Microbial iron management mechanisms in extremely acidic environments: comparative genomics evidence for diversity and versatility

Osório, Héctor S.; Martínez, Verónica; Nieto, Pamela A.; Holmes, David S.; Quatrini, Raquel

doi:10.1186/1471-2180-8-203

Cited by 56 publications

(61 citation statements)

References 82 publications

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“…The TonB system imports ferric iron into the cytoplasm as siderophore-chelated Fe 3? (Osorio et al 2008) and is controlled by the Fur protein at the transcriptional level. Its lower abundance negatively correlated with a higher abundance of Fur under anaerobic conditions.…”

Section: Kinetics Of Ferric Iron Anaerobic Reduction By Elemental Sulmentioning

confidence: 99%

Kinetics of anaerobic elemental sulfur oxidation by ferric iron in Acidithiobacillus ferrooxidans and protein identification by comparative 2-DE-MS/MS

Kučera

Bouchal

Cerná

et al. 2011

Antonie van Leeuwenhoek

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Elemental sulfur oxidation by ferric iron in Acidithiobacillus ferrooxidans was investigated. The apparent Michaelis constant for ferric iron was 18.6 mM. An absence of anaerobic ferric iron reduction ability was observed in bacteria maintained on elemental sulfur for an extended period of time. Upon transition from ferrous iron to elemental sulfur medium, the cells exhibited similar kinetic characteristics of ferric iron reduction under anaerobic conditions to those of cells that were originally maintained on ferrous iron. Nevertheless, a total loss of anaerobic ferric iron reduction ability after the sixth passage in elemental sulfur medium was demonstrated. The first proteomic screening of total cell lysates of anaerobically incubated bacteria resulted in the detection of 1599 protein spots in the master two-dimensional electrophoresis gel. A set of 59 more abundant and 49 less abundant protein spots that changed their protein abundances in an anaerobiosis-dependent manner was identified and compared to iron- and sulfur-grown cells, respectively. Proteomic analysis detected a significant increase in abundance under anoxic conditions of electron transporters, such as rusticyanin and cytochrome c(552), involved in the ferrous iron oxidation pathway. Therefore we suggest the incorporation of rus-operon encoded proteins in the anaerobic respiration pathway. Two sulfur metabolism proteins were identified, pyridine nucleotide-disulfide oxidoreductase and sulfide-quinone reductase. The important transcription regulator, ferric uptake regulation protein, was anaerobically more abundant. The anaerobic expression of several proteins involved in cell envelope formation indicated a gradual adaptation to elemental sulfur oxidation.

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Section: Kinetics Of Ferric Iron Anaerobic Reduction By Elemental Sulmentioning

confidence: 99%

Kinetics of anaerobic elemental sulfur oxidation by ferric iron in Acidithiobacillus ferrooxidans and protein identification by comparative 2-DE-MS/MS

Kučera

Bouchal

Cerná

et al. 2011

Antonie van Leeuwenhoek

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“…ferrooxidans fixes carbon dioxide for cellular carbon and couples ferrous iron, inorganic sulfur compound, and hydrogen oxidation to the reduction of either molecular oxygen or ferric iron. The type strain genome sequence is available (Valdes et al, 2008) and the genetic basis of many aspects of its metabolism has been elucidated (Osorio et al, 2008, 2013; Quatrini et al, 2009; Esparza et al, 2010; Ponce et al, 2012). Acidihalobacter prosperus (originally described as “ Thiobacillus prosperus ”) is another autotrophic and acidophilic species capable of growth via oxidation of ferrous iron and inorganic sulfur compounds (Huber and Stetter, 1989; Cardenas et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Multiple Osmotic Stress Responses in Acidihalobacter prosperus Result in Tolerance to Chloride Ions

