Extensive gain and loss of photosystem I subunits in chromerid algae, photosynthetic relatives of apicomplexans

Roman Sobotka,Aleš Horák,Heather J. Esson,Lenka Moravcová,Peter Koník,Petra Dufková,Eliška Trsková,Miroslav Oborník

doi:10.1038/s41598-017-13575-x

Abstract

In oxygenic photosynthesis the initial photochemical processes are carried out by photosystem I (PSI) and II (PSII). Although subunit composition varies between cyanobacterial and plastid photosystems, the core structures of PSI and PSII are conserved throughout photosynthetic eukaryotes. So far, the photosynthetic complexes have been characterised in only a small number of organisms. We performed in silico and biochemical studies to explore the organization and evolution of the photosynthetic apparatus in the chromerids Chromera velia and Vitrella brassicaformis, autotrophic relatives of apicomplexans. We catalogued the presence and location of genes coding for conserved subunits of the photosystems as well as cytochrome b6f and ATP synthase in chromerids and other phototrophs and performed a phylogenetic analysis. We then characterised the photosynthetic complexes of Chromera and Vitrella using 2D gels combined with mass-spectrometry and further analysed the purified Chromera PSI. Our data suggest that the photosynthetic apparatus of chromerids underwent unique structural changes. Both photosystems (as well as cytochrome b6f and ATP synthase) lost several canonical subunits, while PSI gained one superoxide dismutase (Vitrella) or two superoxide dismutases and several unknown proteins (Chromera) as new regular subunits. We discuss these results in light of the extraordinarily efficient photosynthetic processes described in Chromera.

Highlights

Photosystem I (PSI) and photosystem II (PSII) are large pigment-protein complexes, assembled from tens of subunits and harboring various cofactors, embedded in the thylakoid membranes of oxygenic phototrophs
The core of the PSII complex consists of four large proteins - D1, D2, CP47 and CP43 - that bind most of the chlorophyll molecules (~30) and most of the other cofactors
PSI composition in different taxa varies mostly due to the chlorophyll-binding, light-harvesting complexes associated with PSI that are present in eukaryotes but absent in cyanobacteria, where PSI is associated with phycobilisomes

Summary

Results and Discussion

Loss of plastid proteins associated with photosynthetic complexes. To obtain a broader view on the evolution of photosynthetic complexes we retrieved the amino acid sequences of 55 proteins associated with PSI, PSII, cytochrome b6f and ATP synthase from sequence databases (genes and accession numbers are given in Table S1, Supplementary Material). Chromera and Vitrella, in particular, have sustained several losses that have not occurred in the majority of other red plastids; these genes – namely psaI, psaJ, ycf[4], psbI, psbY, ycf12/psb[30], petL, petM, petN, atpD, atpE, atpF and atpG - are likely to have been lost in a recent common ancestor of the chromerid plastids This would constitute a relatively rapid loss of photosystem proteins when compared to gene loss patterns in other plastid lineages. Protein complexes were further separated in a second dimension by SDS-PAGE and individual putative subunits (co-migrating with PSI/PSII bands) were analysed by mass spectrometry (MS) As noted above, both PSI and PSII subunits can be found in a large structure at the top of the native gel with α-DM (Fig. 3), which suggests that in Chromera photosystems are tightly associated. More biochemical and physiological work is needed to elaborate this hypothesis, these results, together with previous reports[31,92] contribute to our growing understanding of the metabolic changes undergone in the ancestors of apicomplexans as they made the transition from alga to parasite

Materials and Methods

Author Contributions

Additional Information