Physiological characterization of a halotolerant anoxygenic phototrophic Fe(II)-oxidizing green-sulfur bacterium isolated from a marine sediment

Abstract

Anoxygenic photoautotrophic bacteria which use light energy and electrons from Fe(II) for growth, so-called photoferrotrophs, are suggested to have been amongst the first phototrophic microorganisms on Earth and to have contributed to the deposition of sedimentary iron mineral deposits, i.e. banded iron formations. To date only two isolates of marine photoferrotrophic bacteria exist, both of which are closely related purple non-sulfur bacteria. Here we present a novel green-sulfur photoautotrophic Fe(II) oxidizer isolated from a marine coastal sediment, Chlorobium sp. strain N1, which is closely related to the freshwater green-sulfur bacterium Chlorobium luteolum DSM273 that is incapable of Fe(II) oxidation. Besides Fe(II), our isolated strain grew phototrophically with other inorganic and organic substrates such as sulfide, hydrogen, lactate or yeast extract. Highest Fe(II) oxidation rates were measured at pH 7.0-7.3, the temperature optimum was 25°C. Mössbauer spectroscopy identified ferrihydrite as the main Fe(III) mineral and fluorescence and helium-ion microscopy revealed cell-mineral aggregates without obvious cell encrustation. In summary, our study showed that the new isolate is physiologically adapted to the conditions of its natural habitat but also to conditions as proposed for early Earth and is thus a suitable model organism for further studies addressing phototrophic Fe(II) oxidation on early Earth.

Microbial anaerobic Fe(II) oxidation – Ecology, mechanisms and environmental implications

“…These include Chlorobium ferrooxidans strain KoFox (Heising et al ., ) and two recently isolated species: Chlorobium phaeoferrooxidans (Crowe et al ., ; Thompson et al ., ) and Chlorobium sp. strain N1 which is closely related to Chlorobium luteolum (Laufer et al ., ). These organisms typically oxidize aqueous Fe(II) completely under normal culture conditions, similarly to Culture KS and in contrast to most other NRFeOx bacteria.…”

“…Green sulfur bacteria such as Chlorobium sp. strain N1, however, utilize higher light intensities (saturation at 400 lux) thus they are not limited to very low light environments (Laufer et al, 2017). All isolated anoxygenic phototrophic Fe(II)oxidizers are metabolically flexible and have the ability to utilize multiple electron donors for CO 2 fixation instead of Fe(II), such as H 2 and H 2 S (Croal et al, 2009).…”

“…Yet, the extent to which cells and minerals are associated seems to be strain-specific. Furthermore, varying cell-mineral aggregate morphologies, ranging from irregular and bulbous to more symmetric (e.g., flowerand star-like shapes) have been reported and seem to depend on the mineralogy and age of culture (Ehrenreich and Widdel, 1994;Kappler and Newman, 2004;Jiao et al, 2005;Posth et al, 2010;Wu et al, 2014;Gauger et al, 2015;Laufer et al, 2017).…”

Proteome Response of a Metabolically Flexible Anoxygenic Phototroph to Fe(II) Oxidation

“…Ϫ ϩ 4Fe 2ϩ ϩ 10H 2 O ϩ hv → (CH 2 O) ϩ 4Fe(OH) 3 ϩ 7H ϩ (1) This process is thought to have fueled the Earth's biosphere prior to the evolution of oxygenic photosynthesis and is likely to have been a key contributor in the deposition of vast formations of layered Fe(II)-Fe(III) and Si-rich rock during Earth's early history (1)(2)(3). Organisms capable of this metabolism are still found in many modern environments, including Fe(II)-rich (4)(5)(6)(7) and Fe(II)-poor (8) stratified lakes, as well as both freshwater (9,10) and marine sediments (11)(12)(13)(14). These microorganisms belong to the purple sulfur bacteria (Gammaproteobacteria), purple nonsulfur bacteria (Alphaproteobacteria), and green sulfur bacteria (Chlorobi).…”

“…Anoxygenic phototrophs show remarkable versatility with regard to their metabolism. They can fix CO 2 using Fe(II), H 2 , or H 2 S as an electron donor (photoautotrophy), or they can use organic compounds as a carbon source (photoheterotrophy) (9,10,12,14,15). Some isolates can also grow chemoheterotrophically with dioxygen without any light at all, e.g., Rhodopseudomonas palustris TIE-1 (Jiao et al [9]).…”