Coexistence of Fe(II)- and Mn(II)-oxidizing bacteria govern the formation of deep sea umber deposits

Peng, Xiaotong; Ta, Kaiwen; Chen, Shun; Zhang, Lijuan; Xu, Hengchao

doi:10.1016/j.gca.2015.09.011

Cited by 28 publications

(18 citation statements)

References 48 publications

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“…Similar to the marine crust, electron acceptors and donors include iron ( Emerson et al, 2007 ; Heim et al, 2017 ), manganese ( Peng et al, 2015 ; Sylvan et al, 2015 ), sulfur species and hydrogen ( Osburn et al, 2014 ). Use of other metal species is reported but their significance is often unclear ( Kashefi and Lovley, 2000 ; Oremland, 2003 ; Lee et al, 2015 ).…”

Section: Earth’s Subsurface Habitat Typesmentioning

confidence: 99%

Low Energy Subsurface Environments as Extraterrestrial Analogs

2018

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Earth’s subsurface is often isolated from phototrophic energy sources and characterized by chemotrophic modes of life. These environments are often oligotrophic and limited in electron donors or electron acceptors, and include continental crust, subseafloor oceanic crust, and marine sediment as well as subglacial lakes and the subsurface of polar desert soils. These low energy subsurface environments are therefore uniquely positioned for examining minimum energetic requirements and adaptations for chemotrophic life. Current targets for astrobiology investigations of extant life are planetary bodies with largely inhospitable surfaces, such as Mars, Europa, and Enceladus. Subsurface environments on Earth thus serve as analogs to explore possibilities of subsurface life on extraterrestrial bodies. The purpose of this review is to provide an overview of subsurface environments as potential analogs, and the features of microbial communities existing in these low energy environments, with particular emphasis on how they inform the study of energetic limits required for life. The thermodynamic energetic calculations presented here suggest that free energy yields of reactions and energy density of some metabolic redox reactions on Mars, Europa, Enceladus, and Titan could be comparable to analog environments in Earth’s low energy subsurface habitats.

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Section: Earth’s Subsurface Habitat Typesmentioning

confidence: 99%

Low Energy Subsurface Environments as Extraterrestrial Analogs

2018

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“…Another structure that has commonly been observed in marine iron mats are short (~5–50 μm) Y-shaped tubular filaments (Emerson and Moyer, 2010 ; Breier et al, 2012 ; Moeller et al, 2014 ; Peng et al, 2015 ). In the intact mats these structures were commonly observed colonizing either the sheaths or stalks (Figure 6 ).…”

Section: Resultsmentioning

confidence: 99%

The Architecture of Iron Microbial Mats Reflects the Adaptation of Chemolithotrophic Iron Oxidation in Freshwater and Marine Environments

et al. 2016

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Microbes form mats with architectures that promote efficient metabolism within a particular physicochemical environment, thus studying mat structure helps us understand ecophysiology. Despite much research on chemolithotrophic Fe-oxidizing bacteria, Fe mat architecture has not been visualized because these delicate structures are easily disrupted. There are striking similarities between the biominerals that comprise freshwater and marine Fe mats, made by Beta- and Zetaproteobacteria, respectively. If these biominerals are assembled into mat structures with similar functional morphology, this would suggest that mat architecture is adapted to serve roles specific to Fe oxidation. To evaluate this, we combined light, confocal, and scanning electron microscopy of intact Fe microbial mats with experiments on sheath formation in culture, in order to understand mat developmental history and subsequently evaluate the connection between Fe oxidation and mat morphology. We sampled a freshwater sheath mat from Maine and marine stalk and sheath mats from Loihi Seamount hydrothermal vents, Hawaii. Mat morphology correlated to niche: stalks formed in steeper O2 gradients while sheaths were associated with low to undetectable O2 gradients. Fe-biomineralized filaments, twisted stalks or hollow sheaths, formed the highly porous framework of each mat. The mat-formers are keystone species, with nascent marine stalk-rich mats comprised of novel and uncommon Zetaproteobacteria. For all mats, filaments were locally highly parallel with similar morphologies, indicating that cells were synchronously tracking a chemical or physical cue. In the freshwater mat, cells inhabited sheath ends at the growing edge of the mat. Correspondingly, time lapse culture imaging showed that sheaths are made like stalks, with cells rapidly leaving behind an Fe oxide filament. The distinctive architecture common to all observed Fe mats appears to serve specific functions related to chemolithotrophic Fe oxidation, including (1) removing Fe oxyhydroxide waste without entombing cells or clogging flow paths through the mat and (2) colonizing niches where Fe(II) and O2 overlap. This work improves our understanding of Fe mat developmental history and how mat morphology links to metabolism. We can use these results to interpret biogenicity, metabolism, and paleoenvironmental conditions of Fe microfossil mats, which would give us insight into Earth's Fe and O2 history.

