Metabolite-based mutualism between Pseudomonas aeruginosa PA14 and Enterobacter aerogenes enhances current generation in bioelectrochemical systems

Venkataraman, Arvind; Perkins, Sarah D.; Werner, Jeffrey J.; Angenent, Largus T.

doi:10.1039/c1ee01377g

Cited by 112 publications

(112 citation statements)

References 68 publications

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“…Oxygen concentrations influence the production of these antimicrobials by P. aeruginosa through quorum sensing (Schuster and Greenberg, 2008), and therefore we maintained two oxygen tensions: (i) microaerobic by passive oxygen diffusion and (ii) aerobic by vigorously shaken cultures. Similar to our earlier observation (Venkataraman et al, 2011), the PYO concentrations in P. aeruginosa cultures were considerably higher with 2,3-butanediol compared with glucose for both microaerobic and aerobic conditions (Figure 1e). The outcome was more nuanced for pyoverdine, which had lower concentrations with 2,3-butanediol for microaerobic conditions, but higher concentrations for aerobic conditions compared with glucose ( Figure 1f).…”

Section: Resultssupporting

confidence: 78%

“…However, a mechanistic understanding was absent. We found in a bioreactor study with a co-culture of Enterobacter aerogenes and P. aeruginosa that phenazine production was greatly enhanced compared with a pure culture of P. aeruginosa with selective production toward PYO rather than the other phenazines (Venkataraman et al, 2011). Our study also showed a positive microbe-microbe interaction through phenazines, which had not been studied in detail before.…”

Section: Introductionsupporting

confidence: 50%

“…Microaerobic, pure culture studies of S. aureus and S. marcescens showed that cell-free supernatant from a P. aeruginosa PA14 culture grown with 2,3-butanediol was considerably more inhibitory to these fermenters than supernatant from P. aeruginosa grown on glucose (Figure 2a). However, there was no significant inhibition of E. aerogenes and K. pneumoniae and it is known that, for example, E. aerogenes can co-exist with P. aeruginosa (Venkataraman et al, 2011), whereas S. aureus showed growth retardation (Pal'chykovs'ka et al, 2008).…”

Section: Resultsmentioning

confidence: 99%

“…The advantage for P. aeruginosa is to maintain redox homeostasis, and thus to survive, under anaerobic conditions within the deeper layers of the biofilm when PYO is present (Dietrich et al, 2013). This extracellular electron transfer with oxygen over a distance can be measured quantitatively and in real time by electric current production through the oxidation of reduced PYO at an electrode as the solid-state electron acceptor in a bioelectrochemical system (Rabaey et al, 2005;Venkataraman et al, 2011). In our earlier work with bioelectrochemical systems under microaerobic conditions (Venkataraman et al, 2011), we observed that the electric current doubled for P. aeruginosa with 2,3-butanediol vs glucose due to an increase in total phenazine concentration and a shift to its production of mainly PYO.…”

Section: Resultsmentioning

confidence: 99%

“…This extracellular electron transfer with oxygen over a distance can be measured quantitatively and in real time by electric current production through the oxidation of reduced PYO at an electrode as the solid-state electron acceptor in a bioelectrochemical system (Rabaey et al, 2005;Venkataraman et al, 2011). In our earlier work with bioelectrochemical systems under microaerobic conditions (Venkataraman et al, 2011), we observed that the electric current doubled for P. aeruginosa with 2,3-butanediol vs glucose due to an increase in total phenazine concentration and a shift to its production of mainly PYO. In addition, in the presence of oxidized PYO, E. aerogenes (the producer of 2,3-butanediol with glucose as a substrate) respired at least partially with the electrode, resulting in enhancement of its growth.…”

Section: Resultsmentioning

confidence: 99%

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Metabolite transfer with the fermentation product 2,3-butanediol enhances virulence by Pseudomonas aeruginosa

et al. 2014

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The respiratory tract of cystic fibrosis (CF) patients harbor persistent microbial communities (CF airway microbiome) with Pseudomonas aeruginosa emerging as a dominant pathogen. Within a polymicrobial infection, interactions between co-habitant microbes can be important for pathogenesis, but even when considered, these interactions are not well understood. Here, we show with in vitro experiments that, compared with glucose, common fermentation products from co-habitant bacteria significantly increase virulence factor production, antimicrobial activity and biofilm formation of P. aeruginosa. The maximum stimulating effect was produced with the fermentation product 2,3-butanediol, which is a substrate for P. aeruginosa, resulting in a metabolic relationship between fermenters and this pathogen. The global transcription regulator LasI LasR, which controls quorum sensing, was upregulated threefold with 2,3-butanediol, resulting in higher phenazine and exotoxin concentrations and improved biofilm formation. This indicates that the success of P. aeruginosa in CF airway microbiomes could be governed by the location within the food web with fermenting bacteria. Our findings suggest that interbacterial metabolite transfer in polymicrobial infections stimulates virulence of P. aeruginosa and could have a considerable impact on disease progression.

