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Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin.

Llirós M, García-Armisen T, Darchambeau F, Morana C, Triadó-Margarit X, Inceoğlu Ö, Borrego CM, Bouillon S, Servais P, Borges AV, Descy JP, Canfield DE, Crowe SA - Sci Rep (2015)

Bottom Line: These photoferrotrophs produce oxidized iron {Fe(III)} and biomass, and support a diverse pelagic microbial community including heterotrophic Fe(III)-reducers, sulfate reducers, fermenters and methanogens.At modest light levels, rates of photoferrotrophy in KB exceed those predicted for early Earth primary production, and are sufficient to generate Earth's largest sedimentary iron ore deposits.Fe cycling, however, is efficient, and complex microbial community interactions likely regulate Fe(III) and organic matter export from the photic zone.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Freshwater Ecology, Research Unit in Environmental and Evolutionary Biology, University of Namur, B-5000 Namur, Belgium.

ABSTRACT
Iron-rich (ferruginous) ocean chemistry prevailed throughout most of Earth's early history. Before the evolution and proliferation of oxygenic photosynthesis, biological production in the ferruginous oceans was likely driven by photoferrotrophic bacteria that oxidize ferrous iron {Fe(II)} to harness energy from sunlight, and fix inorganic carbon into biomass. Photoferrotrophs may thus have fuelled Earth's early biosphere providing energy to drive microbial growth and evolution over billions of years. Yet, photoferrotrophic activity has remained largely elusive on the modern Earth, leaving models for early biological production untested and imperative ecological context for the evolution of life missing. Here, we show that an active community of pelagic photoferrotrophs comprises up to 30% of the total microbial community in illuminated ferruginous waters of Kabuno Bay (KB), East Africa (DR Congo). These photoferrotrophs produce oxidized iron {Fe(III)} and biomass, and support a diverse pelagic microbial community including heterotrophic Fe(III)-reducers, sulfate reducers, fermenters and methanogens. At modest light levels, rates of photoferrotrophy in KB exceed those predicted for early Earth primary production, and are sufficient to generate Earth's largest sedimentary iron ore deposits. Fe cycling, however, is efficient, and complex microbial community interactions likely regulate Fe(III) and organic matter export from the photic zone.

No MeSH data available.


Microbial diversity in Kabuno Bay.(a) Pie charts showing relative sequence abundances of retrieved bacterial phyla, with detailed hierarchy for the Chlorobi phylum, detected in epilimnetic (left, E), and chemocline (right, C) waters of KB. (b) Relative abundances of Chlorobi sequences (dark green) retrieved by pyrosequencing (pyrotags) and cell abundances (light green) determined by flow cytometry (FC) from KB water samples. (c) 16S rRNA gene phylogenetic tree of the Chlorobiaceae including representative OTUs (0.03 cut-off) from those depths with maximum relative abundances of GSB from both the rainy (RS; asterisk) and dry (DS; omega) season water samples, as well as full 16S rRNA gene sequences from the KB isolate. The identifier code for each OTU and the metadata describing the depths and the layers (E for epilimnion, C for chemocline, and M for monimolimnion) where sequences were recovered are also indicated.
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f2: Microbial diversity in Kabuno Bay.(a) Pie charts showing relative sequence abundances of retrieved bacterial phyla, with detailed hierarchy for the Chlorobi phylum, detected in epilimnetic (left, E), and chemocline (right, C) waters of KB. (b) Relative abundances of Chlorobi sequences (dark green) retrieved by pyrosequencing (pyrotags) and cell abundances (light green) determined by flow cytometry (FC) from KB water samples. (c) 16S rRNA gene phylogenetic tree of the Chlorobiaceae including representative OTUs (0.03 cut-off) from those depths with maximum relative abundances of GSB from both the rainy (RS; asterisk) and dry (DS; omega) season water samples, as well as full 16S rRNA gene sequences from the KB isolate. The identifier code for each OTU and the metadata describing the depths and the layers (E for epilimnion, C for chemocline, and M for monimolimnion) where sequences were recovered are also indicated.