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“…Edwards et al, 2011;Emerson & Moyer, 2010;Johannessen et al, 2017;Peng, Ta, Chen, Zhang, & Xu, 2015;Scott et al, 2015) and have been assigned to Zetaproteobacteria through fluorescent in situ hybridization(Emerson, Scott, Leavitt, Fleming, & Moyer, 2017). The relatively short lengths of the tubes, along with their sporadic distribution and attachment to both sheaths and twisted stalks ledChan, McAllister, et al (2016) to propose that the tube-forming Fe-oxidizing micro-organism is a secondary colonizer adapted to the low O 2 concentrations prevailing at depth in the mat.…”

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On the biogenicity of Fe‐oxyhydroxide filaments in silicified low‐temperature hydrothermal deposits: Implications for the identification of Fe‐oxidizing bacteria in the rock record

et al. 2019

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Microaerophilic Fe(II)‐oxidizing bacteria produce biomineralized twisted and branched stalks, which are promising biosignatures of microbial Fe oxidation in ancient jaspers and iron formations. Extracellular Fe stalks retain their morphological characteristics under experimentally elevated temperatures, but the extent to which natural post‐depositional processes affect fossil integrity remains to be resolved. We examined siliceous Fe deposits from laminated mounds and chimney structures from an extinct part of the Jan Mayen Vent Fields on the Arctic Mid‐Ocean Ridge. Our aims were to determine how early seafloor diagenesis affects morphological and chemical signatures of Fe‐oxyhydroxide biomineralization and how extracellular stalks differ from abiogenic features. Optical and scanning electron microscopy in combination with focused ion beam‐transmission electron microscopy (FIB‐TEM) was used to study the filamentous textures and cross sections of individual stalks. Our results revealed directional, dendritic, and radial arrangements of biogenic twisted stalks and randomly organized networks of hollow tubes. Stalks were encrusted by concentric Fe‐oxyhydroxide laminae and silica casings. Element maps produced by energy dispersive X‐ray spectroscopy (EDS) in TEM showed variations in the content of Si, P, and S within filaments, demonstrating that successive hydrothermal fluid pulses mediate early diagenetic alteration and modify the chemical composition and surface features of stalks through Fe‐oxyhydroxide mineralization. The carbon content of the stalks was generally indistinguishable from background levels, suggesting that organic compounds were either scarce initially or lost due to percolating hydrothermal fluids. Dendrites and thicker abiotic filaments from a nearby chimney were composed of nanometer‐sized microcrystalline iron particles and silica and showed Fe growth bands indicative of inorganic precipitation. Our study suggests that the identification of fossil stalks and sheaths of Fe‐oxidizing bacteria in hydrothermal paleoenvironments may not rely on the detection of organic carbon and demonstrates that abiogenic filaments differ from stalks and sheaths of Fe‐oxidizing bacteria with respect to width distribution, ultrastructure, and textural context.

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Coexistence of Fe(II)- and Mn(II)-oxidizing bacteria govern the formation of deep sea umber deposits

Cited by 28 publications

References 48 publications

Low Energy Subsurface Environments as Extraterrestrial Analogs

Low Energy Subsurface Environments as Extraterrestrial Analogs

The Architecture of Iron Microbial Mats Reflects the Adaptation of Chemolithotrophic Iron Oxidation in Freshwater and Marine Environments

On the biogenicity of Fe‐oxyhydroxide filaments in silicified low‐temperature hydrothermal deposits: Implications for the identification of Fe‐oxidizing bacteria in the rock record

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