Heme A-containing oxidases evolved in the ancestors of iron oxidizing bacteria

AbstractThe origin of oxygen respiration in bacteria has long intrigued biochemists, microbiologists and evolutionary biologists. The earliest enzymes that consume oxygen to extract energy did not evolve in the same lineages of photosynthetic bacteria that released oxygen on primordial earth, leading to the great oxygenation event (GOE). A widespread type of such enzymes is proton pumping cytochrome c oxidase (COX) that contains heme A, a unique prosthetic group for these oxidases. Here we show that the most ancestral proteins for the biosynthesis of heme A are present in extant acidophilic Fe2+-oxidizing Proteobacteria. Acidophilic Fe2+-oxidizers lived on emerged land around the time of the GOE, as suggested by the earliest geochemical evidence for aerobic respiration on paleoproterozoic earth. The gene for heme A synthase in acidophilic Fe2+-oxidizing Proteobacteria is associated with the COX gene cluster for iron oxidation. Compared to many other soil bacteria, the COX subunits encoded by this gene cluster are early diverging. Our data suggest that the ancient bacterial lineage which first evolved heme A-containing COX was related to the ancestors of present acidophilic Fe2+-oxidizers such as Acidiferrobacter and Acidithiobacillus spp. The copper leaching activity of such bacteria might have constituted a key ecological factor to promote COX evolution.

Download Full-text

Biogeochemistry and microbiology of microaerobic Fe(II) oxidation

Biochemical Society Transactions ◽

10.1042/bst20120154 ◽

2012 ◽

Vol 40 (6) ◽

pp. 1211-1216 ◽

Cited By ~ 22

Author(s):

David Emerson

Keyword(s):

Hydrothermal Vents ◽

Cytoplasmic Membrane ◽

Iron Oxidation ◽

Morphological Characteristics ◽

Genomic Analysis ◽

Freshwater Wetlands ◽

Iron Oxidizing Bacteria ◽

Resident Populations ◽

Extracellular Electron Transport

Today high Fe(II) environments are relegated to oxic–anoxic habitats with opposing gradients of O2 and Fe(II); however, during the late Archaean and early Proterozoic eons, atmospheric O2 concentrations were much lower and aqueous Fe(II) concentrations were significantly higher. In current Fe(II)-rich environments, such as hydrothermal vents, mudflats, freshwater wetlands or the rhizosphere, rusty mat-like deposits are common. The presence of abundant biogenic microtubular or filamentous iron oxyhydroxides readily reveals the role of FeOB (iron-oxidizing bacteria) in iron mat formation. Cultivation and cultivation-independent techniques, confirm that FeOB are abundant in these mats. Despite remarkable similarities in morphological characteristics between marine and freshwater FeOB communities, the resident populations of FeOB are phylogenetically distinct, with marine populations related to the class Zetaproteobacteria, whereas freshwater populations are dominated by members of the Gallionallaceae, a family within the Betaproteobacteria. Little is known about the mechanism of how FeOB acquire electrons from Fe(II), although it is assumed that it involves electron transfer from the site of iron oxidation at the cell surface to the cytoplasmic membrane. Comparative genomics between freshwater and marine strains reveals few shared genes, except for a suite of genes that include a class of molybdopterin oxidoreductase that could be involved in iron oxidation via extracellular electron transport. Other genes are implicated as well, and the overall genomic analysis reveals a group of organisms exquisitely adapted for growth on iron.

Download Full-text

Terraced Iron Formations: Biogeochemical Processes Contributing to Microbial Biomineralization and Microfossil Preservation

Geosciences ◽

10.3390/geosciences8120480 ◽

2018 ◽

Vol 8 (12) ◽

pp. 480 ◽

Cited By ~ 2

Author(s):

Jeremiah Shuster ◽

Maria Rea ◽

Barbara Etschmann ◽

Joël Brugger ◽

Frank Reith

Keyword(s):

