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Assessment of metabolic flux distribution in the thermophilic hydrogen producer Caloramator celer as affected by external pH and hydrogen partial pressure

Ciranna, Alessandro; Pawar, Sudhanshu LU ; Santala, Ville; Karp, Matti and van Niel, Ed LU (2014) In Microbial Cell Factories 13(48). p.16-48
Abstract
Background: Caloramator celer is a strict anaerobic, alkalitolerant, thermophilic bacterium capable of converting

glucose to hydrogen (H2), carbon dioxide, acetate, ethanol and formate by a mixed acid fermentation. Depending

on the growth conditions C. celer can produce H2 at high yields. For a biotechnological exploitation of this

bacterium for H2 production it is crucial to understand the factors that regulate carbon and electron fluxes and

therefore the final distribution of metabolites to channel the metabolic flux towards the desired product.

Results: Combining experimental results from batch fermentations with genome analysis, reconstruction of central

carbon metabolism and... (More)
Background: Caloramator celer is a strict anaerobic, alkalitolerant, thermophilic bacterium capable of converting

glucose to hydrogen (H2), carbon dioxide, acetate, ethanol and formate by a mixed acid fermentation. Depending

on the growth conditions C. celer can produce H2 at high yields. For a biotechnological exploitation of this

bacterium for H2 production it is crucial to understand the factors that regulate carbon and electron fluxes and

therefore the final distribution of metabolites to channel the metabolic flux towards the desired product.

Results: Combining experimental results from batch fermentations with genome analysis, reconstruction of central

carbon metabolism and metabolic flux analysis (MFA), this study shed light on glucose catabolism of the

thermophilic alkalitolerant bacterium C. celer. Two innate factors pertaining to culture conditions have been

identified to significantly affect the metabolic flux distribution: culture pH and partial pressures of H2 (PH2). Overall,

at alkaline to neutral pH the rate of biomass synthesis was maximized, whereas at acidic pH the lower growth rate

and the less efficient biomass formation are accompanied with more efficient energy recovery from the substrate

indicating high cell maintenance possibly to sustain intracellular pH homeostasis. Higher H2 yields were associated

with fermentation at acidic pH as a consequence of the lower synthesis of other reduced by-products such as

formate and ethanol. In contrast, PH2 did not affect the growth of C. celer on glucose. At high PH2 the cellular redox

state was balanced by rerouting the flow of carbon and electrons to ethanol and formate production allowing

unaltered glycolytic flux and growth rate, but resulting in a decreased H2 synthesis.

Conclusion: C. celer possesses a flexible fermentative metabolism that allows redistribution of fluxes at key

metabolic nodes to simultaneously control redox state and efficiently harvest energy from substrate even under

unfavorable conditions (i.e. low pH and high PH2). With the H2 production in mind, acidic pH and low PH2 should

be preferred for a high yield-oriented process, while a high productivity-oriented process can be achieved at

alkaline pH and high PH2. (Less)
Please use this url to cite or link to this publication:
author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Caloramator, Biohydrogen production, Metabolic flux analysis, Redox state, Hydrogen tolerance, Fermentation, Pyruvate node, Metabolic shift, Ethanol, Formate
in
Microbial Cell Factories
volume
13
issue
48
pages
16 - 48
publisher
BioMed Central
external identifiers
  • wos:000334717700001
  • scopus:84897413447
ISSN
1475-2859
DOI
10.1186/1475-2859-13-48
language
English
LU publication?
yes
id
3b7cd4fa-ea13-4c7a-8c10-487827a69e70 (old id 4389118)
date added to LUP
2014-04-28 11:10:53
date last changed
2017-07-30 03:55:25
@article{3b7cd4fa-ea13-4c7a-8c10-487827a69e70,
  abstract     = {Background: Caloramator celer is a strict anaerobic, alkalitolerant, thermophilic bacterium capable of converting<br/><br>
glucose to hydrogen (H2), carbon dioxide, acetate, ethanol and formate by a mixed acid fermentation. Depending<br/><br>
on the growth conditions C. celer can produce H2 at high yields. For a biotechnological exploitation of this<br/><br>
bacterium for H2 production it is crucial to understand the factors that regulate carbon and electron fluxes and<br/><br>
therefore the final distribution of metabolites to channel the metabolic flux towards the desired product.<br/><br>
Results: Combining experimental results from batch fermentations with genome analysis, reconstruction of central<br/><br>
carbon metabolism and metabolic flux analysis (MFA), this study shed light on glucose catabolism of the<br/><br>
thermophilic alkalitolerant bacterium C. celer. Two innate factors pertaining to culture conditions have been<br/><br>
identified to significantly affect the metabolic flux distribution: culture pH and partial pressures of H2 (PH2). Overall,<br/><br>
at alkaline to neutral pH the rate of biomass synthesis was maximized, whereas at acidic pH the lower growth rate<br/><br>
and the less efficient biomass formation are accompanied with more efficient energy recovery from the substrate<br/><br>
indicating high cell maintenance possibly to sustain intracellular pH homeostasis. Higher H2 yields were associated<br/><br>
with fermentation at acidic pH as a consequence of the lower synthesis of other reduced by-products such as<br/><br>
formate and ethanol. In contrast, PH2 did not affect the growth of C. celer on glucose. At high PH2 the cellular redox<br/><br>
state was balanced by rerouting the flow of carbon and electrons to ethanol and formate production allowing<br/><br>
unaltered glycolytic flux and growth rate, but resulting in a decreased H2 synthesis.<br/><br>
Conclusion: C. celer possesses a flexible fermentative metabolism that allows redistribution of fluxes at key<br/><br>
metabolic nodes to simultaneously control redox state and efficiently harvest energy from substrate even under<br/><br>
unfavorable conditions (i.e. low pH and high PH2). With the H2 production in mind, acidic pH and low PH2 should<br/><br>
be preferred for a high yield-oriented process, while a high productivity-oriented process can be achieved at<br/><br>
alkaline pH and high PH2.},
  author       = {Ciranna, Alessandro and Pawar, Sudhanshu and Santala, Ville and Karp, Matti and van Niel, Ed},
  issn         = {1475-2859},
  keyword      = {Caloramator,Biohydrogen production,Metabolic flux analysis,Redox state,Hydrogen tolerance,Fermentation,Pyruvate node,Metabolic shift,Ethanol,Formate},
  language     = {eng},
  number       = {48},
  pages        = {16--48},
  publisher    = {BioMed Central},
  series       = {Microbial Cell Factories},
  title        = {Assessment of metabolic flux distribution in the thermophilic hydrogen producer Caloramator celer as affected by external pH and hydrogen partial pressure},
  url          = {http://dx.doi.org/10.1186/1475-2859-13-48},
  volume       = {13},
  year         = {2014},
}