The induction of pyrenoid synthesis by hyperoxia and its implications for the natural diversity of photosynthetic responses in Chlamydomonas.

Peter Neofotis,Ben Lucker,Joseph Weissman,Alecia Withrow,Nicole Norris,Eric Pollner,Barbara Sears,Melinda Frame,Oliver L Tessmer,Greg Mogos,David Hall,Joshua Temple,David M Kramer,Jacob Bibik,Sarathi M Weraduwage

doi:10.7554/elife.67565

Abstract

In algae, it is well established that the pyrenoid, a component of the carbon-concentrating mechanism (CCM), is essential for efficient photosynthesis at low CO2. However, the signal that triggers the formation of the pyrenoid has remained elusive. Here, we show that, in Chlamydomonas reinhardtii, the pyrenoid is strongly induced by hyperoxia, even at high CO2 or bicarbonate levels. These results suggest that the pyrenoid can be induced by a common product of photosynthesis specific to low CO2 or hyperoxia. Consistent with this view, the photorespiratory by-product, H2O2, induced the pyrenoid, suggesting that it acts as a signal. Finally, we show evidence for linkages between genetic variations in hyperoxia tolerance, H2O2 signaling, and pyrenoid morphologies.

Highlights

The maximal primary productivity of algae is often determined by the efficiency of photosynthesis, which is strongly impacted by environmental factors
This varying tolerance was observed when cultures were continuously sparged in batch culture (Appendix 1—figure 2), when the cultures were CO2 saturated, indicating that the differential sensitivity was caused by hyperoxia rather than depletion of inorganic carbon sources
1981 were screening for mutants that were highly sensitive to even low light (~90 μmoles m–2 s–1 photosynthetically active radiation (PAR)), we grew our wild-type strains of Chlamydomonas under hyperoxia with diurnal sinusoidal light with peak light intensities of 2000 μmoles m–2 s–1 PAR

Summary

Introduction

The maximal primary productivity of algae is often determined by the efficiency of photosynthesis, which is strongly impacted by environmental factors. The products of photosynthesis can impact local environmental conditions, leading to feedback- (or self-) limitations (Livansky, 1996; Pulz, 2001; Raso et al, 2012; Torzillo et al, 1998; Vonshak et al, 1996; Weissman et al, 1988). Hyperoxia has been directly associated with loss of productivity in a wide range of algal and cyanobacterial species, including Nannochroposis (Raso et al, 2012), Chlamydomonas reinhardtii (Kliphuis et al, 2011), Neochloris oleabundans (Peng et al, 2016a; Sousa et al, 2012), Chlorella sorokiniana (Ugwu et al, 2007), and Spirulina (Vonshak et al, 1996)

Methods

Results

Discussion

Conclusion