Genome-scale comparison and constraint-based metabolic reconstruction of the facultative anaerobic Fe(III)-reducer Rhodoferax ferrireducens

Abstract

BackgroundRhodoferax ferrireducens is a metabolically versatile, Fe(III)-reducing, subsurface microorganism that is likely to play an important role in the carbon and metal cycles in the subsurface. It also has the unique ability to convert sugars to electricity, oxidizing the sugars to carbon dioxide with quantitative electron transfer to graphite electrodes in microbial fuel cells. In order to expand our limited knowledge about R. ferrireducens, the complete genome sequence of this organism was further annotated and then the physiology of R. ferrireducens was investigated with a constraint-based, genome-scale in silico metabolic model and laboratory studies.ResultsThe iterative modeling and experimental approach unveiled exciting, previously unknown physiological features, including an expanded range of substrates that support growth, such as cellobiose and citrate, and provided additional insights into important features such as the stoichiometry of the electron transport chain and the ability to grow via fumarate dismutation. Further analysis explained why R. ferrireducens is unable to grow via photosynthesis or fermentation of sugars like other members of this genus and uncovered novel genes for benzoate metabolism. The genome also revealed that R. ferrireducens is well-adapted for growth in the subsurface because it appears to be capable of dealing with a number of environmental insults, including heavy metals, aromatic compounds, nutrient limitation and oxidative stress.ConclusionThis study demonstrates that combining genome-scale modeling with the annotation of a new genome sequence can guide experimental studies and accelerate the understanding of the physiology of under-studied yet environmentally relevant microorganisms.

Insights into the Structure and Metabolic Function of Microbes That Shape Pelagic Iron-Rich Aggregates (“Iron Snow”)

“…We detected mostly chaperonin GroEL and nucleic acid/protein synthesis-related proteins in iron snow samples. Interestingly, retrieved flagellin-like proteins (Rfer_0630 and Rfer_0631) indicated motility, which agrees with previous findings (62,63). Malate dehydrogenase (Rfer_1803), a carbon metabolism protein involved in the citric acid cycle, was also detected.…”

“…It has a pH optimum of 7.0 (62); therefore, it was not surprising to find much higher abundances of the Albidiferax genus in the northern basin than in the central basin using cloning and qPCR approaches. Although some of these members are capable of autotrophic growth, A. ferrireducens has only an incomplete pathway associated with CO 2 fixation in its genome (63). We detected mostly chaperonin GroEL and nucleic acid/protein synthesis-related proteins in iron snow samples.…”

“…Although Albidiferax ferrireducens and Geobacter are neutrophilic FeRM, their relatives were detected as the two most abundant groups in the northern basin, suggesting their tolerance of slightly acidic conditions. A. ferrireducens is a metabolically versatile microorganism that likely plays an important role in subsurface carbon and metal cycles (62,63). It has a pH optimum of 7.0 (62); therefore, it was not surprising to find much higher abundances of the Albidiferax genus in the northern basin than in the central basin using cloning and qPCR approaches.…”

Genome-scale analysis of anaerobic benzoate and phenol metabolism in the hyperthermophilic archaeon Ferroglobus placidus

“…However, F. placidus is a strict anaerobe (Hafenbradl et al, 1996), and no genes for aerobic metabolism of benzoate via hydroxylation or the BOX pathway (Zaar et al, 2001;Gescher et al, 2002;Risso et al, 2009) were apparent in the genome. Multiple anaerobic BCLs have also been detected in other organisms.…”

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

“…On the other hand, Ferroglobus and Geoglobus, both hyperthermophilic archaea that are known to effectively couple the complete oxidation of organic compounds with Fe(III) reduction (20,21), contain numerous multiheme c-type cytochromes. More than half of these multiheme c-type cytochromes have homologues in Fe(III)-reducing bacteria from the genera Geobacter, Shewanella (48), Rhodoferax (66), and Thermincola (67), organisms that also are efficient at electron transfer from the oxidation of organic compounds to Fe(III). Many of the multiheme cytochromes found in Ferroglobus, Geoglobus, and Fe(III)-reducing bacteria are class III, which means that they have heme groups with reduction potentials that can vary significantly (68).…”