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

Tong Li,Maryam Ataeian,Marc Strous,Dirk De Beer,Christine E Sharp

doi:10.3389/fmicb.2018.02490

Abstract

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 (CO2) from the biofilms increased two- to four-fold. This could be explained by the conversion of CO2, leaking from cyanobacterial cells, by eCA, to bicarbonate. Bicarbonate is then taken up again by the cyanobacteria. In suspensions, eCA reduced the CO2 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 CO2 loss to the medium is reduced due to mass transfer resistance.

Highlights

Alkaline Soda lakes are extremely productive due to the high dissolved organic carbon (DIC) availability, and can be found in various geographical locations around the globe (Melack, 1981; Priscu et al, 1982; Kompantseva et al, 2009)
The pH increased from 8.7 at the surface to 10 in biofilms cultivated with low DIC (∼13 mM) when extracellular carbonic anhydrase (eCA) inhibitor was not present
Biofilms cultivated at higher DIC concentrations suffered less productivity loss after eCA inhibition

Summary

Introduction

Alkaline Soda lakes are extremely productive due to the high DIC availability, and can be found in various geographical locations around the globe (Melack, 1981; Priscu et al, 1982; Kompantseva et al, 2009). Soda lakes are believed to have existed throughout the geological record of Earth, and are abundant in dry terrestrial biomes. These lakes support the growth of an large array of microorganisms that are of ecological and economic importance (Antony et al, 2013). Microalgae that thrive in the high pH and salinity can highly efficiently photosynthesize due to the elevated dissolved organic carbon (DIC) levels. This makes biofilms from alkaline environments potentially eCA in Alkaliphilic Phototrophic Biofilm useful for carbon capture. A mechanistic understanding of the DIC uptake in the biomass is desired and the aim of this study

Objectives

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Discussion

Conclusion