Mentions: The physical and chemical stratification of the water column is also reflected in microbial community composition. In the oxic sunlit waters (between surface and 10.0 m depth), cyanobacteria (ca. 10% of total cell counts by flow cytometry), algae, and heterotrophic bacteria typical of freshwater environments10 dominate (Fig. 1d,h; Fig. 2a; Supplementary Table S2). Light, however, penetrates well below these surface waters illuminating the Fe(II)-rich anoxic waters below (Fig. 1d,h). Here, we find a very different microbial community (Fig. 2a; Supplementary Fig. S2b,c,f,g). Anoxygenic photosynthetic green-sulfur bacteria (GSB) dominate in the chemocline where they comprise up to 30% of the total microbial community (Fig. 2b). Concentrations of Bacteriochlorophyll (BChl) e, a photosynthetic pigment utilized by brown-coloured, low light adapted GSB1112 reach up to ca. 235 μg l−1 (Fig. 1d,h) and clearly delineate the distribution of GSB in the chemocline waters. Depth-integrated BChl e concentrations (130 mg m−2) are 10-fold higher than Chlorophyll (Chl) a (13 mg m−2) concentrations in the upper waters. Analysis of the 16S small subunit rRNA gene reveals that the GSB present in KB are closely related to Chlorobium (Chl.) ferrooxidans strain KoFox (Fig. 2c and Supplementary Fig. S3 and S4). To date, str. KoFox is the sole member of the GSB known to conduct photoferrotrophy13 using Fe(II) as electron donor, and lacking the capacity to grow with reduced sulfur species13. Such physiology is consistent with the sub-μM concentrations (0–0.6 μM, maximum at 10.5 m; Fig. 1b,f) of reduced sulfur species observed in the illuminated waters of KB.


Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin.

Llirós M, García-Armisen T, Darchambeau F, Morana C, Triadó-Margarit X, Inceoğlu Ö, Borrego CM, Bouillon S, Servais P, Borges AV, Descy JP, Canfield DE, Crowe SA - Sci Rep (2015)

Microbial diversity in Kabuno Bay.(a) Pie charts showing relative sequence abundances of retrieved bacterial phyla, with detailed hierarchy for the Chlorobi phylum, detected in epilimnetic (left, E), and chemocline (right, C) waters of KB. (b) Relative abundances of Chlorobi sequences (dark green) retrieved by pyrosequencing (pyrotags) and cell abundances (light green) determined by flow cytometry (FC) from KB water samples. (c) 16S rRNA gene phylogenetic tree of the Chlorobiaceae including representative OTUs (0.03 cut-off) from those depths with maximum relative abundances of GSB from both the rainy (RS; asterisk) and dry (DS; omega) season water samples, as well as full 16S rRNA gene sequences from the KB isolate. The identifier code for each OTU and the metadata describing the depths and the layers (E for epilimnion, C for chemocline, and M for monimolimnion) where sequences were recovered are also indicated.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4562300&req=5