Iron Oxidation ◽

Open Pit ◽

Annual Rainfall ◽

Biogeochemical Processes ◽

Iron Oxyhydroxide ◽

Iron Oxidizing Bacteria ◽

Ph Conditions ◽

Laminated Structures ◽

Iron Formations ◽

Circumneutral Ph

Terraced iron formations (TIFs) are laminated structures that cover square meter-size areas on the surface of weathered bench faces and tailings piles at the Mount Morgan mine, which is a non-operational open pit mine located in Queensland, Australia. Sampled TIFs were analyzed using molecular and microanalytical techniques to assess the bacterial communities that likely contributed to the development of these structures. The bacterial community from the TIFs was more diverse compared to the tailings on which the TIFs had formed. The detection of both chemolithotrophic iron-oxidizing bacteria, i.e., Acidithiobacillus ferrooxidans and Mariprofundus ferrooxydans, and iron-reducing bacteria, i.e., Acidobacterium capsulatum, suggests that iron oxidation/reduction are continuous processes occurring within the TIFs. Acidophilic, iron-oxidizing bacteria were enriched from the TIFs. High-resolution electron microscopy was used to characterize iron biomineralization, i.e., the association of cells with iron oxyhydroxide mineral precipitates, which served as an analog for identifying the structural microfossils of individual cells as well as biofilms within iron oxyhydroxide laminations—i.e., alternating layers containing schwertmannite (Fe16O16(OH)12(SO4)2) and goethite (FeO(OH)). Kinetic modeling estimated that it would take between 0.25–2.28 years to form approximately one gram of schwertmannite as a lamination over a one-m2 surface, thereby contributing to TIF development. This length of time could correspond with seasonable rainfall or greater than average annual rainfall. In either case, the presence of water is critical for sustaining microbial activity, and subsequently iron oxyhydroxide mineral precipitation. The TIFs from the Mount Morgan mine also contain laminations of gypsum (CaSO·2H2O) alternating with iron oxyhydroxide laminations. These gypsum laminations likely represented drier periods of the year, in which millimeter-size gypsum crystals presumably precipitated as water gradually evaporated. Interestingly, gypsum acted as a substrate for the attachment of cells and the growth of biofilms that eventually became mineralized within schwertmannite and goethite. The dissolution and reprecipitation of gypsum suggest that microenvironments with circumneutral pH conditions could exist within TIFs, thereby supporting iron oxidation under circumneutral pH conditions. In conclusion, this study highlights the relationship between microbes for the development of TIFs and also provides interpretations of biogeochemical processes contributing to the preservation of bacterial cells and entire biofilms under acidic conditions.

Download Full-text

Genome reduction in an abundant and ubiquitous soil bacterial lineage

10.1101/053942 ◽

2016 ◽

Cited By ~ 2

Author(s):

Tess E Brewer ◽

Kim M Handley ◽

Paul Carini ◽

Jack A Gibert ◽

Noah Fierer

Keyword(s):

Soil Bacteria ◽

Large Population ◽

Metabolic Reconstruction ◽

Soil Environment ◽

Genomic Databases ◽

Bacterial Phylotypes ◽

Bacterial Lineage ◽

Metabolic Versatility ◽

Soil Metagenome ◽

Soil Bacterial

AbstractAlthough bacteria within theVerrucomicrobiaphylum are pervasive in soils around the world, they are underrepresented in both isolate collections and genomic databases. Here we describe a single verrucomicrobial phylotype within the classSpartobacteriathat is not closely related to any previously described taxa. We examined >1000 soils and found this spartobacterial phylotype to be ubiquitous and consistently one of the most abundant soil bacterial phylotypes, particularly in grasslands, where it was typically the most abundant phylotype. We reconstructed a nearly complete genome of this phylotype from a soil metagenome for which we propose the provisional name ‘CandidatusUdaeobacter copiosus’. TheCa. U. copiosus genome is unusually small for soil bacteria, estimated to be only 2.81 Mbp compared to the predicted effective mean genome size of 4.74 Mbp for soil bacteria. Metabolic reconstruction suggests thatCa. U. copiosus is an aerobic chemoorganoheterotroph with numerous amino acid and vitamin auxotrophies. The large population size, relatively small genome and multiple putative auxotrophies characteristic ofCa. U. copiosus suggests that it may be undergoing streamlining selection to minimize cellular architecture, a phenomenon previously thought to be restricted to aquatic bacteria. Although many soil bacteria need relatively large, complex genomes to be successful in soil,Ca. U. copiosus appears to have identified an alternate strategy, sacrificing metabolic versatility for efficiency to become dominant in the soil environment.

Download Full-text

A Previously Uncharacterized, Nonphotosynthetic Member of the Chromatiaceae Is the Primary CO2-Fixing Constituent in a Self-Regenerating Biocathode

Applied and Environmental Microbiology ◽

10.1128/aem.02947-14 ◽

2014 ◽

Vol 81 (2) ◽

pp. 699-712 ◽

Cited By ~ 56

Author(s):

Zheng Wang ◽

Dagmar H. Leary ◽

Anthony P. Malanoski ◽

Robert W. Li ◽

W. Judson Hervey ◽

...