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Section: Resultssupporting

confidence: 78%

Section: Introductionsupporting

confidence: 50%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Metabolite transfer with the fermentation product 2,3-butanediol enhances virulence by Pseudomonas aeruginosa

et al. 2014

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Enhanced Microbial Process in the Sustainable Fuel Production

Hakalehto

2015

Handbook of Clean Energy Systems

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Various biomass sources, such as wood and other plant materials, animal wastes, food and other industry wastes, household wastes, sludge varieties, marine biomass, peat and other carbon‐rich organic reservoirs, offer raw materials for continuous recycling in sustainable bioindustries. The corresponding circulation of matter also maintains the balance in the ecosystems and is powered mainly by the solar energy. A substantial portion of this energy is stored in different forms of biomasses and is liberated by the microbes in “the economy of the nature.” In order to achieve the goals of sustainable development, human agriculture, industries, and other activities should fit into this framework set by the microbial degradation and the reuse of molecules. Those principles are adaptable into the production of energy and chemicals. Microbes constitute ecosystems of their own, for example, in the intestinal milieu, or in lake sediments. Everywhere, the microbial communities interact with their surroundings. The types of molecular communication in the microscopic level determine the functioning of larger scale ecosystems and also the bioprocesses. In both natural and industrial settings, the ecological principles are alike. Microbes circulate the elements and convert chemical energy into novel formations. If the microbial population is dense and versatile, different species often develop symbiotic forms of action. Biotechnical processes consist of several steps. In order to achieve optimal biorefining results from a particular process, all these steps require careful consideration. Various biomasses could be combined with each other in order to obtain optimal starting material and conditions in the process. Physicochemical characteristics (dry weight, consistence, pH , etc.) need to be adjusted according to the process needs. Initial steps of sample preparation include homogenization, hydrolysis, and other pretreatments. In most biotechnical procedures, operation temperature plays a significant role. Controlling it becomes more challenging as the biomass volumes increase. Biorefineries could resemble “activity fields” where different substances flow and are then converted further into meaningful direction, adding value into the production process. Biomass exploitation could be based on the vast potential of biocatalysis in designing processes with positive net energy balance. In microbial fermentations, carbon dioxide is one main product of the biochemical pathways. However, alternative routes for the production of some biochemicals, such as 2,3‐butanediol, with diminished carbon dioxide generation and more substantial recycling of carbon have been found using a testing system for enhanced microbial culturing, the portable microbe enrichment unit ( PMEU ). For example, in the conversion of food industry wastes, levels of 8–10 g/L/h of 2,3‐butanediol have been observed. Also, enhanced productions of organic acids, ethanol and butanol, as well as methane and hydrogen, have been achieved by this method. The bioconversion approach opens up novel views on producing fuels from waste materials with lower investment costs. Besides the aerobiosis, the microaerobic and anaerobic (low oxygen containing) processes and their enhancement offer alternatives from the point of microbial metabolism. As a bioreactor system is usually based on the conversion of biomass raw materials, the success of the entire process is dependent on the careful management of these conversions. Organic macromolecules are degraded to smaller molecules by physical, chemical, and biochemical hydrolyzation. They act as a starting point for microbiological metabolic pathways. Speeding up the process often builds up a gradient where joint effects of metabolic regulation and diffusion limitation, as well as overcoming them, play an essential role in the product formation. Microbial strains and their enzymes act as biocatalysts, which can also be circulated in the process or immobilized. Surfaces between different phases create conditions where the accelerated gradient formation improves overall performances of a bioreactor. Besides optimized upstream processes, successful production of organic substances by microbes for energy and chemicals requires an integrated downstream processing system. Different aspects for bioprocess design are presented here with respect to increased production efficiency and improved overall sustainability in biofuel production.

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Development of Bacteria‐Based Cellular Computing Circuits for Sensing and Control in Biological Systems

TerAvest

Angenent

2012

Biomolecular Information Processing

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Metabolite-based mutualism between Pseudomonas aeruginosa PA14 and Enterobacter aerogenes enhances current generation in bioelectrochemical systems

Cited by 112 publications

References 68 publications

Metabolite transfer with the fermentation product 2,3-butanediol enhances virulence by Pseudomonas aeruginosa

Metabolite transfer with the fermentation product 2,3-butanediol enhances virulence by Pseudomonas aeruginosa

Enhanced Microbial Process in the Sustainable Fuel Production

Development of Bacteria‐Based Cellular Computing Circuits for Sensing and Control in Biological Systems

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