Experimental diagenesis of organo-mineral structures formed by microaerophilic Fe(II)-oxidizing bacteria

Picard, Aude; Kappler, Andreas; Schmid, Gregor; Quaroni, Luca; Obst, Martin

doi:10.1038/ncomms7277

Cited by 85 publications

(95 citation statements)

References 66 publications

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“…As for all laboratory simulations, the present experiments do not exactly mimic what really occurs in natural settings during millions of years 22, 25, 29, 31, 33–35 . Biodegradation and early taphonomic processes that may occur within sediments have not been simulated here, even though they may also alter the chemical composition of organic materials before the beginning of thermal maturation 14, 56 .…”

Section: Discussionmentioning

confidence: 59%

Organic molecular heterogeneities can withstand diagenesis

Alleon

Bernard

Guillou

et al. 2017

Sci Rep

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Reconstructing the original biogeochemistry of organic fossils requires quantifying the extent of the chemical transformations that they underwent during burial-induced maturation processes. Here, we performed laboratory experiments on chemically different organic materials in order to simulate the thermal maturation processes that occur during diagenesis. Starting organic materials were microorganisms and organic aerosols. Scanning transmission X-ray microscopy (STXM) was used to collect X-ray absorption near edge spectroscopy (XANES) data of the organic residues. Results indicate that even after having been submitted to 250 °C and 250 bars for 100 days, the molecular signatures of microorganisms and aerosols remain different in terms of nitrogen-to-carbon atomic ratio and carbon and nitrogen speciation. These observations suggest that burial-induced thermal degradation processes may not completely obliterate the chemical and molecular signatures of organic molecules. In other words, the present study suggests that organic molecular heterogeneities can withstand diagenesis and be recognized in the fossil record.The fossil record contains crucial information about the evolution of Life on Earth 1, 2 . Molecular investigations regarding ancient Life are yet limited by the poor quality of the 'biogeochemical' signals preserved in the fossil record: in addition to biodegradation, burial-induced alteration processes (i.e. thermal maturation) inevitably modify the original biochemical signatures of fossilized organic molecules 1, 3 . With increasing temperature, weaker organic bonds are thermally broken and significant deoxygenation and dehydrogenation reactions occur 1, 4 . Thermal degradation eventually promotes increasing structural reorganization and may ultimately lead to the formation of pure graphite 5,6 .It has long been recognized that biomacromolecules exhibit conspicuous differences in decay in natural environments 7,8 . For instance, cell-wall biopolymers that protect some algae, cysts, spores and pollen grains are intrinsically more resistant than polysaccharides, proteins and nucleic acids 9-11 . In some contexts, taxon-specific chemosystematic data can even be preserved in the fossil record 12,13 . Still, the general perception in paleobiology remains that thermal maturation processes lead to a converging composition of organic materials from different origins, thereby limiting the use of chemical composition for discriminating between possibly different fossilized taxa 14 .Taking advantage of advanced spectroscopic tools (including synchrotron-based techniques), a number of studies have demonstrated that organic molecules may undergo only partial degradation during diagenesis in natural settings [15][16][17][18][19][20][21][22][23][24] . In parallel, laboratory experiments have helped evaluating the influence of key factors such as the pressure-temperature conditions, the redox conditions, the presence or absence of a fluid or of certain mineral phases on the degradation of organics 22,[25][26][27][28...

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Section: Discussionmentioning

confidence: 59%

Organic molecular heterogeneities can withstand diagenesis

Alleon

Bernard

Guillou

et al. 2017

Sci Rep

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“…In the organic carbon fraction of the twisted stalks, we found polysaccharides, saturated aliphatic compounds (most probably lipids), and a very small amount of protein. Similar compounds have been detected in stalks of other marine and also freshwater microaerophilic Fe(II)-oxidizing bacteria, but not all authors detected lipids (29,(32)(33)(34)(35). The indication of membrane lipids we found by FTIR could be due to the adsorption of cellular material, which might also be true for the detected protein.…”

Section: Figmentioning

confidence: 59%

“…saccharides, saturated lipids, and a small amount of protein (29,(32)(33)(34)(35). However, more detailed information on the exact nature of these organic compounds is so far lacking.…”

mentioning

confidence: 99%

Microaerophilic Fe(II)-Oxidizing Zetaproteobacteria Isolated from Low-Fe Marine Coastal Sediments: Physiology and Composition of Their Twisted Stalks