Keyword(s):

Microbial Fuel Cells ◽

Iron Oxidation ◽

Extracellular Electron Transfer ◽

Hydrogen Electrode ◽

Content Type ◽

Iron Oxidizing Bacteria ◽

Distinct Cluster ◽

The Family

ABSTRACTBiocathode extracellular electron transfer (EET) may be exploited for biotechnology applications, including microbially mediated O2reduction in microbial fuel cells and microbial electrosynthesis. However, biocathode mechanistic studies needed to improve or engineer functionality have been limited to a few select species that form sparse, homogeneous biofilms characterized by little or no growth. Attempts to cultivate isolates from biocathode environmental enrichments often fail due to a lack of some advantage provided by life in a consortium, highlighting the need to study and understand biocathode consortiain situ. Here, we present metagenomic and metaproteomic characterization of a previously described biocathode biofilm (+310 mV versus a standard hydrogen electrode [SHE]) enriched from seawater, reducing O2, and presumably fixing CO2for biomass generation. Metagenomics identified 16 distinct cluster genomes, 15 of which could be assigned at the family or genus level and whose abundance was roughly divided betweenAlpha- andGammaproteobacteria. A total of 644 proteins were identified from shotgun metaproteomics and have been deposited in the the ProteomeXchange with identifier PXD001045. Cluster genomes were used to assign the taxonomic identities of 599 proteins, withMarinobacter,Chromatiaceae, andLabrenziathe most represented. RubisCO and phosphoribulokinase, along with 9 other Calvin-Benson-Bassham cycle proteins, were identified fromChromatiaceae. In addition, proteins similar to those predicted for iron oxidation pathways of known iron-oxidizing bacteria were observed forChromatiaceae. These findings represent the first description of putative EET and CO2fixation mechanisms for a self-regenerating, self-sustaining multispecies biocathode, providing potential targets for functional engineering, as well as new insights into biocathode EET pathways using proteomics.

Download Full-text

Molecular Response of the Acidophilic Iron Oxidizer “Ferrovum” sp. JA12 to the Exposure to Elevated Concentrations of Ferrous Iron

Solid State Phenomena ◽

10.4028/www.scientific.net/ssp.262.482 ◽

2017 ◽

Vol 262 ◽

pp. 482-486 ◽

Cited By ~ 1

Author(s):

Sophie R. Ullrich ◽

Anja Poehlein ◽

Gloria J. Levicán ◽

Michael Schlömann ◽

Martin Mühling

Keyword(s):

Oxidative Stress ◽

Reactive Oxygen Species ◽

Gene Cluster ◽

Ferrous Iron ◽

Iron Oxidation ◽

Molecular Response ◽

Oxygen Species ◽

Transcriptome Data ◽

Oxidation Model ◽

Transcriptome Level

The response to elevated ferrous iron concentrations was investigated in the acidophilic iron oxidizer “Ferrovum” sp. JA12 at transcriptome level. Detoxification of reactive oxygen species appears to be the most important strategy to cope with oxidative stress. The proposed iron oxidation model in “Ferrovum” spp. was supported by the transcriptome data of “Ferrovum” sp. JA12. Several gene candidates of the iron oxidation model are organized in a gene cluster conserved in iron oxidizing betaproteobacteria and zetaproteobacteria possibly indicating a common origin of iron oxidation.

Download Full-text

Continuous biological ferrous iron oxidation in a submerged membrane bioreactor

Water Science & Technology ◽

10.2166/wst.2005.0622 ◽

2005 ◽

Vol 51 (6-7) ◽

pp. 59-68 ◽

Cited By ~ 5

Author(s):

D. Park ◽

D.S. Lee ◽

J.M. Park

Keyword(s):

Ferrous Iron ◽

Membrane Bioreactor ◽

Ferric Iron ◽

Iron Oxidation ◽

Membrane Module ◽

Microbial Oxidation ◽

High Density Culture ◽

Submerged Membrane Bioreactor ◽

Ferrous Iron Oxidation ◽

Iron Oxidizing Bacteria

Microbial oxidation of ferrous iron may be available alternative method of producing ferric iron, which is a reagent used for removal of H2S from biogas. In this study, a submerged membrane bioreactor (MBR) system was employed to oxidize ferrous iron to ferric iron. In the submerged MBR system, we could keep high concentration of iron-oxidizing bacteria and high oxidation rate of ferrous iron. There was membrane fouling caused by chemical precipitates such as K-jarosite and ferric phosphate. However, a strong acidity (pH 1.75) of solution and low ferrous iron concentration (below 3000 mg/l) significantly reduced the fouling of membrane module during the bioreactor operation. A fouled membrane module could be easily regenerated with a 1 M of sulfuric acid solution. In conclusion, the submerged MBR could be used for high-density culture of iron-oxidizing bacteria and for continuous ferrous iron oxidation. As far as our knowledge concerns, this is the first study on the application of a submerged MBR to high acidic conditions (below pH 2).

