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Anoxic metabolism and biochemical production in Pseudomonas putida F1 driven by a bioelectrochemical system

Bin Lai, Shiqin Yu, Paul V Bernhardt, Korneel Rabaey UGent, Bernardino Virdis and Jens O Krömer (2016) BIOTECHNOLOGY FOR BIOFUELS. 9.
abstract
Background: Pseudomonas putida is a promising host for the bioproduction of chemicals, but its industrial applications are significantly limited by its obligate aerobic character. The aim of this paper is to empower the anoxic metabolism of wild-type Pseudomonas putida to enable bioproduction anaerobically, with the redox power from a bioelectrochemical system (BES). Results: The obligate aerobe Pseudomonas putida F1 was able to survive and produce almost exclusively 2-Ketogluconate from glucose under anoxic conditions due to redox balancing with electron mediators in a BES. 2-Keto-gluconate, a precursor for industrial anti-oxidant production, was produced at an overall carbon yield of over 90 % based on glucose. Seven different mediator compounds were tested, and only those with redox potential above 0.207 V (vs standard hydrogen electrode) showed interaction with the cells. The productivity increased with the increasing redox potential of the mediator, indicating this was a key factor affecting the anoxic production process. P. putida cells survived under anaerobic conditions, and limited biofilm formation could be observed on the anode's surface. Analysis of the intracellular pools of ATP, ADP and AMP showed that cells had an increased adenylate energy charge suggesting that cells were able to generate energy using the anode as terminal electron acceptor. The analysis of NAD(H) and NADP(H) showed that in the presence of specific extracellular electron acceptors, the NADP(H) pool was more oxidised, while the NAD(H) pool was unchanged. This implies a growth limitation under anaerobic conditions due to a shortage of NADPH and provides a way to limit biomass formation, while allowing cell maintenance and catalysis at high purity and yield. Conclusions: For the first time, this study proved the principle that a BES-driven bioconversion of glucose can be achieved for a wild-type obligate aerobe. This non-growth bioconversion was in high yields, high purity and also could deliver the necessary metabolic energy for cell maintenance. By combining this approach with metabolic engineering strategies, this could prove to be a powerful new way to produce bio-chemicals and fuels from renewables in both high yield and high purity.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
SOLVENT-TOLERANT PSEUDOMONAS, GRAPHITE ELECTRODE, ADENINE-NUCLEOTIDES, EXTRACELLULAR ELECTRON-TRANSFER, Bio-production, Chemical feedstocks, IN-VIVO, NEUTRAL RED, MICROBIAL FUEL-CELLS, DISSOLVED-OXYGEN, ESCHERICHIA-COLI, ENTNER-DOUDOROFF, Anoxic metabolism, Extracellular electron transfer, Pseudomonas putida F1, Bioelectrochemical system, Redox mediators
journal title
BIOTECHNOLOGY FOR BIOFUELS
Biotechnol. Biofuels
volume
9
article number
39
pages
13 pages
Web of Science type
Article
Web of Science id
000370320300001
JCR category
BIOTECHNOLOGY & APPLIED MICROBIOLOGY
JCR impact factor
5.203 (2016)
JCR rank
18/158 (2016)
JCR quartile
1 (2016)
ISSN
1754-6834
DOI
10.1186/s13068-016-0452-y
language
English
UGent publication?
yes
classification
A1
additional info
correction published in: Biotechnol. Biofuels (2017) 10, 155 ; DOI: 10.1186/s13068-017-0843-8
copyright statement
Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
id
7153121
handle
http://hdl.handle.net/1854/LU-7153121
date created
2016-03-17 11:55:06
date last changed
2018-01-17 10:28:51
@article{7153121,
  abstract     = {Background: Pseudomonas putida is a promising host for the bioproduction of chemicals, but its industrial applications are significantly limited by its obligate aerobic character. The aim of this paper is to empower the anoxic metabolism of wild-type Pseudomonas putida to enable bioproduction anaerobically, with the redox power from a bioelectrochemical system (BES). 
