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Microbial metabolic networks in a complex electrogenic biofilm recovered from a stimulus-induced metatranscriptomics approach.

Ishii S, Suzuki S, Tenney A, Norden-Krichmar TM, Nealson KH, Bretschger O - Sci Rep (2015)

Bottom Line: Potential metabolic switches between eleven dominant members were mainly observed for acetate, hydrogen, and ethanol metabolisms.These results have enabled the estimation of a multi-species metabolic network and the associated short-term responses to EET stimuli that induce changes to metabolic flow and cooperative or competitive microbial interactions.This systematic meta-omics approach represents a next step towards understanding complex microbial roles within a community and how community members respond to specific environmental stimuli.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA 92037, USA.

ABSTRACT
Microorganisms almost always exist as mixed communities in nature. While the significance of microbial community activities is well appreciated, a thorough understanding about how microbial communities respond to environmental perturbations has not yet been achieved. Here we have used a combination of metagenomic, genome binning, and stimulus-induced metatranscriptomic approaches to estimate the metabolic network and stimuli-induced metabolic switches existing in a complex microbial biofilm that was producing electrical current via extracellular electron transfer (EET) to a solid electrode surface. Two stimuli were employed: to increase EET and to stop EET. An analysis of cell activity marker genes after stimuli exposure revealed that only two strains within eleven binned genomes had strong transcriptional responses to increased EET rates, with one responding positively and the other responding negatively. Potential metabolic switches between eleven dominant members were mainly observed for acetate, hydrogen, and ethanol metabolisms. These results have enabled the estimation of a multi-species metabolic network and the associated short-term responses to EET stimuli that induce changes to metabolic flow and cooperative or competitive microbial interactions. This systematic meta-omics approach represents a next step towards understanding complex microbial roles within a community and how community members respond to specific environmental stimuli.

No MeSH data available.


Related in: MedlinePlus

Overall gene expression levels and dynamics related to microbial metabolisms for each Bin-genome.Gene expression levels and changes were calculated (see Supplementary Data 2) for selected metabolism-related marker gene families associated to respiration (A) substrate consumption or byproduct production (B) and glycolysis and TCA cycle (C). Normalized gene expression levels (mRNA-RPKM/DNA-RPKM) for each Bin-genome under the three operational conditions is described by the size of circle, while gene expression dynamics (mRNA-RPKM/mRNA-RPKM) is described by the circle color of SP (expression fold-change from MFC to SP) and the circle color of OC (expression fold-change from SP to OC). Important gene sets for the metabolic pathway analyses within the community are indicated by yellow rectangles highlighting the circles. Bars indicate partial pathways of a given KEGG module or no existence of the KEGG orthology/module, and the elements of the incompleteness are described below the bar. Red rectangles indicate potential metabolism switches after stimuli addition.
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f4: Overall gene expression levels and dynamics related to microbial metabolisms for each Bin-genome.Gene expression levels and changes were calculated (see Supplementary Data 2) for selected metabolism-related marker gene families associated to respiration (A) substrate consumption or byproduct production (B) and glycolysis and TCA cycle (C). Normalized gene expression levels (mRNA-RPKM/DNA-RPKM) for each Bin-genome under the three operational conditions is described by the size of circle, while gene expression dynamics (mRNA-RPKM/mRNA-RPKM) is described by the circle color of SP (expression fold-change from MFC to SP) and the circle color of OC (expression fold-change from SP to OC). Important gene sets for the metabolic pathway analyses within the community are indicated by yellow rectangles highlighting the circles. Bars indicate partial pathways of a given KEGG module or no existence of the KEGG orthology/module, and the elements of the incompleteness are described below the bar. Red rectangles indicate potential metabolism switches after stimuli addition.

Mentions: Next, we analyzed the specific metabolic activities of each strain. Since a majority of metabolic interactions among microbes are related to fermentation and/or electron transfer reactions24, we analyzed the expression profiles of gene families associated with KEGG pathways or KEGG modules29 that are known to relate to these metabolic activities (Supplementary Data 2). From the list, we depicted gene expression trends of appropriate gene family modules for describing respiration pathways (Fig. 4A) ubiquitously occurring in the earth environments30, substrate consumption or byproduct production (Fig. 4B) which are well-known intermediate compounds within anaerobic metabolic networks31, and glycolysis and the TCA cycle (Fig. 4C) from highly expressed KEGG modules (Supplementary Data 3). Several marker genes were selected based on known key enzymes of the specific pathway (e.g. citrate synthase, gltA in TCA cycle) or highly expressed genes within the Bin-genomes (Supplementary Data 4) that correlated to a specific metabolic function (e.g. alcohol dehydrogenase, yiaY and cation/acetate symporter, actP).


