Genome and proteome of the chlorophyll f-producing cyanobacterium Halomicronema hongdechloris: adaptative proteomic shifts under different light conditions

Abstract

BackgroundHalomicronema hongdechloris was the first cyanobacterium to be identified that produces chlorophyll (Chl) f. It contains Chl a and uses phycobiliproteins as its major light-harvesting components under white light conditions. However, under far-red light conditions H. hongdechloris produces Chl f and red-shifted phycobiliprotein complexes to absorb and use far-red light. In this study, we report the genomic sequence of H. hongdechloris and use quantitative proteomic approaches to confirm the deduced metabolic pathways as well as metabolic and photosynthetic changes in response to different photo-autotrophic conditions.ResultsThe whole genome of H. hongdechloris was sequenced using three different technologies and assembled into a single circular scaffold with a genome size of 5,577,845 bp. The assembled genome has 54.6% GC content and encodes 5273 proteins covering 83.5% of the DNA sequence. Using Tandem Mass Tag labelling, the total proteome of H. hongdechloris grown under different light conditions was analyzed. A total of 1816 proteins were identified, with photosynthetic proteins accounting for 24% of the total mass spectral readings, of which 35% are phycobiliproteins. The proteomic data showed that essential cellular metabolic reactions remain unchanged under shifted light conditions. The largest differences in protein content between white and far-red light conditions reflect the changes to photosynthetic complexes, shifting from a standard phycobilisome and Chl a-based light harvesting system under white light, to modified, red-shifted phycobilisomes and Chl f-containing photosystems under far-red light conditions.ConclusionWe demonstrate that essential cellular metabolic reactions under different light conditions remain constant, including most of the enzymes in chlorophyll biosynthesis and photosynthetic carbon fixation. The changed light conditions cause significant changes in the make-up of photosynthetic protein complexes to improve photosynthetic light capture and reaction efficiencies. The integration of the global proteome with the genome sequence highlights that cyanobacterial adaptation strategies are focused on optimizing light capture and utilization, with minimal changes in other metabolic pathways. Our quantitative proteomic approach has enabled a deeper understanding of both the stability and the flexibility of cellular metabolic networks of H. hongdechloris in response to changes in its environment.Electronic supplementary materialThe online version of this article (10.1186/s12864-019-5587-3) contains supplementary material, which is available to authorized users.

Structural basis for the adaptation and function of chlorophyll f in photosystem I

“…4a, b), and the overall structures are similar to that of the cyanobacterial PSI trimer (containing only Chl a) reported previously 6,11 , except for PsaF, PsaJ, and PsaX (and PsaK in the case of white PSI). Although the gene for PsaX was not found in the genome of H. hongdechloris, the genes for PsaF, PsaJ, and PsaK are present 29 . In the atomic model of the white PSI, each monomer contains five membrane-spanning subunits (PsaA, PsaB, PsaI, PsaL, and PsaM) and three stromal subunits (PsaC, PsaD, and PsaE) ( Fig.…”

“…1d), this result indicates an even weaker association of them with the PSI core. One of the reasons for this loose association of PsaF and PsaJ may be owing to the replacement of psaA, psaB, as well as psaF, psaI, psaL, and psaJ genes under the far-red light condition (see below) 3,29 . PsaF was previously suggested to be involved in binding of the electron donor, such as the c-type cytochrome 30 .…”

“…The root mean square deviation (RMSD) between the white and far-red PSI is 0.62 Å for 1855 C α atoms from subunits whose structures were built in both PSI cores, suggesting a large similarity in the overall structures of the two PSI cores. However, it is known that far-red light induces an extensive remodeling of the photosynthetic apparatus of H. hongdechloris by changing the expression of genes encoding the PSI core subunits as well as the synthesis of pigments (including change of Chl a to Chl f) of PSI [22][23][24][25]29 . Indeed, the sequences of some subunits in the structure of the far-red PSI were found to be different from that of the white PSI.…”

“…In our structure, PsaA_2, PsaB_2, PsaI_3, and PsaL_2 subunits in the white PSI were changed to PsaA_1, PsaB_1, PsaI_2, and PsaL_1 subunits in the far-red PSI, respectively. These four subunits are encoded by different genes with different amino-acid sequences between the white and farred PSI, whereas the other subunits are encoded by the same genes 29 . The sequence identities for the four subunits, PsaA, PsaB, PsaI, and PsaL between the white and far-red PSI are 74.6%, 80.9%, 36.8%, and 43.4%, respectively, in this cyanobacterium.…”

“…Some cyanobacteria have been found to undergo extensive remodeling regarding the expression of some photosynthetic genes upon transfer from white light to far-red light, which is accompanied by the synthesis of Chl f and its incorporation and functioning in the photosystems [3][4][5][21][22][23][24]29,31 . The present structural analyses indeed revealed the changes of the sequences and structures of four subunits, PsaA, PsaB, PsaI, and PsaL, between white PSI and far-red PSI.…”