Exploring the low photosynthetic efficiency of cyanobacteria in blue light using a mutant lacking phycobilisomes

Veerle M. Luimstra,Jef Huisman,Klaas J. Hellingwerf,Carolina F. M. de Carvalho,J. Merijn Schuurmans,Hans C. P. Matthijs

doi:10.1007/s11120-019-00630-z

Abstract

The ubiquitous chlorophyll a (Chl a) pigment absorbs both blue and red light. Yet, in contrast to green algae and higher plants, most cyanobacteria have much lower photosynthetic rates in blue than in red light. A plausible but not yet well-supported hypothesis is that blue light results in limited energy transfer to photosystem II (PSII), because cyanobacteria invest most Chl a in photosystem I (PSI), whereas their phycobilisomes (PBS) are mostly associated with PSII but do not absorb blue photons. In this paper, we compare the photosynthetic performance in blue and orange-red light of wildtype Synechocystis sp. PCC 6803 and a PBS-deficient mutant. Our results show that the wildtype had much lower biomass, Chl a content, PSI:PSII ratio and O2 production rate per PSII in blue light than in orange-red light, whereas the PBS-deficient mutant had a low biomass, Chl a content, PSI:PSII ratio, and O2 production rate per PSII in both light colors. More specifically, the wildtype displayed a similar low photosynthetic efficiency in blue light as the PBS-deficient mutant in both light colors. Our results demonstrate that the absorption of light energy by PBS and subsequent transfer to PSII are crucial for efficient photosynthesis in cyanobacteria, which may explain both the low photosynthetic efficiency of PBS-containing cyanobacteria and the evolutionary success of chlorophyll-based light-harvesting antennae in environments dominated by blue light.

Highlights

Cyanobacteria are the oldest known oxygen-producing photosynthetic organisms on our planet and their photosynthetic activity is widely held responsible for oxygenation of the Earth’s atmosphere about 2.3 billion years ago (Holland 2002; Schirrmeister et al 2015)
It is often hypothesized that the distribution of absorbed light energy between photosystem I (PSI) and photosystem II (PSII) plays a key role (Fujita 1997; El Bissati and Kirilovsky 2001; Wang et al 2007; Singh et al 2009; Solhaug et al 2014; Kirilovsky 2015; Luimstra et al 2018)
Most of the PBS are typically associated with PSII, but PBS can be relocated to PSI at time scales of seconds to minutes, or

Summary

Introduction

Cyanobacteria are the oldest known oxygen-producing photosynthetic organisms on our planet and their photosynthetic activity is widely held responsible for oxygenation of the Earth’s atmosphere about 2.3 billion years ago (Holland 2002; Schirrmeister et al 2015). Why cyanobacteria perform less well in blue light is not yet fully resolved. It is often hypothesized that the distribution of absorbed light energy between photosystem I (PSI) and photosystem II (PSII) plays a key role (Fujita 1997; El Bissati and Kirilovsky 2001; Wang et al 2007; Singh et al 2009; Solhaug et al 2014; Kirilovsky 2015; Luimstra et al 2018). To optimize absorption of light energy, cyanobacteria use phycobilisomes (PBS) as light-harvesting antennae, which transfer absorbed light energy to the photosystems (Grossman et al 1993; Tandeau de Marsac 2003). Most of the PBS are typically associated with PSII (state 1), but PBS can be relocated to PSI (state 2) at time scales of seconds to minutes, or

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