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Oxygenic photosynthesis as a protection mechanism for cyanobacteria against iron-encrustation in environments with high Fe(2+) concentrations.

Ionescu D, Buchmann B, Heim C, Häusler S, de Beer D, Polerecky L - Front Microbiol (2014)

Bottom Line: Hitherto, no mechanism has been proposed for cyanobacteria from Fe(2+)-rich environments; these produce O2 but are seldom found encrusted in iron.Modeling based on in-situ O2 and pH profiles showed that cyanobacteria from the Fe(2+)-rich reactor were not exposed to significant Fe(2+) concentrations.This mechanism sheds new light on the possible role of cyanobacteria in precipitation of banded iron formations.

View Article: PubMed Central - PubMed

Affiliation: Microsensor Group, Max-Planck Institute for Marine Microbiology Bremen, Germany ; Department of Stratified Lakes, Leibniz Institute for Freshwater Ecology and Inland Fisheries Stechlin, Germany.

ABSTRACT
If O2 is available at circumneutral pH, Fe(2+) is rapidly oxidized to Fe(3+), which precipitates as FeO(OH). Neutrophilic iron oxidizing bacteria have evolved mechanisms to prevent self-encrustation in iron. Hitherto, no mechanism has been proposed for cyanobacteria from Fe(2+)-rich environments; these produce O2 but are seldom found encrusted in iron. We used two sets of illuminated reactors connected to two groundwater aquifers with different Fe(2+) concentrations (0.9 μM vs. 26 μM) in the Äspö Hard Rock Laboratory (HRL), Sweden. Cyanobacterial biofilms developed in all reactors and were phylogenetically different between the reactors. Unexpectedly, cyanobacteria growing in the Fe(2+)-poor reactors were encrusted in iron, whereas those in the Fe(2+)-rich reactors were not. In-situ microsensor measurements showed that O2 concentrations and pH near the surface of the cyanobacterial biofilms from the Fe(2+)-rich reactors were much higher than in the overlying water. This was not the case for the biofilms growing at low Fe(2+) concentrations. Measurements with enrichment cultures showed that cyanobacteria from the Fe(2+)-rich environment increased their photosynthesis with increasing Fe(2+) concentrations, whereas those from the low Fe(2+) environment were inhibited at Fe(2+) > 5 μM. Modeling based on in-situ O2 and pH profiles showed that cyanobacteria from the Fe(2+)-rich reactor were not exposed to significant Fe(2+) concentrations. We propose that, due to limited mass transfer, high photosynthetic activity in Fe(2+)-rich environments forms a protective zone where Fe(2+) precipitates abiotically at a non-lethal distance from the cyanobacteria. This mechanism sheds new light on the possible role of cyanobacteria in precipitation of banded iron formations.

No MeSH data available.


Percent change in O2 fluxes and pH gradients calculated from microprofiles measured in cyanobacterial biofilms grown from enrichment cultures from the Fe2+-rich and Fe2+-poor reactors at pH 7 (A) and pH 8 (C). The shown fluxes are averaged measurements in 3 different biofilms with 3–4 steady state profiles each. Example of profiles from which these fluxes were calculated are shown in (B,D), respectively. Depth zero corresponds to the biofilm surface.
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Figure 3: Percent change in O2 fluxes and pH gradients calculated from microprofiles measured in cyanobacterial biofilms grown from enrichment cultures from the Fe2+-rich and Fe2+-poor reactors at pH 7 (A) and pH 8 (C). The shown fluxes are averaged measurements in 3 different biofilms with 3–4 steady state profiles each. Example of profiles from which these fluxes were calculated are shown in (B,D), respectively. Depth zero corresponds to the biofilm surface.

Mentions: In addition to in-situ measurements, we conducted laboratory microsensor measurements to characterize the response of photosynthesis to increased Fe2+ concentrations in biofilms prepared from the cyanobacterial enrichment cultures obtained from the two reactor types. When the bulk pH was 7.1, the addition of up to 50 μM Fe2+ stimulated net O2 production in the enrichment cultures from the non-aerated Fe2+-rich reactor (Figure 3A — open triangles; Spearman correlation coefficient ρ = 0.952, p = 2 × 10−7), suggesting stimulation of photosynthetic activity by Fe2+. This was consistent with the observed increase in pH gradients at the biofilm-medium interface (Figure 3A, filled triangles; ρ = 0.854, p = 2 × 10−7). In contrast, increasing Fe2+ lead to a decrease in both O2 fluxes and pH gradients in biofilms prepared from the enrichment cultures from the aerated Fe2+-rich (O2: ρ = −0.686, p = 7.45 × 10−4; pH: ρ = −0.741, p = 0.011) and Fe2+-poor reactor (O2: ρ = −0.865, p = 2 × 10−7; pH: ρ = −0.986, p = 2 × 10−7), with the largest part of this decrease occurring for Fe2+ concentrations between 1 and 10 μM (Figures 3A,B). Analysis of covariance (ANCOVA) revealed that the slope of the regression line for the culture enriched from the non-aerated Fe2+-rich reactor was significantly greater than that for the enrichment cultures from the aerated Fe2+-rich and aerated Fe2+-poor reactors (p = 2 × 10−9), whereas the latter two were not significantly different (p = 0.97).