Laufer

Nordhoff

Halama

et al. 2017

Appl Environ Microbiol

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Microaerophilic Fe(II) oxidizers are commonly found in habitats containing elevated Fe(II) and low O 2 concentrations and often produce characteristic Fe mineral structures, so-called twisted stalks or tubular sheaths. Isolates originating from freshwater habitats are all members of the Betaproteobacteria, while isolates from marine habitats belong almost exclusively to the Zetaproteobacteria. So far, only a few isolates of marine microaerophilic Fe(II) oxidizers have been described, all of which are obligate microaerophilic Fe(II) oxidizers and have been thought to be restricted to Fe-rich systems. Here, we present two new isolates of marine microaerophilic Fe(II)-oxidizing Zetaproteobacteria that originate from typical coastal marine sediments containing only low Fe concentrations (2 to 11 mg of total Fe/g of sediment [dry weight]; 70 to 100 M dissolved Fe 2ϩ in the porewater). The two novel Zetaproteobacteria share characteristic physiological properties of the Zetaproteobacteria group, even though they come from low-Fe environments: the isolates are obligate microaerophilic Fe(II) oxidizers and, like most isolated Zetaproteobacteria, they produce twisted stalks. We found a low organic carbon content in the stalks (ϳ0.3 wt%), with mostly polysaccharides and saturated aliphatic chains (most likely lipids). The Fe minerals in the stalks were identified as lepidocrocite and possibly ferrihydrite. Immobilization experiments with Ni 2ϩ showed that the stalks can function as a sink for trace metals. Our findings show that obligate microaerophilic Fe(II) oxidizers belonging to the Zetaproteobacteria group are not restricted to Fe-rich environments but can also be found in low-Fe marine environments, which increases their overall importance for the global biogeochemical Fe cycle.IMPORTANCE So far, only a few isolates of benthic marine microaerophilic Fe(II) oxidizers belonging to the Zetaproteobacteria exist, and most isolates were obtained from habitats containing elevated Fe concentrations. Consequently, it was thought that these microorganisms are important mainly in habitats with high Fe concentrations. The two novel isolates of Zetaproteobacteria that are presented in the present study were isolated from typical coastal marine sediments that do not contain elevated Fe concentrations. This increases the knowledge about possible habitats in which Zetaproteobacteria can exist. Furthermore, we show that the physiology and the typical organo-mineral structures (twisted stalks) that are produced by the isolates do not notably differ from the physiology and the cell-mineral structures of

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“…Fe oxide stalks from freshwater mats have been shown to survive metamorphic conditions similar to those of the least metamorphosed BIFs (Picard et al, 2015). Indeed, stalk-like morphologies have been observed in the rock record (Hofmann & Farmer, 2000;Little et al, 2004;Slack et al, 2007), although stalks have not yet been observed in BIFs.…”

Section: Fe Microbial Matsmentioning

confidence: 99%

The role of microaerophilic Fe‐oxidizing micro‐organisms in producing banded iron formations

2016

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Despite the historical and economic significance of banded iron formations (BIFs), we have yet to resolve the formation mechanisms. On modern Earth, neutrophilic microaerophilic Fe-oxidizing micro-organisms (FeOM) produce copious amounts of Fe oxyhydroxides, leading us to wonder whether similar organisms played a role in producing BIFs. To evaluate this, we review the current knowledge of modern microaerophilic FeOM in the context of BIF paleoenvironmental studies. In modern environments wherever Fe(II) and O2 co-exist, microaerophilic FeOM proliferate. These organisms grow in a variety of environments, including the marine water column redoxcline, which is where BIF precursor minerals likely formed. FeOM can grow across a range of O2 concentrations, measured as low as 2 μm to date, although lower concentrations have not been tested. While some extant FeOM can tolerate high O2 concentrations, many FeOM appear to prefer and thrive at low O2 concentrations (~3-25 μm). These are similar to the estimated dissolved O2 concentrations in the few hundred million years prior to the 'Great Oxidation Event' (GOE). We compare biotic and abiotic Fe oxidation kinetics in the presence of varying levels of O2 and show that microaerophilic FeOM contribute substantially to Fe oxidation, at rates fast enough to account for BIF deposition. Based on this synthesis, we propose that microaerophilic FeOM were capable of playing a significant role in depositing the largest, most well-known BIFs associated with the GOE, as well as afterward when global O2 levels increased.

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Experimental diagenesis of organo-mineral structures formed by microaerophilic Fe(II)-oxidizing bacteria

Cited by 85 publications

References 66 publications

Organic molecular heterogeneities can withstand diagenesis

Organic molecular heterogeneities can withstand diagenesis

Microaerophilic Fe(II)-Oxidizing Zetaproteobacteria Isolated from Low-Fe Marine Coastal Sediments: Physiology and Composition of Their Twisted Stalks

The role of microaerophilic Fe‐oxidizing micro‐organisms in producing banded iron formations

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