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.

Highlights

  • Halomicronema hongdechloris was the first cyanobacterium to be identified that produces chlorophyll (Chl) f

  • Chl d and Chl f can use light of wavelengths greater than 700 nm efficiently because of their red-shifted absorption properties, and as such they are called “red-shifted chlorophylls” [5,6,7,8]. These red-shifted Chls have been found in cyanobacteria that can thrive in extreme low light conditions, especially in light filtered by Chl a/b-containing organisms, where visible light is scarce and far-red (FR) light (> 700 nm), is more available [9,10,11,12,13,14]

  • Genome sequence assembly The H. hongdechloris DNA sequence reads were assembled de novo in a hybrid assembly using MIRA 4.9.2 [33] with further analysis using MUMmer [34] and manual contig joining in Gap5 [35] using PacBio long reads as described in the methods

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Summary

Introduction

Halomicronema 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. Chl d and Chl f can use light of wavelengths greater than 700 nm efficiently because of their red-shifted absorption properties, and as such they are called “red-shifted chlorophylls” [5,6,7,8] These red-shifted Chls have been found in cyanobacteria that can thrive in extreme low light conditions, especially in light filtered by Chl a/b-containing organisms, where visible light is scarce and far-red (FR) light (> 700 nm), is more available [9,10,11,12,13,14]

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