Download Full-text

Respiratory gene clusters of Metallosphaera sedula – differential expression and transcriptional organization

Microbiology ◽

10.1099/mic.0.27515-0 ◽

2005 ◽

Vol 151 (1) ◽

pp. 35-43 ◽

Cited By ~ 42

Author(s):

Ulrike Kappler ◽

Lindsay I. Sly ◽

Alastair G. McEwan

Keyword(s):

Differential Expression ◽

Gene Cluster ◽

Iron Oxidation ◽

Gene Clusters ◽

Terminal Oxidase ◽

Difference Spectra ◽

Oxidase Gene ◽

Expression Levels ◽

Metallosphaera Sedula ◽

Complex Analogue

Metallosphaera sedula is a thermoacidophilic Crenarchaeon which is capable of leaching metals from sulfidic ores. The authors have investigated the presence and expression of genes encoding respiratory complexes in this organism when grown heterotrophically or chemolithotrophically on either sulfur or pyrite. The presence of three gene clusters, encoding two terminal oxidase complexes, the quinol oxidase SoxABCD and the SoxM oxidase supercomplex, and a gene cluster encoding a high-potential cytochrome b and components of a bc 1 complex analogue (cbsBA–soxL2N gene cluster) was established. Expression studies showed that the soxM gene was expressed to high levels during heterotrophic growth of M. sedula on yeast extract, while the soxABCD mRNA was most abundant in cells grown on sulfur. Reduced-minus-oxidized difference spectra of cell membranes showed cytochrome-related peaks that correspond to published spectra of Sulfolobus-type terminal oxidase complexes. In pyrite-grown cells, expression levels of the two monitored oxidase gene clusters were reduced by a factor of 10–12 relative to maximal expression levels, although spectra of membranes clearly contained oxidase-associated haems, suggesting the presence of additional gene clusters encoding terminal oxidases in M. sedula. Pyrite- and sulfur-grown cells contained high levels of the cbsA transcript, which encodes a membrane-bound cytochrome b with a possible role in iron oxidation or chemolithotrophy. The cbsA gene is not co-transcribed with the soxL2N genes, and therefore does not appear to be an integral part of this bc 1 complex analogue. The data show for the first time the differential expression of the Sulfolobus-type terminal oxidase gene clusters in a Crenarchaeon in response to changing growth modes.

Download Full-text

Carbonate polymorphism controlled by microbial iron redox dynamics at a natural CO2 leakage site (Crystal Geyser, Utah)

10.31223/x5pw43 ◽

2021 ◽

Author(s):

Julie Cosmidis ◽

Shane O'Reilly ◽

Eric Ellison ◽

Katherine Crispin ◽

David Diercks ◽

...

Keyword(s):

Iron Oxide ◽

Carbon Capture ◽

Iron Oxidation ◽

Carbon Capture And Storage ◽

Co2 Leakage ◽

Natural Analog ◽

Carbonate Formation ◽

Iron Oxidizing Bacteria ◽

Microbial Iron Oxidation ◽

Iron Redox

Crystal Geyser (Utah, USA) is a CO2-rich low-temperature geyser that is studied as a natural analog for CO2 leakage from carbon capture and storage (CCS) sites. In order to better constrain the biogeochemical processes influencing CaCO3 precipitation at geological CO2 escape sites, we characterized fast-forming iron-rich calcium carbonate pisoids and travertines precipitating from the fluids expelled by the geyser. The pisoids, located within a few meters from the vent, are composed of concentric layers of aragonite and calcite. Calcite layers contain abundant ferrihydrite shrubs in which iron is encasing bacterial forms. The aragonite layers contain less abundant and finely dispersed iron, present either as iron-oxide microspherules or iron adsorbed to organic matter dispersed within the carbonate matrix. We propose that carbonate polymorphism in the pisoids is mostly controlled by local fluctuations of the iron redox state of the fluids from which they form, caused by episodic blooms of iron-oxidizing bacteria. Indeed, the waters expelled by Crystal Geyser contain >200 µM dissolved iron (Fe2+), a known inhibitor of calcite growth. The calcite layers of the pisoids may record episodes of intense microbial iron oxidation, consistent with observations of iron-oxide rich biofilms thriving in the rimstone pools around the geyser and previous metagenomic analyses showing abundant neutrophilic, microaerophilic iron-oxidizing bacteria in vent water. In turn, aragonite layers of the pisoids likely precipitate from Fe2+-rich waters, registering periods of less intense iron oxidation. Separately, CaCO3 polymorphism in the travertines, where calcite and aragonite precipitate concurrently, is not controlled by iron dynamics, but may be locally influenced by the presence of microbial biofilms. This study documents for the first time an influence of microbial iron oxidation on CaCO3 polymorphism in the environment, and informs our understanding of carbonate formation at CO2 leakage sites and in CCS contexts.

