Cyanobacteria in Sulfidic Spring Microbial Mats Can Perform Oxygenic and Anoxygenic Photosynthesis Simultaneously during an Entire Diurnal Period.

Stefan Häusler,Dirk De Beer,Judith M Klatt,Lubos Polerecky

doi:10.3389/fmicb.2016.01973

Abstract

We used microsensors to study the regulation of anoxygenic and oxygenic photosynthesis (AP and OP, respectively) by light and sulfide in a cyanobacterium dominating microbial mats from cold sulfidic springs. Both photosynthetic modes were performed simultaneously over all H2S concentrations (1–2200 μM) and irradiances (4–52 μmol photons m-2 s-1) tested. AP increased with H2S concentration while the sum of oxygenic and anoxygenic photosynthetic rates was constant at each light intensity. Thus, the total photosynthetically driven electron transport rate was solely controlled by the irradiance level. The partitioning between the rates of these two photosynthetic modes was regulated by both light and H2S concentration. The plastoquinone pool (PQ) receives electrons from sulfide:quinone:reductase (SQR) in AP and from photosystem II (PSII) in OP. It is thus the link in the electron transport chain where both pathways intersect, and the compound that controls their partitioning. We fitted our data with a model of the photosynthetic electron transport that includes the kinetics of plastoquinone reduction and oxidation. The model results confirmed that the observed partitioning between photosynthetic modes can be explained by a simple kinetic control based on the affinity of SQR and PSII toward PQ. The SQR enzyme and PSII have similar affinities toward PQ, which explains the concurrent OP and AP over an astonishingly wide range of H2S concentrations and irradiances. The elegant kinetic control of activity makes the cyanobacterium successful in the fluctuating spring environment. We discuss how these specific regulation mechanisms may have played a role in ancient H2S-rich oceans.

Highlights

Oxygenic photosynthesis (OP) is a process where light energy is used to extract electrons from water to reduce CO2
We sampled a mat that was characterized by a green cyanobacterial layer on top of a distinct, very thin layer of large sulfur oxidizing bacteria (SOB)
The examined subsample of the cyanobacterial layer was dominated by a single filamentous cyanobacterium with a diameter of ∼4 μm (Figure 3)

Summary

Introduction

Oxygenic photosynthesis (OP) is a process where light energy is used to extract electrons from water to reduce CO2. It has been hypothesized that AP performed by obligate anoxygenic phototrophs and cyanobacteria capable of both AP and OP (referred to as versatile cyanobacteria) was an important photosynthetic mode on a global scale before the complete oxygenation of the Earth’s atmosphere and oceans during the Neoproterozoic oxidation event (Johnston et al, 2009) It is intriguing how oxygenic phototrophs were so successful in oxygenating Earth despite the widespread availability of electron donors for anoxygenic phototrophs and the toxic effects of H2S on the components of OP, especially considering that AP is a biochemically less complicated and energetically less demanding process than OP (Miller and Bebout, 2004; Klatt et al, 2015a)

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