Abstract
Anoxygenic phototrophic bacteria can be important primary producers in some meromictic lakes. Green sulfur bacteria (GSB) have been detected in ferruginous lakes, with some evidence that they are photosynthesizing using Fe(II) as an electron donor (i.e., photoferrotrophy). However, some photoferrotrophic GSB can also utilize reduced sulfur compounds, complicating the interpretation of Fe-dependent photosynthetic primary productivity. An enrichment (BLA1) from meromictic ferruginous Brownie Lake, Minnesota, United States, contains an Fe(II)-oxidizing GSB and a metabolically flexible putative Fe(III)-reducing anaerobe. “Candidatus Chlorobium masyuteum” grows photoautotrophically with Fe(II) and possesses the putative Fe(II) oxidase-encoding cyc2 gene also known from oxygen-dependent Fe(II)-oxidizing bacteria. It lacks genes for oxidation of reduced sulfur compounds. Its genome encodes for hydrogenases and a reverse TCA cycle that may allow it to utilize H2 and acetate as electron donors, an inference supported by the abundance of this organism when the enrichment was supplied by these substrates and light. The anaerobe “Candidatus Pseudopelobacter ferreus” is in low abundance (∼1%) in BLA1 and is a putative Fe(III)-reducing bacterium from the Geobacterales ord. nov. While “Ca. C. masyuteum” is closely related to the photoferrotrophs C. ferroooxidans strain KoFox and C. phaeoferrooxidans strain KB01, it is unique at the genomic level. The main light-harvesting molecule was identified as bacteriochlorophyll c with accessory carotenoids of the chlorobactene series. BLA1 optimally oxidizes Fe(II) at a pH of 6.8, and the rate of Fe(II) oxidation was 0.63 ± 0.069 mmol day–1, comparable to other photoferrotrophic GSB cultures or enrichments. Investigation of BLA1 expands the genetic basis for phototrophic Fe(II) oxidation by GSB and highlights the role these organisms may play in Fe(II) oxidation and carbon cycling in ferruginous lakes.
Highlights
Iron is a major redox-active element on Earth (Raiswell and Canfield, 2012)
Prior to the development of oxygenated surface waters after the Great Oxidation Event (GOE) at ∼2.4 billion years ago (Ga), anoxygenic photosynthetic bacteria (APB) that could utilize Fe(II) in the photic zone may have been the major marine primary producers fueling the biosphere in the Archean (4.0–2.5 Ga), sustaining up to 10% of modern-day primary productivity prior to the evolution of oxygenic photosynthesis by Cyanobacteria (Canfield et al, 2006; Jones et al, 2015)
The enrichment was subsequently named “BLA1,” as the first enrichment (A1) from Browne Lake (BL), and this epithet is applied to the dominant strain within the enrichment
Summary
Iron is a major redox-active element on Earth (Raiswell and Canfield, 2012). The biogeochemical cycling between the two main redox states, Fe(II) and Fe(III), is accomplished by both aerobic and anaerobic microbes, as well as abiotic chemical reactions (Melton et al, 2014). Prior to the development of oxygenated surface waters after the Great Oxidation Event (GOE) at ∼2.4 billion years ago (Ga), anoxygenic photosynthetic bacteria (APB) that could utilize Fe(II) in the photic zone may have been the major marine primary producers fueling the biosphere in the Archean (4.0–2.5 Ga), sustaining up to 10% of modern-day primary productivity prior to the evolution of oxygenic photosynthesis by Cyanobacteria (Canfield et al, 2006; Jones et al, 2015) These organisms, collectively known as photoferrotrophs, are bacteria that use light energy, Fe(II) as an electron donor, and inorganic carbon to perform anoxygenic photosynthesis (Ehrenreich and Widdel, 1994; Kappler et al, 2005): light (hv) + 4Fe2+ + CO2 + 11H2O. The organism described here is only the second photoferrotroph to be brought into enrichment from a ferruginous water column, which highlights the difficulties, and value, in bringing these organisms into culture
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