subunit sequence resulted in a large conformational change of the tetramer and loss of electronic coupling (2) but with little effect on the conformation of the basic αβ dimer and no reported physiological consequences.

However, normal sequences are still expressed at a low level, which raises the possibility of quantum switching in response to environmental conditions. Examination of recently-determined three-dimensional structures suggest that much of the sequence diversity could be accomodated on surface loops and free N-termini. Although the β subunit sequences are almost identical to those of the red algal ancestor, there is one major change in secondary structure in the absence of sequence differences. Rather than considering competition and selection at the organismal level to explain evolution of this antenna, perhaps competition between α subunits for binding to β subunits played the major role. Was the acquisition of the new gene that became the α subunit actually the driver for the disintegraton of the phycobilisome?

References

[1] S. Harrop et al., PNAS 2014, E2666–E2675.
[2] P.A. Arptin et al., J. Phys. Chem. B 2015, 119, 10025-10034
[3] Supported by DARPA-QuBE, NSERC, ARC, US-DOE, Moore Foundation.