Global Transcriptional Profiling of the Cyanobacterium Chlorogloeopsis fritschii PCC 9212 in Far-Red Light: Insights Into the Regulation of Chlorophyll d Synthesis.

Ming-Yang Ho,Donald A Bryant

doi:10.3389/fmicb.2019.00465

Ming-Yang Ho, Donald A Bryant

Open Access

https://doi.org/10.3389/fmicb.2019.00465

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Abstract

Some terrestrial cyanobacteria can acclimate to and then utilize far-red light (FRL; λ = 700–800 nm) to perform oxygenic photosynthesis through a process called Far-Red Light Photoacclimation (FaRLiP). During FaRLiP, cells synthesize chlorophylls (Chl) d and Chl f and extensively remodel their photosynthetic apparatus by modifying core subunits of photosystem (PS)I, PSII, and the phycobilisome (PBS). Three regulatory proteins, RfpA, RfpB, and RfpC, are encoded in the FaRLiP gene cluster; they sense FRL and control the synthesis of Chl f and expression of the FaRLiP gene cluster. It was previously uncertain if Chl d synthesis and other physiological and metabolic changes to FRL are regulated by RfpABC. In this study we show that Chl d synthesis is regulated by RfpABC; however, most other transcriptional changes leading to the FRL physiological state are not regulated by RfpABC. Surprisingly, we show that erythromycin induces Chl d synthesis in vivo. Transcriptomic and pigment analyses indicate that thiol compounds and/or cysteine proteases could be involved in Chl d synthesis in FRL. We conclude that the protein(s) responsible for Chl d synthesis is/are probably encoded within the FaRLiP gene cluster. Transcriptional responses to FRL help cells to conserve and produce energy and reducing power to overcome implicit light limitation of photosynthesis during the initial acclimation process to FRL.

Highlights

Active radiation for oxygenic photosynthesis by cyanobacteria was long-believed to be limited to visible light (λ = 400 to 700 nm)
When cells were grown in far-red light (FRL) for 48 h in the presence of Em, no Chl f synthesis was detected in the rfpA, rfpB, and rfpC deletion mutants (Figures 1B–D); previous studies showed that such cells no longer accumulate the paralogous photosystem I (PSI), photosystem II (PSII), and PBS complexes typically observed in WT cells grown in FRL (Zhao et al, 2015; Ho et al, 2017a)
In this study we definitively establish that the RfpABC regulatory proteins control Chl d synthesis as well as specific cellular responses involving the FarRed Light Photoacclimation (FaRLiP) gene cluster (Figure 9)

Summary

Introduction

FaRLiP is especially important for terrestrial cyanobacteria because they frequently occur in niches where visible light is strongly filtered by Chl a or strongly scattered, leading to enrichment in wavelengths longer than 700 nm. These environments include shaded areas under plant canopies, soil crusts, microbial mats, dense algal blooms, caves, beach rocks and stromatolites (Chen et al, 2012; Behrendt et al, 2015; Gan and Bryant, 2015; Trampe and Kühl, 2016; Ohkubo and Miyashita, 2017)

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