Cyanobacteria in sulfidic spring microbial mats can perform oxygenic and anoxygenic photosynthesis simultaneously during an entire diurnal period

We used microsensors to study the regulation of oxygenic and anoxygenic photosynthesis 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...

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Main Authors: Judith M Klatt, Dirk De Beer, Stefan Häusler, Lubos Polerecky
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01973/full
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author Judith M Klatt
Judith M Klatt
Dirk De Beer
Stefan Häusler
Lubos Polerecky
Lubos Polerecky
author_facet Judith M Klatt
Judith M Klatt
Dirk De Beer
Stefan Häusler
Lubos Polerecky
Lubos Polerecky
author_sort Judith M Klatt
collection DOAJ
description We used microsensors to study the regulation of oxygenic and anoxygenic photosynthesis 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. Anoxygenic photosynthesis 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 anoxygenic photosynthesis and from photosystem II (PSII) in oxygenic photosynthesis. 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 towards PQ. The SQR enzyme and PSII have similar affinities towards PQ, which explains the concurrent oxygenic and anoxygenic photosynthesis 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.
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spelling doaj.art-ac133e9c15a84e2890fdb8b93821ee7a2022-12-21T17:32:12ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2016-12-01710.3389/fmicb.2016.01973228285Cyanobacteria in sulfidic spring microbial mats can perform oxygenic and anoxygenic photosynthesis simultaneously during an entire diurnal periodJudith M Klatt0Judith M Klatt1Dirk De Beer2Stefan Häusler3Lubos Polerecky4Lubos Polerecky5University of MichiganMax-Planck-Institute for Marine MicrobiologyMax-Planck-Institute for Marine MicrobiologyMax-Planck-Institute for Marine MicrobiologyMax-Planck-Institute for Marine MicrobiologyUtrecht UniversityWe used microsensors to study the regulation of oxygenic and anoxygenic photosynthesis 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. Anoxygenic photosynthesis 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 anoxygenic photosynthesis and from photosystem II (PSII) in oxygenic photosynthesis. 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 towards PQ. The SQR enzyme and PSII have similar affinities towards PQ, which explains the concurrent oxygenic and anoxygenic photosynthesis 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.http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01973/fullCyanobacteriamicrobial matmicrosensorshydrogen sulfide (H2S)anoxygenic photosynthesissulfide:quinone:reductase
spellingShingle Judith M Klatt
Judith M Klatt
Dirk De Beer
Stefan Häusler
Lubos Polerecky
Lubos Polerecky
Cyanobacteria in sulfidic spring microbial mats can perform oxygenic and anoxygenic photosynthesis simultaneously during an entire diurnal period
Frontiers in Microbiology
Cyanobacteria
microbial mat
microsensors
hydrogen sulfide (H2S)
anoxygenic photosynthesis
sulfide:quinone:reductase
title Cyanobacteria in sulfidic spring microbial mats can perform oxygenic and anoxygenic photosynthesis simultaneously during an entire diurnal period
title_full Cyanobacteria in sulfidic spring microbial mats can perform oxygenic and anoxygenic photosynthesis simultaneously during an entire diurnal period
title_fullStr Cyanobacteria in sulfidic spring microbial mats can perform oxygenic and anoxygenic photosynthesis simultaneously during an entire diurnal period
title_full_unstemmed Cyanobacteria in sulfidic spring microbial mats can perform oxygenic and anoxygenic photosynthesis simultaneously during an entire diurnal period
title_short Cyanobacteria in sulfidic spring microbial mats can perform oxygenic and anoxygenic photosynthesis simultaneously during an entire diurnal period
title_sort cyanobacteria in sulfidic spring microbial mats can perform oxygenic and anoxygenic photosynthesis simultaneously during an entire diurnal period
topic Cyanobacteria
microbial mat
microsensors
hydrogen sulfide (H2S)
anoxygenic photosynthesis
sulfide:quinone:reductase
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01973/full
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