f2: Microbial diversity in Kabuno Bay.(a) Pie charts showing relative sequence abundances of retrieved bacterial phyla, with detailed hierarchy for the Chlorobi phylum, detected in epilimnetic (left, E), and chemocline (right, C) waters of KB. (b) Relative abundances of Chlorobi sequences (dark green) retrieved by pyrosequencing (pyrotags) and cell abundances (light green) determined by flow cytometry (FC) from KB water samples. (c) 16S rRNA gene phylogenetic tree of the Chlorobiaceae including representative OTUs (0.03 cut-off) from those depths with maximum relative abundances of GSB from both the rainy (RS; asterisk) and dry (DS; omega) season water samples, as well as full 16S rRNA gene sequences from the KB isolate. The identifier code for each OTU and the metadata describing the depths and the layers (E for epilimnion, C for chemocline, and M for monimolimnion) where sequences were recovered are also indicated.
Mentions: The physical and chemical stratification of the water column is also reflected in microbial community composition. In the oxic sunlit waters (between surface and 10.0 m depth), cyanobacteria (ca. 10% of total cell counts by flow cytometry), algae, and heterotrophic bacteria typical of freshwater environments10 dominate (Fig. 1d,h; Fig. 2a; Supplementary Table S2). Light, however, penetrates well below these surface waters illuminating the Fe(II)-rich anoxic waters below (Fig. 1d,h). Here, we find a very different microbial community (Fig. 2a; Supplementary Fig. S2b,c,f,g). Anoxygenic photosynthetic green-sulfur bacteria (GSB) dominate in the chemocline where they comprise up to 30% of the total microbial community (Fig. 2b). Concentrations of Bacteriochlorophyll (BChl) e, a photosynthetic pigment utilized by brown-coloured, low light adapted GSB1112 reach up to ca. 235 μg l−1 (Fig. 1d,h) and clearly delineate the distribution of GSB in the chemocline waters. Depth-integrated BChl e concentrations (130 mg m−2) are 10-fold higher than Chlorophyll (Chl) a (13 mg m−2) concentrations in the upper waters. Analysis of the 16S small subunit rRNA gene reveals that the GSB present in KB are closely related to Chlorobium (Chl.) ferrooxidans strain KoFox (Fig. 2c and Supplementary Fig. S3 and S4). To date, str. KoFox is the sole member of the GSB known to conduct photoferrotrophy13 using Fe(II) as electron donor, and lacking the capacity to grow with reduced sulfur species13. Such physiology is consistent with the sub-μM concentrations (0–0.6 μM, maximum at 10.5 m; Fig. 1b,f) of reduced sulfur species observed in the illuminated waters of KB.

Bottom Line: These photoferrotrophs produce oxidized iron {Fe(III)} and biomass, and support a diverse pelagic microbial community including heterotrophic Fe(III)-reducers, sulfate reducers, fermenters and methanogens.At modest light levels, rates of photoferrotrophy in KB exceed those predicted for early Earth primary production, and are sufficient to generate Earth's largest sedimentary iron ore deposits.Fe cycling, however, is efficient, and complex microbial community interactions likely regulate Fe(III) and organic matter export from the photic zone.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Freshwater Ecology, Research Unit in Environmental and Evolutionary Biology, University of Namur, B-5000 Namur, Belgium.

ABSTRACT
Iron-rich (ferruginous) ocean chemistry prevailed throughout most of Earth's early history. Before the evolution and proliferation of oxygenic photosynthesis, biological production in the ferruginous oceans was likely driven by photoferrotrophic bacteria that oxidize ferrous iron {Fe(II)} to harness energy from sunlight, and fix inorganic carbon into biomass. Photoferrotrophs may thus have fuelled Earth's early biosphere providing energy to drive microbial growth and evolution over billions of years. Yet, photoferrotrophic activity has remained largely elusive on the modern Earth, leaving models for early biological production untested and imperative ecological context for the evolution of life missing. Here, we show that an active community of pelagic photoferrotrophs comprises up to 30% of the total microbial community in illuminated ferruginous waters of Kabuno Bay (KB), East Africa (DR Congo). These photoferrotrophs produce oxidized iron {Fe(III)} and biomass, and support a diverse pelagic microbial community including heterotrophic Fe(III)-reducers, sulfate reducers, fermenters and methanogens. At modest light levels, rates of photoferrotrophy in KB exceed those predicted for early Earth primary production, and are sufficient to generate Earth's largest sedimentary iron ore deposits. Fe cycling, however, is efficient, and complex microbial community interactions likely regulate Fe(III) and organic matter export from the photic zone.

No MeSH data available.