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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.


Physical and chemical depth profiles from Kabuno Bay.Data in the upper panels are from the rainy season (RS; February 2012) and lower panels from the dry season (DS; October 2012). (a,e) temperature (ºC), conductivity (μS cm−1), and pH; (b,f) dissolved oxygen (DO, μM), sulfide (HS−, μM), sulfate (SO4−, μM), and dissolved ferrous Fe (μM); (c,g) particulate ferrous Fe {Fe(II)} and ferric Fe {Fe(III)} (μM), and ratio of particulate Fe(II) with respect to total particulate Fe (i.e., particulate Fe(II)/[particulate Fe(II) + particulate Fe(III)]); (d,h) light (% PAR) and turbidity (FTU) profiles, and Chl a (μg l−1) and intercalibrated BChl e concentration (μg l−1) measured with multiparametric probes.
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f1: Physical and chemical depth profiles from Kabuno Bay.Data in the upper panels are from the rainy season (RS; February 2012) and lower panels from the dry season (DS; October 2012). (a,e) temperature (ºC), conductivity (μS cm−1), and pH; (b,f) dissolved oxygen (DO, μM), sulfide (HS−, μM), sulfate (SO4−, μM), and dissolved ferrous Fe (μM); (c,g) particulate ferrous Fe {Fe(II)} and ferric Fe {Fe(III)} (μM), and ratio of particulate Fe(II) with respect to total particulate Fe (i.e., particulate Fe(II)/[particulate Fe(II) + particulate Fe(III)]); (d,h) light (% PAR) and turbidity (FTU) profiles, and Chl a (μg l−1) and intercalibrated BChl e concentration (μg l−1) measured with multiparametric probes.

Mentions: Kabuno Bay (KB) is a ferruginous sub-basin of Lake Kivu, situated in the heart of East Africa on the border of the Democratic Republic of Congo (DRC) and Rwanda (Supplementary Fig. S1). Lake Kivu is of tectonic origin and is fed by deep-water inflows containing high concentrations of dissolved salts and geogenic gases7. KB is separated from the main basin of Lake Kivu by a shallow volcanic sill that restricts water exchange between the basins7. KB has a strongly stratified water column with oxic surface waters giving way to anoxic waters below about 10 m (Fig. 1a,b,e,f; Supplementary Fig. S2a,e)7. The deep anoxic waters of KB are iron-rich (Fe(II), 0.5M HCl extractable), containing up to 1.2 mM ferrous Fe {Fe(II)}, unlike the deep waters of Lake Kivu’s main basin, which contain abundant hydrogen sulfide (ca. 0.3 mM in deep waters)8. Fe(II)-rich hydrothermal springs with chemistry matching deep waters of KB are observed within the catchment basin9 (Supplementary Table S1), implicating hydrothermal Fe inputs to KB. Oxidation of upward diffusing Fe(II) generates both sharp gradients in dissolved Fe(II) concentration and an accumulation of mixed-valence Fe particles around the oxic-anoxic boundary (i.e., chemocline; Fig. 1b,c,f,g). Reduction of the settling particulate ferric Fe {Fe(III)} to Fe(II) partly closes the Fe-cycle (Fig. 1c,g).


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)

Physical and chemical depth profiles from Kabuno Bay.Data in the upper panels are from the rainy season (RS; February 2012) and lower panels from the dry season (DS; October 2012). (a,e) temperature (ºC), conductivity (μS cm−1), and pH; (b,f) dissolved oxygen (DO, μM), sulfide (HS−, μM), sulfate (SO4−, μM), and dissolved ferrous Fe (μM); (c,g) particulate ferrous Fe {Fe(II)} and ferric Fe {Fe(III)} (μM), and ratio of particulate Fe(II) with respect to total particulate Fe (i.e., particulate Fe(II)/[particulate Fe(II) + particulate Fe(III)]); (d,h) light (% PAR) and turbidity (FTU) profiles, and Chl a (μg l−1) and intercalibrated BChl e concentration (μg l−1) measured with multiparametric probes.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f1: Physical and chemical depth profiles from Kabuno Bay.Data in the upper panels are from the rainy season (RS; February 2012) and lower panels from the dry season (DS; October 2012). (a,e) temperature (ºC), conductivity (μS cm−1), and pH; (b,f) dissolved oxygen (DO, μM), sulfide (HS−, μM), sulfate (SO4−, μM), and dissolved ferrous Fe (μM); (c,g) particulate ferrous Fe {Fe(II)} and ferric Fe {Fe(III)} (μM), and ratio of particulate Fe(II) with respect to total particulate Fe (i.e., particulate Fe(II)/[particulate Fe(II) + particulate Fe(III)]); (d,h) light (% PAR) and turbidity (FTU) profiles, and Chl a (μg l−1) and intercalibrated BChl e concentration (μg l−1) measured with multiparametric probes.
Mentions: Kabuno Bay (KB) is a ferruginous sub-basin of Lake Kivu, situated in the heart of East Africa on the border of the Democratic Republic of Congo (DRC) and Rwanda (Supplementary Fig. S1). Lake Kivu is of tectonic origin and is fed by deep-water inflows containing high concentrations of dissolved salts and geogenic gases7. KB is separated from the main basin of Lake Kivu by a shallow volcanic sill that restricts water exchange between the basins7. KB has a strongly stratified water column with oxic surface waters giving way to anoxic waters below about 10 m (Fig. 1a,b,e,f; Supplementary Fig. S2a,e)7. The deep anoxic waters of KB are iron-rich (Fe(II), 0.5M HCl extractable), containing up to 1.2 mM ferrous Fe {Fe(II)}, unlike the deep waters of Lake Kivu’s main basin, which contain abundant hydrogen sulfide (ca. 0.3 mM in deep waters)8. Fe(II)-rich hydrothermal springs with chemistry matching deep waters of KB are observed within the catchment basin9 (Supplementary Table S1), implicating hydrothermal Fe inputs to KB. Oxidation of upward diffusing Fe(II) generates both sharp gradients in dissolved Fe(II) concentration and an accumulation of mixed-valence Fe particles around the oxic-anoxic boundary (i.e., chemocline; Fig. 1b,c,f,g). Reduction of the settling particulate ferric Fe {Fe(III)} to Fe(II) partly closes the Fe-cycle (Fig. 1c,g).

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.