Download Full-text

Immobilization of New Isolated Iron Oxidizing Bacteria on Natural Carriers

Advanced Materials Research ◽

10.4028/www.scientific.net/amr.825.388 ◽

2013 ◽

Vol 825 ◽

pp. 388-391 ◽

Cited By ~ 1

Author(s):

Arevik K. Vardanyan ◽

L.S. Markosyan ◽

Narine S. Vardanyan

Keyword(s):

Immobilized Cells ◽

Iron Oxidation ◽

Ferrous Ion ◽

Enzymatic System ◽

Iron Oxidizing Bacteria ◽

Physico Chemical ◽

Glass Column ◽

Shake Flasks ◽

Chemical Conditions ◽

Sulfide Ions

The bioleaching of sulfide minerals by iron oxidizing bacteria are implemented by direct and indirect mechanisms. The direct dissolution of minerals is caused by the attack of sulfide ions by enzymatic system of bacteria. In the indirect mechanism the ferric ion from oxidation of ferrous iron serves as a leaching agent that reacts chemically with the minerals. The increase of ferrous ion oxidation contributes to the intensification of bioleaching process. On this purpose the immobilization of iron oxidizing bacteria on different organic and inorganic carriers (calcium alginate, carragiran, ceramic support, activated carbon, porous glass, etc.) has been implemented which allows to increase cell concentration. In the present work for the first time the native shungit, zeolit and their chemically modified forms have been used for immobilization of new isolated iron oxidizing bacteria of the genera Leptospirillum and Sulfobacillus. Efficient physico-chemical conditions for immobilization on the mentioned carriers have been developed. The ferrous ion oxidation by immobilized cells has been studied both in shake-flasks experiments and in the glass column using air-lift process. It has been shown that in both cases the rate of iron oxidation considerably enhances in comparison with free cells.

Download Full-text

Bioleaching of E-Waste: Influence of Printed Circuit Boards on the Activity of Acidophilic Iron-Oxidizing Bacteria

Frontiers in Microbiology ◽

10.3389/fmicb.2021.669738 ◽

2021 ◽

Vol 12 ◽

Author(s):

Juan Anaya-Garzon ◽

Agathe Hubau ◽

Catherine Joulian ◽

Anne-Gwénaëlle Guezennec

Keyword(s):

Microbial Activity ◽

Printed Circuit Boards ◽

Iron Oxidation ◽

Circuit Boards ◽

Printed Circuit ◽

Inhibiting Effect ◽

Promising Strategy ◽

Iron Oxidizing Bacteria ◽

Valuable Metals ◽

Enriched Environments

Bioleaching is a promising strategy to recover valuable metals from spent printed circuit boards (PCBs). The performance of the process is catalyzed by microorganisms, which the toxic effect of PCBs can inhibit. This study aimed to investigate the capacity of an acidophilic iron-oxidizing culture, mainly composed of Leptospirillum ferriphilum, to oxidize iron in PCB-enriched environments. The culture pre-adapted to 1% (w/v) PCB content successfully thrived in leachates with the equivalent of 6% of PCBs, containing 8.5 g L–1 Cu, 8 g L–1 Fe, 1 g L–1 Zn, 92 mg L–1 Ni, 12.6 mg L–1 Pb, and 4.4 mg L–1 Co, among other metals. However, the inhibiting effect of PCBs limited the microbial activity by delaying the onset of the exponential iron oxidation. Successive subcultures boosted the activity of the culture by reducing this delay by up to 2.6 times under batch conditions. Subcultures also favored the rapid establishment of high microbial activity in continuous mode.

Download Full-text