Mechanisms Involved in Fe(III) Respiration by the Hyperthermophilic Archaeon Ferroglobus placidus

Abstract

The hyperthermophilic archaeon Ferroglobus placidus can utilize a wide variety of electron donors, including hydrocarbons and aromatic compounds, with Fe(III) serving as an electron acceptor. In Fe(III)-reducing bacteria that have been studied to date, this process is mediated by c-type cytochromes and type IV pili. However, there currently is little information available about how this process is accomplished in archaea. In silico analysis of the F. placidus genome revealed the presence of 30 genes coding for putative c-type cytochrome proteins (more than any other archaeon that has been sequenced to date), five of which contained 10 or more heme-binding motifs. When cell extracts were analyzed by SDS-PAGE followed by heme staining, multiple bands corresponding to c-type cytochromes were detected. Different protein expression patterns were observed in F. placidus cells grown on soluble and insoluble iron forms. In order to explore this result further, transcriptomic studies were performed. Eight genes corresponding to multiheme c-type cytochromes were upregulated when F. placidus was grown with insoluble Fe(III) oxide compared to soluble Fe(III) citrate as an electron acceptor. Numerous archaella (archaeal flagella) also were observed on Fe(III)-grown cells, and genes coding for two type IV pilin-like domain proteins were differentially expressed in Fe(III) oxidegrown cells. This study provides insight into the mechanisms for dissimilatory Fe(III) respiration by hyperthermophilic archaea.

A Membrane-Bound Cytochrome EnablesMethanosarcina acetivoransto Conserve Energy to Support Growth from Extracellular Electron Transfer

“…The putative function of outer-surface cytochromes is terminal electron transfer to extracellular electron acceptors, similar to the role that outer surface c -type cytochromes play in extracellular electron transfer in Gram-negative bacteria such as Shewanella and Geobacter species (20–22). Similar c -type cytochrome electrical contacts have been proposed for Fe(III)-reducing Archaea such as Ferroglobus and Geoglobus species (23, 24). However, the study of the mechanisms for extracellular electron transfer in these archaea has been stymied by the lack of microorganisms available in pure culture that can grow via extracellular electron transfer and are genetically tractable.…”

“…A wide diversity of archaea are capable of extracellular electron transfer (72), but the mechanisms are poorly understood. For archaea such as Ferroglobus placidus (23), Geoglobus ahangari (24), and diverse ANME (13–19) it has been proposed that outer-membrane cytochromes are the terminal reductase. The rapid non-physiological reduction of extracellular electron acceptors by a range of redox-active proteins and co-factors in vitro necessitates genetically tractable model organisms for physiologically relevant functional studies.…”

A Metagenomics-Based Metabolic Model of Nitrate-Dependent Anaerobic Oxidation of Methane by Methanoperedens-Like Archaea

“…An exception to this formed MPEBLZ_02042 which had many homologs in the bacterial and archaeal domain albeit with only moderate sequence identity (= 37%). Homologs that were found for many of the other proteins comprised proteins from the Fe(III) reducing Euryarchaeota Ferroglobus placidus and Geoglobus acetivorans (Mardanov et al, 2015 ; Smith et al, 2015 ). The sequence identity was generally low and spanned only part of the protein (Table 2 ).…”

Cytochromes c in Archaea: distribution, maturation, cell architecture, and the special case of Ignicoccus hospitalis

“…The results suggest that these proteins might form extracellular conductive structures or pili as in Shewanella or Geobacter . Here, periplasmic, outer-membrane, or pilus-bound Cytc transfer electrons to and from the cells (reviewed for example in Gorby et al, 2006 ; Richter et al, 2012 ; Boesen and Nielsen, 2013 ; Smith et al, 2015 ). This might provide a structural and biochemical basis of the metal ion-reducing and the presumed electron-conductive capabilities of the iron-metabolizing Archaea.…”

“…In a recent study, many heme-stained bands were found SDS gels of extracts of Fe 3+ -grown F. placidus cells. The number of bands and of transcripts of Cytc genes differed depending on the solution state of the iron: there were more Cytc proteins and corresponding transcripts in cells grown on solid compared to soluble Fe 3+ species; in addition there were numerous type IV pili suggesting close attachment of the cells to the substrate and/or electrically conductive pili (Smith et al, 2015 ). By analogy, the sulfate reducer Archaeoglobus veneficus with a total of 16 Cytc genes should also be able to grow by metal respiration (Figure 2 ).…”