Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin.
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.
Laboratory of Freshwater Ecology, Research Unit in Environmental and Evolutionary Biology, University of Namur, B-5000 Namur, Belgium.|Department of Genetics and Microbiology, Universitat Autònoma de Barcelona, E-08913 Bellaterra, Catalonia, Spain.
Marc
M
Llirós
Ecologie des Systèmes Aquatiques, Université Libre de Bruxelles, B-1050 Brussels, Belgium.
Tamara
T
García-Armisen
Chemical Oceanography Unit, University of Liège, B-4000 Liège, Belgium.
François
F
Darchambeau
Department of Earth and Environmental Sciences, Katholieke Universiteit Leuven, B-3001 Leuven, Belgium.
Cédric
C
Morana
Integrative Freshwater Ecology Group, Center for Advanced Studies of Blanes - Spanish Research Council, E-17300 Blanes, Spain.|Group of Molecular Microbial Ecology, Institute of Aquatic Ecology, University of Girona, E-17071 Girona, Catalonia, Spain.
Xavier
X
Triadó-Margarit
Ecologie des Systèmes Aquatiques, Université Libre de Bruxelles, B-1050 Brussels, Belgium.
Özgül
Ö
Inceoğlu
Group of Molecular Microbial Ecology, Institute of Aquatic Ecology, University of Girona, E-17071 Girona, Catalonia, Spain.|Water Quality and Microbial Diversity, Catalan Institute for Water Research, E-17003, Girona, Catalonia, Spain.
Carles M
CM
Borrego
Department of Earth and Environmental Sciences, Katholieke Universiteit Leuven, B-3001 Leuven, Belgium.
Steven
S
Bouillon
Ecologie des Systèmes Aquatiques, Université Libre de Bruxelles, B-1050 Brussels, Belgium.
Pierre
P
Servais
Chemical Oceanography Unit, University of Liège, B-4000 Liège, Belgium.
Alberto V
AV
Borges
Laboratory of Freshwater Ecology, Research Unit in Environmental and Evolutionary Biology, University of Namur, B-5000 Namur, Belgium.
Jean-Pierre
JP
Descy
Institute of Biology, Nordic Center for Earth Evolution, University of Southern Denmark, 5230 Odense, Denmark.
Don E
DE
Canfield
Institute of Biology, Nordic Center for Earth Evolution, University of Southern Denmark, 5230 Odense, Denmark.|Departments of Microbiology and Immunology and Earth, Ocean, and Atmospheric Sciences, University of British Columbia, V6T 1Z3 Vancouver, Canada.
Sean A
SA
Crowe
D044822:Biodiversity; D003223:Congo; D018534:Earth, Planet; D004783:Environmental Microbiology; D005290:Ferric Compounds; D007501:Iron / Q000737:chemistry; D012432:Rwanda; D014867:Water / Q000737:chemistry*
D005290:Ferric Compounds; D014867:Water; D007501:Iron