A novel metatranscriptomic approach to identify gene expression dynamics during extracellular electron transfer

Ishii, Shun’ichi; Suzuki, Shino; Norden-Krichmar, Trina M.; Tenney, Aaron; Chain, Patrick; Scholz, Matthew; Nealson, Kenneth H.; Bretschger, Orianna

doi:10.1038/ncomms2615

Cited by 173 publications

(144 citation statements)

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“…Our previous metatranscriptomic analyses indicated that Desulfuromonadales (including genus Geobacter) and Desulfobulbus strains responded to surface potential changes by different gene expression levels of outer membrane c-type cytochromes. These significant changes in gene transcription were related to increases in EET rates when exposed to SP electropositive conditions (Ishii et al, 2013). These data suggest that different c-type cytochromes may define an affinity for microbial electron transfer to substrates with specific surface potentials.…”

Section: Discussionmentioning

confidence: 65%

“…Using electrochemical approaches in MFC systems, the EET activity in a microbial community can be monitored as operational current generation, anodic limiting (maximum) current density and per-biomass electrode reducing rate throughout system operations (Ishii et al, 2008). In addition, the anode potential can be controlled by potentiostatic set-potential (SP) operation (Wagner et al, 2010), which allows acceleration or suppression of EET rates in the community as a function of applied surface redox potential (Aelterman et al, 2008;Ishii et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Microbial population and functional dynamics associated with surface potential and carbon metabolism

Ishii¹,

et al. 2013

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Microbial extracellular electron transfer (EET) to solid surfaces is an important reaction for metal reduction occurring in various anoxic environments. However, it is challenging to accurately characterize EET-active microbial communities and each member's contribution to EET reactions because of changes in composition and concentrations of electron donors and solid-phase acceptors. Here, we used bioelectrochemical systems to systematically evaluate the synergistic effects of carbon source and surface redox potential on EET-active microbial community development, metabolic networks and overall electron transfer rates. The results indicate that faster biocatalytic rates were observed under electropositive electrode surface potential conditions, and under fatty acid-fed conditions. Temporal 16S rRNA-based microbial community analyses showed that Geobacter phylotypes were highly diverse and apparently dependent on surface potentials. The well-known electrogenic microbes affiliated with the Geobacter metallireducens clade were associated with lower surface potentials and less current generation, whereas Geobacter subsurface clades 1 and 2 were associated with higher surface potentials and greater current generation. An association was also observed between specific fermentative phylotypes and Geobacter phylotypes at specific surface potentials. When sugars were present, Tolumonas and Aeromonas phylotypes were preferentially associated with lower surface potentials, whereas Lactococcus phylotypes were found to be closely associated with Geobacter subsurface clades 1 and 2 phylotypes under higher surface potential conditions. Collectively, these results suggest that surface potentials provide a strong selective pressure, at the species and strain level, for both solid surface respirators and fermentative microbes throughout the EET-active community development.

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Section: Discussionmentioning

confidence: 65%

Section: Introductionmentioning

confidence: 99%

Microbial population and functional dynamics associated with surface potential and carbon metabolism

Ishii¹,

et al. 2013

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“…The KEGG orthology (KO) functional annotation has been determined for 107 marker genes that are typically found to be in single copies in more than 95% of bacterial genomes (33,34). The number of these marker genes in each Metawatt cluster was determined from the KO assignments made in the KEGG annotation of the metagenome contigs.…”

Section: Methodsmentioning

confidence: 99%

A Previously Uncharacterized, Nonphotosynthetic Member of the Chromatiaceae Is the Primary CO ₂ -Fixing Constituent in a Self-Regenerating Biocathode

