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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.


Light (A) and autofluorescence (B) microscopic images of iron-encrusted cyanobacterial filaments from the aerated Fe2+-poor reactor. Upon treatment with 0.3 M oxalic acid most of the Fe crystals dissolved (C) and the natural red autofluorescence induced by green light resumed (D). Filaments from the aerated (E) and non-aerated (F) Fe2+-rich reactors were not found encrusted.
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Figure 1: Light (A) and autofluorescence (B) microscopic images of iron-encrusted cyanobacterial filaments from the aerated Fe2+-poor reactor. Upon treatment with 0.3 M oxalic acid most of the Fe crystals dissolved (C) and the natural red autofluorescence induced by green light resumed (D). Filaments from the aerated (E) and non-aerated (F) Fe2+-rich reactors were not found encrusted.

Mentions: Filamentous cyanobacteria in the aerated reactors connected to the Fe2+-poor aquifer formed veil-like biofilms (2–3 cm long, 2–3 mm thick) that slowly but continuously moved due to the slow water flow in the reactor. Their pale-green color coincided with a low chlorophyll a (Chl a) concentration (0.2 μg Chl a mg−1 wet weight) and thus presumably low cyanobacterial biomass. Microscopic observations of biofilm subsamples revealed clear iron encrustation and largely diminished auto-fluorescence of the filaments (Figures 1A,B). Upon addition of 0.3 M oxalic acid, most of the Fe-oxide crystals dissolved and the red auto-fluorescence induced by green light, which is typical for cyanobacteria due to their Chl a and phycocyanin content, significantly increased (Figures 1C,D). Due to an extremely low biomass, biofilms from the non-aerated reactor from the Fe2+-poor site were not studied.


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)

Light (A) and autofluorescence (B) microscopic images of iron-encrusted cyanobacterial filaments from the aerated Fe2+-poor reactor. Upon treatment with 0.3 M oxalic acid most of the Fe crystals dissolved (C) and the natural red autofluorescence induced by green light resumed (D). Filaments from the aerated (E) and non-aerated (F) Fe2+-rich reactors were not found encrusted.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Light (A) and autofluorescence (B) microscopic images of iron-encrusted cyanobacterial filaments from the aerated Fe2+-poor reactor. Upon treatment with 0.3 M oxalic acid most of the Fe crystals dissolved (C) and the natural red autofluorescence induced by green light resumed (D). Filaments from the aerated (E) and non-aerated (F) Fe2+-rich reactors were not found encrusted.
Mentions: Filamentous cyanobacteria in the aerated reactors connected to the Fe2+-poor aquifer formed veil-like biofilms (2–3 cm long, 2–3 mm thick) that slowly but continuously moved due to the slow water flow in the reactor. Their pale-green color coincided with a low chlorophyll a (Chl a) concentration (0.2 μg Chl a mg−1 wet weight) and thus presumably low cyanobacterial biomass. Microscopic observations of biofilm subsamples revealed clear iron encrustation and largely diminished auto-fluorescence of the filaments (Figures 1A,B). Upon addition of 0.3 M oxalic acid, most of the Fe-oxide crystals dissolved and the red auto-fluorescence induced by green light, which is typical for cyanobacteria due to their Chl a and phycocyanin content, significantly increased (Figures 1C,D). Due to an extremely low biomass, biofilms from the non-aerated reactor from the Fe2+-poor site were not studied.

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.