Results: The obligate aerobe Pseudomonas putida F1 was able to survive and produce almost exclusively 2-Ketogluconate from glucose under anoxic conditions due to redox balancing with electron mediators in a BES. 2-Keto-gluconate, a precursor for industrial anti-oxidant production, was produced at an overall carbon yield of over 90 \% based on glucose. Seven different mediator compounds were tested, and only those with redox potential above 0.207 V (vs standard hydrogen electrode) showed interaction with the cells. The productivity increased with the increasing redox potential of the mediator, indicating this was a key factor affecting the anoxic production process. P. putida cells survived under anaerobic conditions, and limited biofilm formation could be observed on the anode's surface. Analysis of the intracellular pools of ATP, ADP and AMP showed that cells had an increased adenylate energy charge suggesting that cells were able to generate energy using the anode as terminal electron acceptor. The analysis of NAD(H) and NADP(H) showed that in the presence of specific extracellular electron acceptors, the NADP(H) pool was more oxidised, while the NAD(H) pool was unchanged. This implies a growth limitation under anaerobic conditions due to a shortage of NADPH and provides a way to limit biomass formation, while allowing cell maintenance and catalysis at high purity and yield. 
Conclusions: For the first time, this study proved the principle that a BES-driven bioconversion of glucose can be achieved for a wild-type obligate aerobe. This non-growth bioconversion was in high yields, high purity and also could deliver the necessary metabolic energy for cell maintenance. By combining this approach with metabolic engineering strategies, this could prove to be a powerful new way to produce bio-chemicals and fuels from renewables in both high yield and high purity.},
  articleno    = {39},
  author       = {Lai, Bin and Yu, Shiqin and Bernhardt, Paul V and Rabaey, Korneel and Virdis, Bernardino and Kr{\"o}mer, Jens O},
  issn         = {1754-6834},
  journal      = {BIOTECHNOLOGY FOR BIOFUELS},
  keyword      = {SOLVENT-TOLERANT PSEUDOMONAS,GRAPHITE ELECTRODE,ADENINE-NUCLEOTIDES,EXTRACELLULAR ELECTRON-TRANSFER,Bio-production,Chemical feedstocks,IN-VIVO,NEUTRAL RED,MICROBIAL FUEL-CELLS,DISSOLVED-OXYGEN,ESCHERICHIA-COLI,ENTNER-DOUDOROFF,Anoxic metabolism,Extracellular electron transfer,Pseudomonas putida F1,Bioelectrochemical system,Redox mediators},
  language     = {eng},
  pages        = {13},
  title        = {Anoxic metabolism and biochemical production in Pseudomonas putida F1 driven by a bioelectrochemical system},
  url          = {http://dx.doi.org/10.1186/s13068-016-0452-y},
  volume       = {9},
  year         = {2016},
}

Chicago
Lai, Bin, Shiqin Yu, Paul V Bernhardt, Korneel Rabaey, Bernardino Virdis, and Jens O Krömer. 2016. “Anoxic Metabolism and Biochemical Production in Pseudomonas Putida F1 Driven by a Bioelectrochemical System.” Biotechnology for Biofuels 9.
APA
Lai, B., Yu, S., Bernhardt, P. V., Rabaey, K., Virdis, B., & Krömer, J. O. (2016). Anoxic metabolism and biochemical production in Pseudomonas putida F1 driven by a bioelectrochemical system. BIOTECHNOLOGY FOR BIOFUELS, 9.
Vancouver
1.
Lai B, Yu S, Bernhardt PV, Rabaey K, Virdis B, Krömer JO. Anoxic metabolism and biochemical production in Pseudomonas putida F1 driven by a bioelectrochemical system. BIOTECHNOLOGY FOR BIOFUELS. 2016;9.
MLA
Lai, Bin, Shiqin Yu, Paul V Bernhardt, et al. “Anoxic Metabolism and Biochemical Production in Pseudomonas Putida F1 Driven by a Bioelectrochemical System.” BIOTECHNOLOGY FOR BIOFUELS 9 (2016): n. pag. Print.