Oxygenic photosynthesis as a protection mechanism for cyanobacteria against iron-encrustation in environments with high Fe(2+) concentrations.

Ionescu D, Buchmann B, Heim C, Häusler S, de Beer D, Polerecky L - Front Microbiol (2014)

Percent change in O2 fluxes and pH gradients calculated from microprofiles measured in cyanobacterial biofilms grown from enrichment cultures from the Fe2+-rich and Fe2+-poor reactors at pH 7 (A) and pH 8 (C). The shown fluxes are averaged measurements in 3 different biofilms with 3–4 steady state profiles each. Example of profiles from which these fluxes were calculated are shown in (B,D), respectively. Depth zero corresponds to the biofilm surface.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4151041&req=5

Figure 3: Percent change in O2 fluxes and pH gradients calculated from microprofiles measured in cyanobacterial biofilms grown from enrichment cultures from the Fe2+-rich and Fe2+-poor reactors at pH 7 (A) and pH 8 (C). The shown fluxes are averaged measurements in 3 different biofilms with 3–4 steady state profiles each. Example of profiles from which these fluxes were calculated are shown in (B,D), respectively. Depth zero corresponds to the biofilm surface.
Mentions: In addition to in-situ measurements, we conducted laboratory microsensor measurements to characterize the response of photosynthesis to increased Fe2+ concentrations in biofilms prepared from the cyanobacterial enrichment cultures obtained from the two reactor types. When the bulk pH was 7.1, the addition of up to 50 μM Fe2+ stimulated net O2 production in the enrichment cultures from the non-aerated Fe2+-rich reactor (Figure 3A — open triangles; Spearman correlation coefficient ρ = 0.952, p = 2 × 10−7), suggesting stimulation of photosynthetic activity by Fe2+. This was consistent with the observed increase in pH gradients at the biofilm-medium interface (Figure 3A, filled triangles; ρ = 0.854, p = 2 × 10−7). In contrast, increasing Fe2+ lead to a decrease in both O2 fluxes and pH gradients in biofilms prepared from the enrichment cultures from the aerated Fe2+-rich (O2: ρ = −0.686, p = 7.45 × 10−4; pH: ρ = −0.741, p = 0.011) and Fe2+-poor reactor (O2: ρ = −0.865, p = 2 × 10−7; pH: ρ = −0.986, p = 2 × 10−7), with the largest part of this decrease occurring for Fe2+ concentrations between 1 and 10 μM (Figures 3A,B). Analysis of covariance (ANCOVA) revealed that the slope of the regression line for the culture enriched from the non-aerated Fe2+-rich reactor was significantly greater than that for the enrichment cultures from the aerated Fe2+-rich and aerated Fe2+-poor reactors (p = 2 × 10−9), whereas the latter two were not significantly different (p = 0.97).

Bottom Line: Hitherto, no mechanism has been proposed for cyanobacteria from Fe(2+)-rich environments; these produce O2 but are seldom found encrusted in iron.Modeling based on in-situ O2 and pH profiles showed that cyanobacteria from the Fe(2+)-rich reactor were not exposed to significant Fe(2+) concentrations.This mechanism sheds new light on the possible role of cyanobacteria in precipitation of banded iron formations.

View Article: PubMed Central - PubMed

Affiliation: Microsensor Group, Max-Planck Institute for Marine Microbiology Bremen, Germany ; Department of Stratified Lakes, Leibniz Institute for Freshwater Ecology and Inland Fisheries Stechlin, Germany.

ABSTRACT
If O2 is available at circumneutral pH, Fe(2+) is rapidly oxidized to Fe(3+), which precipitates as FeO(OH). Neutrophilic iron oxidizing bacteria have evolved mechanisms to prevent self-encrustation in iron. Hitherto, no mechanism has been proposed for cyanobacteria from Fe(2+)-rich environments; these produce O2 but are seldom found encrusted in iron. We used two sets of illuminated reactors connected to two groundwater aquifers with different Fe(2+) concentrations (0.9 μM vs. 26 μM) in the Äspö Hard Rock Laboratory (HRL), Sweden. Cyanobacterial biofilms developed in all reactors and were phylogenetically different between the reactors. Unexpectedly, cyanobacteria growing in the Fe(2+)-poor reactors were encrusted in iron, whereas those in the Fe(2+)-rich reactors were not. In-situ microsensor measurements showed that O2 concentrations and pH near the surface of the cyanobacterial biofilms from the Fe(2+)-rich reactors were much higher than in the overlying water. This was not the case for the biofilms growing at low Fe(2+) concentrations. Measurements with enrichment cultures showed that cyanobacteria from the Fe(2+)-rich environment increased their photosynthesis with increasing Fe(2+) concentrations, whereas those from the low Fe(2+) environment were inhibited at Fe(2+) > 5 μM. Modeling based on in-situ O2 and pH profiles showed that cyanobacteria from the Fe(2+)-rich reactor were not exposed to significant Fe(2+) concentrations. We propose that, due to limited mass transfer, high photosynthetic activity in Fe(2+)-rich environments forms a protective zone where Fe(2+) precipitates abiotically at a non-lethal distance from the cyanobacteria. This mechanism sheds new light on the possible role of cyanobacteria in precipitation of banded iron formations.

No MeSH data available.