Unraveling Fe(II)-Oxidizing Mechanisms in a Facultative Fe(II) Oxidizer, Sideroxydans lithotrophicus Strain ES-1, via Culturing, Transcriptomics, and Reverse Transcription-Quantitative PCR

Zhou, Nanqing; Keffer, Jessica L.; Polson, Shawn W.; Chan, Clara S.

doi:10.1128/aem.01595-21

Cited by 25 publications

(44 citation statements)

References 71 publications

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“…It is proposed that the unusual features of this protein, including the bis-His coordination of the heme and the fact that the heme is more exposed to the solvent when compared with other monoheme cytochromes, allows it to be sensitive to changes in the local environment, which enables it to function as an electron donor for cytochrome bc 1 , cytochrome bb 3 and CymA ES-1 [105]. Recently, a cultured-based study associated with transcriptomics assays also demonstrated that the cytochrome Cyc2 participates in the Fe(II) oxidation process [106]. Cyc2 is predicted to be a transmembrane beta barrel protein with an N-terminal cytochrome-like region [107].…”

Section: Extracellular Electron Transfer Processes Of Sideroxydans Li...mentioning

confidence: 99%

“…S. lithotrophicus ES-1 contains three cyc2 genes that are adjacent to one another in the genome, and that are more expressed than mtoA in Fe(II)-citrate cultures. Besides cyc2 genes, there are other putative Fe(II) oxidation related genes that were overexpressed, including two periplasmic monoheme cytochromes and a gene cluster composed by five proteins, although their function remains to be elucidated [106].…”

Section: Extracellular Electron Transfer Processes Of Sideroxydans Li...mentioning

confidence: 99%

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Molecular Mechanisms of Microbial Extracellular Electron Transfer: The Importance of Multiheme Cytochromes

Paquete¹,

Morgado²,

Salgueiro³

et al. 2022

Front. Biosci. (Landmark Ed)

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Extracellular electron transfer is a key metabolic process of many organisms that enables them to exchange electrons with extracellular electron donors/acceptors. The discovery of organisms with these abilities and the understanding of their electron transfer processes has become a priority for the scientific and industrial community, given the growing interest on the use of these organisms in sustainable biotechnological processes. For example, in bioelectrochemical systems electrochemical active organisms can exchange electrons with an electrode, allowing the production of energy and added-value compounds, among other processes. In these systems, electrochemical active organisms exchange electrons with an electrode through direct or indirect mechanisms, using, in most cases, multiheme cytochromes. In numerous electroactive organisms, these proteins form a conductive pathway that allows electrons produced from cellular metabolism to be transferred across the cell surface for the reduction of an electrode, or vice-versa. Here, the mechanisms by which the most promising electroactive bacteria perform extracellular electron transfer will be reviewed, emphasizing the proteins involved in these pathways. The ability of some of the organisms to perform bidirectional electron transfer and the pathways used will also be highlighted.

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Section: Extracellular Electron Transfer Processes Of Sideroxydans Li...mentioning

confidence: 99%

Section: Extracellular Electron Transfer Processes Of Sideroxydans Li...mentioning

confidence: 99%

Molecular Mechanisms of Microbial Extracellular Electron Transfer: The Importance of Multiheme Cytochromes

Paquete¹,

Morgado²,

Salgueiro³

et al. 2022

Front. Biosci. (Landmark Ed)

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“…The presence of multiple EET pathways, and modularity of certain components may provide growth/survival advantages to S. lithotrophicus ES-1 under dynamic redox conditions, analogous to how Geobacter sulfurreducens has evolved distinct EET pathways based on redox potential and utilizing different soluble and insoluble sources and/or sinks of electrons in the environment [4,23]. Recent work quantifying expression of genes encoding candidate iron oxidation pathway genes from S. lithotrophicus found that paralogues of cyc2, encoding a protein recently shown to exhibit Fe(II) oxidation activity from M. ferrooxydans [24], were expressed highly mtoA under iron-and non-iron oxidizing conditions [25]. These results suggest that Cyc2, and not Mto, is the major pathway for Fe(II) oxidation in S. lithotrophicus under the conditions tested [25] and that more work should be done to investigate the role of Mto in EET.…”

Section: Inner Membrane and Periplasmic Components Of The Mto And Sli...mentioning

confidence: 99%

“…Recent work quantifying expression of genes encoding candidate iron oxidation pathway genes from S. lithotrophicus found that paralogues of cyc2, encoding a protein recently shown to exhibit Fe(II) oxidation activity from M. ferrooxydans [24], were expressed highly mtoA under iron-and non-iron oxidizing conditions [25]. These results suggest that Cyc2, and not Mto, is the major pathway for Fe(II) oxidation in S. lithotrophicus under the conditions tested [25] and that more work should be done to investigate the role of Mto in EET. In conclusion, we established the electron transfer functionality, interactions and modularity of novel EET components from an Fe(II) oxidizing bacterium that is dependent on EET for its primary metabolism.…”