Wang

Leary

Malanoski

et al. 2015

Appl Environ Microbiol

149

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Biocathode extracellular electron transfer (EET) may be exploited for biotechnology applications, including microbially mediated O 2 reduction 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 consortia in 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 O 2 , and presumably fixing CO 2 for 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 between Alpha-and Gammaproteobacteria. 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, with Marinobacter, Chromatiaceae, and Labrenzia the most represented. RubisCO and phosphoribulokinase, along with 9 other Calvin-Benson-Bassham cycle proteins, were identified from Chromatiaceae. In addition, proteins similar to those predicted for iron oxidation pathways of known iron-oxidizing bacteria were observed for Chromatiaceae. These findings represent the first description of putative EET and CO 2 fixation mechanisms for a selfregenerating, self-sustaining multispecies biocathode, providing potential targets for functional engineering, as well as new insights into biocathode EET pathways using proteomics. Bioelectrochemical systems (BES) use microorganisms as catalysts to drive complex electrochemical reactions, such as electricity generation by microbial fuel cells (MFCs) (1), wastewater treatment (2), and microbial electrosynthesis (3-6), that would not be possible without living cells. The term "biocathode" refers to a biofilm, constituted of a single organism or microbial consortium, that has formed on the cathode of a BES and consumes electrons (e Ϫ ). Cathodes hold great potential as a stable electron source to drive microbial metabolism (7); however, little is known about the underlying extracellular electron transfer (EET) pathways that could be exploited for biocathode functional engineering. Although biocathode EET has been demonstrated for a variety of microorganisms, including acetogens (5) and a methanogenic archaeon (6), studies aimed at identifying EET conduits from the electrode to cells have mostly been confined to the model organisms Geobacter (8) and Shewanella (9), due to the massive effort put forth to understand how these iron-reducing bacteria are able to catalyze EET at bioanodes (10-12). The ability of iron-...

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“…Several molecular studies revealed the role of pili and of multiheme outer-membrane c-type cytochromes in electron transfer (Butler et al, 2010, Lovley, 2012. A comparative metatranscriptomic analysis revealed eight genes with no annotated protein function to be related to electrochemical activity (Ishii et al, 2013). Both the fields of corrosion and microbial fuel cell research can benefit from these in-depth studies.…”

Section: Perspectivesmentioning

confidence: 99%

The dual role of microbes in corrosion

2014

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Corrosion is the result of a series of chemical, physical and (micro) biological processes leading to the deterioration of materials such as steel and stone. It is a world-wide problem with great societal and economic consequences. Current corrosion control strategies based on chemically produced products are under increasing pressure of stringent environmental regulations. Furthermore, they are rather inefficient. Therefore, there is an urgent need for environmentally friendly and sustainable corrosion control strategies. The mechanisms of microbially influenced corrosion and microbially influenced corrosion inhibition are not completely understood, because they cannot be linked to a single biochemical reaction or specific microbial species or groups. Corrosion is influenced by the complex processes of different microorganisms performing different electrochemical reactions and secreting proteins and metabolites that can have secondary effects. Information on the identity and role of microbial communities that are related to corrosion and corrosion inhibition in different materials and in different environments is scarce. As some microorganisms are able to both cause and inhibit corrosion, we pay particular interest to their potential role as corrosion-controlling agents. We show interesting interfaces in which scientists from different disciplines such as microbiology, engineering and art conservation can collaborate to find solutions to the problems caused by corrosion.

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A novel metatranscriptomic approach to identify gene expression dynamics during extracellular electron transfer

Cited by 173 publications

References 46 publications

Microbial population and functional dynamics associated with surface potential and carbon metabolism

Microbial population and functional dynamics associated with surface potential and carbon metabolism

A Previously Uncharacterized, Nonphotosynthetic Member of the Chromatiaceae Is the Primary CO ₂ -Fixing Constituent in a Self-Regenerating Biocathode

The dual role of microbes in corrosion

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A novel metatranscriptomic approach to identify gene expression dynamics during extracellular electron transfer

Cited by 173 publications

References 46 publications

Microbial population and functional dynamics associated with surface potential and carbon metabolism

Microbial population and functional dynamics associated with surface potential and carbon metabolism

A Previously Uncharacterized, Nonphotosynthetic Member of the Chromatiaceae Is the Primary CO 2 -Fixing Constituent in a Self-Regenerating Biocathode

The dual role of microbes in corrosion

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Product

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A Previously Uncharacterized, Nonphotosynthetic Member of the Chromatiaceae Is the Primary CO ₂ -Fixing Constituent in a Self-Regenerating Biocathode