et al. 2017

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Extremely acidophilic microorganisms (pH optima for growth of ≤3) are utilized for the extraction of metals from sulfide minerals in the industrial biotechnology of “biomining.” A long term goal for biomining has been development of microbial consortia able to withstand increased chloride concentrations for use in regions where freshwater is scarce. However, when challenged by elevated salt, acidophiles experience both osmotic stress and an acidification of the cytoplasm due to a collapse of the inside positive membrane potential, leading to an influx of protons. In this study, we tested the ability of the halotolerant acidophile Acidihalobacter prosperus to grow and catalyze sulfide mineral dissolution in elevated concentrations of salt and identified chloride tolerance mechanisms in Ac. prosperus as well as the chloride susceptible species, Acidithiobacillus ferrooxidans. Ac. prosperus had optimum iron oxidation at 20 g L−1 NaCl while At. ferrooxidans iron oxidation was inhibited in the presence of 6 g L−1 NaCl. The tolerance to chloride in Ac. prosperus was consistent with electron microscopy, determination of cell viability, and bioleaching capability. The Ac. prosperus proteomic response to elevated chloride concentrations included the production of osmotic stress regulators that potentially induced production of the compatible solute, ectoine uptake protein, and increased iron oxidation resulting in heightened electron flow to drive proton export by the F0F1 ATPase. In contrast, At. ferrooxidans responded to low levels of Cl− with a generalized stress response, decreased iron oxidation, and an increase in central carbon metabolism. One potential adaptation to high chloride in the Ac. prosperus Rus protein involved in ferrous iron oxidation was an increase in the negativity of the surface potential of Rus Form I (and Form II) that could help explain how it can be active under elevated chloride concentrations. These data have been used to create a model of chloride tolerance in the salt tolerant and susceptible species Ac. prosperus and At. ferrooxidans, respectively.

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“…Alternatively, this enzyme could also be located at the outer membrane (depicted in light grey). Based on our results, the Fe(III) reducing enzyme of SJH does not accept any quinones as electron acceptor, as it does in the case of neutrophiles microorganisms (Osorio et al 2008). This suggests that Fe(III) reduction in acidophiles could occur in the periplasm or even in the cytoplasm.…”

Section: Implications For Mechanisms Of Electron Transfer To Fe(iii) mentioning

confidence: 77%

Absence of humic substance reduction by the acidophilic Fe(III)-reducing strain Acidiphilium SJH: implications for its Fe(III) reduction mechanism and for the stimulation of natural organohalogen formation

Emmerich

Kappler

2011

Biogeochemistry

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A vast amount of volatile organohalogens (VOX) has natural origins. Both soils and sediments have been shown to release VOX, which are most likely produced via redox reactions between Fe(III) and quinones in the presence of halide anions, particularly at acidic pH. We tested whether acidophilic Fe(III)-reducers might indirectly stimulate natural VOX formation at acidic pH by providing reactive Fe and quinone species. However, it is unknown whether acidophilic Fe(III)-reducers can reduce humic acids (HA) or fulvic acids (FA). We therefore tested the ability of the acidophilic Fe(III)-reducer Acidiphilium SJH to reduce macromolecular, suspended HA and dissolved FA at pH 3.1-3.3. We found that (i) SJH can neither reduce HA/FA nor the humic model quinone anthraquinone-2,6-disulfonicacid (AQDS) nor stimulate the formation of FA radicals, (ii) at acidic pH, significantly more electrons are transferred abiotically both from native and reduced FA to dissolved Fe(III) than from native or reduced HA, and (iii) the presence of strain SJH does not stimulate VOX formation. Our results imply that the acidophilic Fe(III)-reducer SJH either uses an enzyme for Fe(III) reduction that can neither be used for HA/FA nor for AQDS reduction or that the location of Fe(III) reduction is inaccessible for these compounds. We further conclude that microorganisms such as strain SJH probably do not indirectly stimulate natural VOX formation at acidic pH via the formation of reactive quinone species.

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Microbial iron management mechanisms in extremely acidic environments: comparative genomics evidence for diversity and versatility

Cited by 56 publications

References 82 publications

Kinetics of anaerobic elemental sulfur oxidation by ferric iron in Acidithiobacillus ferrooxidans and protein identification by comparative 2-DE-MS/MS

Kinetics of anaerobic elemental sulfur oxidation by ferric iron in Acidithiobacillus ferrooxidans and protein identification by comparative 2-DE-MS/MS

Multiple Osmotic Stress Responses in Acidihalobacter prosperus Result in Tolerance to Chloride Ions

Absence of humic substance reduction by the acidophilic Fe(III)-reducing strain Acidiphilium SJH: implications for its Fe(III) reduction mechanism and for the stimulation of natural organohalogen formation

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