Microbial metabolic networks in a complex electrogenic biofilm recovered from a stimulus-induced metatranscriptomics approach.

Ishii S, Suzuki S, Tenney A, Norden-Krichmar TM, Nealson KH, Bretschger O - Sci Rep (2015)

Overall gene expression levels and dynamics related to microbial metabolisms for each Bin-genome.Gene expression levels and changes were calculated (see Supplementary Data 2) for selected metabolism-related marker gene families associated to respiration (A) substrate consumption or byproduct production (B) and glycolysis and TCA cycle (C). Normalized gene expression levels (mRNA-RPKM/DNA-RPKM) for each Bin-genome under the three operational conditions is described by the size of circle, while gene expression dynamics (mRNA-RPKM/mRNA-RPKM) is described by the circle color of SP (expression fold-change from MFC to SP) and the circle color of OC (expression fold-change from SP to OC). Important gene sets for the metabolic pathway analyses within the community are indicated by yellow rectangles highlighting the circles. Bars indicate partial pathways of a given KEGG module or no existence of the KEGG orthology/module, and the elements of the incompleteness are described below the bar. Red rectangles indicate potential metabolism switches after stimuli addition.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4595844&req=5

f4: Overall gene expression levels and dynamics related to microbial metabolisms for each Bin-genome.Gene expression levels and changes were calculated (see Supplementary Data 2) for selected metabolism-related marker gene families associated to respiration (A) substrate consumption or byproduct production (B) and glycolysis and TCA cycle (C). Normalized gene expression levels (mRNA-RPKM/DNA-RPKM) for each Bin-genome under the three operational conditions is described by the size of circle, while gene expression dynamics (mRNA-RPKM/mRNA-RPKM) is described by the circle color of SP (expression fold-change from MFC to SP) and the circle color of OC (expression fold-change from SP to OC). Important gene sets for the metabolic pathway analyses within the community are indicated by yellow rectangles highlighting the circles. Bars indicate partial pathways of a given KEGG module or no existence of the KEGG orthology/module, and the elements of the incompleteness are described below the bar. Red rectangles indicate potential metabolism switches after stimuli addition.
Mentions: Next, we analyzed the specific metabolic activities of each strain. Since a majority of metabolic interactions among microbes are related to fermentation and/or electron transfer reactions24, we analyzed the expression profiles of gene families associated with KEGG pathways or KEGG modules29 that are known to relate to these metabolic activities (Supplementary Data 2). From the list, we depicted gene expression trends of appropriate gene family modules for describing respiration pathways (Fig. 4A) ubiquitously occurring in the earth environments30, substrate consumption or byproduct production (Fig. 4B) which are well-known intermediate compounds within anaerobic metabolic networks31, and glycolysis and the TCA cycle (Fig. 4C) from highly expressed KEGG modules (Supplementary Data 3). Several marker genes were selected based on known key enzymes of the specific pathway (e.g. citrate synthase, gltA in TCA cycle) or highly expressed genes within the Bin-genomes (Supplementary Data 4) that correlated to a specific metabolic function (e.g. alcohol dehydrogenase, yiaY and cation/acetate symporter, actP).

Bottom Line: Potential metabolic switches between eleven dominant members were mainly observed for acetate, hydrogen, and ethanol metabolisms.These results have enabled the estimation of a multi-species metabolic network and the associated short-term responses to EET stimuli that induce changes to metabolic flow and cooperative or competitive microbial interactions.This systematic meta-omics approach represents a next step towards understanding complex microbial roles within a community and how community members respond to specific environmental stimuli.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA 92037, USA.

ABSTRACT
Microorganisms almost always exist as mixed communities in nature. While the significance of microbial community activities is well appreciated, a thorough understanding about how microbial communities respond to environmental perturbations has not yet been achieved. Here we have used a combination of metagenomic, genome binning, and stimulus-induced metatranscriptomic approaches to estimate the metabolic network and stimuli-induced metabolic switches existing in a complex microbial biofilm that was producing electrical current via extracellular electron transfer (EET) to a solid electrode surface. Two stimuli were employed: to increase EET and to stop EET. An analysis of cell activity marker genes after stimuli exposure revealed that only two strains within eleven binned genomes had strong transcriptional responses to increased EET rates, with one responding positively and the other responding negatively. Potential metabolic switches between eleven dominant members were mainly observed for acetate, hydrogen, and ethanol metabolisms. These results have enabled the estimation of a multi-species metabolic network and the associated short-term responses to EET stimuli that induce changes to metabolic flow and cooperative or competitive microbial interactions. This systematic meta-omics approach represents a next step towards understanding complex microbial roles within a community and how community members respond to specific environmental stimuli.

No MeSH data available.


Related in: MedlinePlus