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Role of Extracellular Carbonic Anhydrase in Dissolved Inorganic Carbon Uptake in Alkaliphilic Phototrophic Biofilm

Alkaline Soda Lakes are extremely productive ecosystems, due to their high dissolved inorganic carbon (DIC) concentrations. Here, we studied the dynamics of the carbonate system, in particular, the role of extracellular carbonic anhydrase (eCA) of an alkaliphilic phototrophic biofilm composed of bac...

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Autores principales: Li, Tong, Sharp, Christine E., Ataeian, Maryam, Strous, Marc, de Beer, Dirk
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6204761/
https://www.ncbi.nlm.nih.gov/pubmed/30405559
http://dx.doi.org/10.3389/fmicb.2018.02490
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author Li, Tong
Sharp, Christine E.
Ataeian, Maryam
Strous, Marc
de Beer, Dirk
author_facet Li, Tong
Sharp, Christine E.
Ataeian, Maryam
Strous, Marc
de Beer, Dirk
author_sort Li, Tong
collection PubMed
description Alkaline Soda Lakes are extremely productive ecosystems, due to their high dissolved inorganic carbon (DIC) concentrations. Here, we studied the dynamics of the carbonate system, in particular, the role of extracellular carbonic anhydrase (eCA) of an alkaliphilic phototrophic biofilm composed of bacteria enriched from soda lake benthic mats. By using measurements with microsensors and membrane inlet mass spectrometry, combined with mathematical modeling, we show how eCA controls DIC uptake. In our experiments, the activity of eCA varied four-fold, and was controlled by the bicarbonate concentration during growth: a higher bicarbonate concentration led to lower eCA activity. Inhibition of eCA decreased both the net and the gross photosynthetic productivities of the investigated biofilms. After eCA inhibition, the efflux of carbon dioxide (CO(2)) from the biofilms increased two- to four-fold. This could be explained by the conversion of CO(2), leaking from cyanobacterial cells, by eCA, to bicarbonate. Bicarbonate is then taken up again by the cyanobacteria. In suspensions, eCA reduced the CO(2) leakage to the bulk medium from 90 to 50%. In biofilms cultivated at low bicarbonate concentration (~0.13 mM), the oxygen production was reduced by a similar ratio upon eCA inhibition. The role of eCA in intact biofilms was much less significant compared to biomass suspensions, as CO(2) loss to the medium is reduced due to mass transfer resistance.
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spelling pubmed-62047612018-11-07 Role of Extracellular Carbonic Anhydrase in Dissolved Inorganic Carbon Uptake in Alkaliphilic Phototrophic Biofilm Li, Tong Sharp, Christine E. Ataeian, Maryam Strous, Marc de Beer, Dirk Front Microbiol Microbiology Alkaline Soda Lakes are extremely productive ecosystems, due to their high dissolved inorganic carbon (DIC) concentrations. Here, we studied the dynamics of the carbonate system, in particular, the role of extracellular carbonic anhydrase (eCA) of an alkaliphilic phototrophic biofilm composed of bacteria enriched from soda lake benthic mats. By using measurements with microsensors and membrane inlet mass spectrometry, combined with mathematical modeling, we show how eCA controls DIC uptake. In our experiments, the activity of eCA varied four-fold, and was controlled by the bicarbonate concentration during growth: a higher bicarbonate concentration led to lower eCA activity. Inhibition of eCA decreased both the net and the gross photosynthetic productivities of the investigated biofilms. After eCA inhibition, the efflux of carbon dioxide (CO(2)) from the biofilms increased two- to four-fold. This could be explained by the conversion of CO(2), leaking from cyanobacterial cells, by eCA, to bicarbonate. Bicarbonate is then taken up again by the cyanobacteria. In suspensions, eCA reduced the CO(2) leakage to the bulk medium from 90 to 50%. In biofilms cultivated at low bicarbonate concentration (~0.13 mM), the oxygen production was reduced by a similar ratio upon eCA inhibition. The role of eCA in intact biofilms was much less significant compared to biomass suspensions, as CO(2) loss to the medium is reduced due to mass transfer resistance. Frontiers Media S.A. 2018-10-22 /pmc/articles/PMC6204761/ /pubmed/30405559 http://dx.doi.org/10.3389/fmicb.2018.02490 Text en Copyright © 2018 Li, Sharp, Ataeian, Strous and de Beer. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Li, Tong
Sharp, Christine E.
Ataeian, Maryam
Strous, Marc
de Beer, Dirk
Role of Extracellular Carbonic Anhydrase in Dissolved Inorganic Carbon Uptake in Alkaliphilic Phototrophic Biofilm
title Role of Extracellular Carbonic Anhydrase in Dissolved Inorganic Carbon Uptake in Alkaliphilic Phototrophic Biofilm
title_full Role of Extracellular Carbonic Anhydrase in Dissolved Inorganic Carbon Uptake in Alkaliphilic Phototrophic Biofilm
title_fullStr Role of Extracellular Carbonic Anhydrase in Dissolved Inorganic Carbon Uptake in Alkaliphilic Phototrophic Biofilm
title_full_unstemmed Role of Extracellular Carbonic Anhydrase in Dissolved Inorganic Carbon Uptake in Alkaliphilic Phototrophic Biofilm
title_short Role of Extracellular Carbonic Anhydrase in Dissolved Inorganic Carbon Uptake in Alkaliphilic Phototrophic Biofilm
title_sort role of extracellular carbonic anhydrase in dissolved inorganic carbon uptake in alkaliphilic phototrophic biofilm
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6204761/
https://www.ncbi.nlm.nih.gov/pubmed/30405559
http://dx.doi.org/10.3389/fmicb.2018.02490
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