Section: Inner Membrane and Periplasmic Components Of The Mto And Sli...mentioning

confidence: 99%

Reconstructing electron transfer components from an Fe(II) oxidizing bacterium

2022

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Neutrophilic Fe(II) oxidizing bacteria play an important role in biogeochemical processes and have also received attention for multiple technological applications. These micro-organisms are thought to couple their metabolism with extracellular electron transfer (EET) while oxidizing Fe(II) as electron donor outside the cell. Sideroxydans lithotrophicus ES-1 is a freshwater chemolithoautotrophic Fe(II) oxidizing bacterium that is challenging to culture and not yet genetically tractable. Analysis of the S. lithotrophicus ES-1 genome predicts multiple EET pathways, which are proposed to be involved in Fe(II) oxidation, but not yet validated. Here we expressed components of two of the proposed EET pathways, including the Mto and Slit_0867–0870 PCC3 pathways, from S. lithotrophicus ES-1 into Aeromonas hydrophila , an established model EET organism. We demonstrate that combinations of putative inner membrane and periplasmic components from the Mto and Slit_0867–0870 PCC3 pathways partially complemented EET activity in Aeromonas mutants lacking native components. Our results provide evidence for electron transfer functionality and interactions of inner membrane and periplasmic components from the Mto and Slit_0867–0870 PCC3 pathways. Based on these findings, we suggest that EET in S. lithotrophicus ES-1 could be more complicated than previously considered and raises questions regarding directionality of these electron transfer pathways.

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“…Furthermore, this activation correlates with Mn(II) oxidation and MOB-449 biofilm development, suggesting that Mn(II) oxidation is used to gain energy and survive under adverse environmental conditions. Previous studies in iron-oxidizing Zetaproteobacteria and other neutrophilic Fe-oxidizers have shown that the membrane c-type cytochrome Cyc2 and cytochrome c terminal oxidases are highly expressed in Fe(II)-rich environments and their expression is also stimulated by Fe(II) addition to bacterial cultures (Jewell et al, 2016;McAllister et al, 2020;Zhou et al, 2022). These results, in agreement with our results in MOB-449, suggest a transcriptional regulation mediated by Fe(II) and Mn(II) to allow the electrons derived from their oxidation reactions to be passed through cytochrome c terminal oxidases to reduce oxygen and acquire energy for growth (Jewell et al, 2016;McAllister et al, 2020;Zhou et al, 2022).…”

Section: Accession Descriptionmentioning

confidence: 99%

Manganese oxidation counteracts the deleterious effect of low temperatures on biofilm formation in Pseudomonas sp. MOB-449

Casalini

Piazza

Masotti

et al. 2022

Front. Mol. Biosci.

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Mn removal from groundwater by biological sand filter technology is negatively impacted by low temperatures in winter periods. Therefore, the need to study Mn(II)-oxidizing bacteria (MOB) having the potential to oxidize Mn(II) and form biofilms at low temperatures is imperative. These MOB can have potential as inocula for sand filter bioaugmentation strategies to optimize Mn removal during winter periods. We previously showed that a Pseudomonas sp. MOB-449 (MOB-449), isolated from a Mn biofilter, oxidizes Mn(II) in a biofilm-dependent way at low temperatures. In this work, MOB-449 Mn(II) oxidation and growth capacities were evaluated under planktonic and biofilm conditions at different temperatures. At 18°C, MOB-449 showed enhanced biofilm formation due to the addition of Mn(II) to the medium correlating with Mn(II) oxidation, compared to biofilms grown in control medium. Moreover, this enhancement on biofilm formation due to the addition of Mn(II) was only observed at 18°C. At this temperature, Mn(II) oxidation in membrane fractions collected from biofilms was induced by uncoupling oxidative phosphorylation from the electron transport chain with 2,4-Dinitrophenol. In Pseudomonas, a role for c-type cytochrome in Mn(II) oxidation has been demonstrated. Accordingly, transcriptional profiles of all terminal oxidases genes found in MOB-449 showed an induction of cytochrome c terminal oxidases expression mediated by Mn(II) oxidation at 18°C. Finally, heme peroxidase activity assays and MS analysis revealed that PetC, a cytochrome c5, and also CcmE, involved in the cytochrome c biogenesis machinery, are induced at 18°C only in the presence of Mn(II). These results present evidence supporting that cytochromes c and also the cytochrome c terminal oxidases are activated at low temperatures in the presence of Mn(II). Overall, this work demonstrate that in MOB-449 Mn(II) oxidation is activated at low temperatures to gain energy, suggesting that this process is important for survival under adverse environmental conditions and contributing to the understanding of the physiological role of bacterial Mn(II) oxidation.

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Unraveling Fe(II)-Oxidizing Mechanisms in a Facultative Fe(II) Oxidizer, Sideroxydans lithotrophicus Strain ES-1, via Culturing, Transcriptomics, and Reverse Transcription-Quantitative PCR

Cited by 25 publications

References 71 publications

Molecular Mechanisms of Microbial Extracellular Electron Transfer: The Importance of Multiheme Cytochromes

Molecular Mechanisms of Microbial Extracellular Electron Transfer: The Importance of Multiheme Cytochromes

Reconstructing electron transfer components from an Fe(II) oxidizing bacterium

Manganese oxidation counteracts the deleterious effect of low temperatures on biofilm formation in Pseudomonas sp. MOB-449

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