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Characterization of simultaneous uptake of xylose and glucose in Caldicellulosiruptor kronotskyensis for optimal hydrogen production

Vongkampang, Thitiwut LU ; Sreenivas, Krishnan LU ; Engvall, Jonathan ; Grey, Carl LU and van Niel, Ed W. J. LU (2021) In Biotechnology for Biofuels 14.
Abstract
Background: Caldicellulosiruptor kronotskyensis has gained interest for its ability to grow on various lignocellulosic biomass. The aim of this study was to investigate the growth profles of C. kronotskyensis in the presence of mixtures
of glucose–xylose. Recently, we characterized a diauxic-like pattern for C. saccharolyticus on lignocellulosic sugar mixtures. In this study, we aimed to investigate further whether C. kronotskyensis has adapted to uptake glucose in the disaccharide form (cellobiose) rather than the monosaccharide (glucose).

Results: Interestingly, growth of C. kronotskyensis on glucose and xylose mixtures did not display diauxic-like growth patterns. Closer... (More)
Background: Caldicellulosiruptor kronotskyensis has gained interest for its ability to grow on various lignocellulosic biomass. The aim of this study was to investigate the growth profles of C. kronotskyensis in the presence of mixtures
of glucose–xylose. Recently, we characterized a diauxic-like pattern for C. saccharolyticus on lignocellulosic sugar mixtures. In this study, we aimed to investigate further whether C. kronotskyensis has adapted to uptake glucose in the disaccharide form (cellobiose) rather than the monosaccharide (glucose).

Results: Interestingly, growth of C. kronotskyensis on glucose and xylose mixtures did not display diauxic-like growth patterns. Closer investigation revealed that, in contrast to C. saccharolyticus, C. kronotskyensis does not possess a second uptake system for glucose. Both C. saccharolyticus and C. kronotskyensis share the characteristics of preferring xylose over glucose. Growth on xylose was twice as fast (μmax=0.57 h−1) as on glucose (μmax=0.28 h−1). A study of the sugar uptake was made with diferent glucose–xylose ratios to fnd a kinetic relationship between the two sugars for transport into the cell. High concentrations of glucose inhibited xylose uptake and vice versa. The inhibition constants were estimated to be KI,glu=0.01 cmol L−1 and KI,xyl=0.001 cmol L−1, hence glucose uptake was more severely
inhibited by xylose uptake. Bioinformatics analysis could not exclude that C. kronotskyensis possesses more than one transporter for glucose. As a next step it was investigated whether glucose uptake by C. kronotskyensis improved in
the form of cellobiose. Indeed, cellobiose is taken up faster than glucose; nevertheless, the growth rate on each sugar remained similar.

Conclusions: C. kronotskyensis possesses a xylose transporter that might take up glucose at an inferior rate even in the absence of xylose. Alternatively, glucose can be taken up in the form of cellobiose, but growth performance is still inferior to growth on xylose. Therefore, we propose that the catabolism of C. kronotskyensis has adapted more strongly to pentose rather than hexose, thereby having obtained a specifc survival edge in thermophilic lignocellulosic degradation communities. (Less)
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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Caldicellulosiruptor kronotskyensis, non-diauxic, xylose uptake, glucose uptake, cellobiose uptake
in
Biotechnology for Biofuels
volume
14
article number
91
pages
11 pages
publisher
BioMed Central (BMC)
external identifiers
  • scopus:85104067173
  • pmid:33832529
ISSN
1754-6834
DOI
10.1186/s13068-021-01938-6
language
English
LU publication?
yes
id
e7a65ec8-1b8c-4636-8165-7e46e0e2be2a
date added to LUP
2021-04-14 10:48:28
date last changed
2022-04-27 01:30:49
@article{e7a65ec8-1b8c-4636-8165-7e46e0e2be2a,
  abstract     = {{<b>Background</b>: <i>Caldicellulosiruptor kronotskyensis</i> has gained interest for its ability to grow on various lignocellulosic biomass. The aim of this study was to investigate the growth profles of <i>C. kronotskyensis</i> in the presence of mixtures <br/>of glucose–xylose. Recently, we characterized a diauxic-like pattern for <i>C. saccharolyticus</i> on lignocellulosic sugar mixtures. In this study, we aimed to investigate further whether <i>C. kronotskyensis</i> has adapted to uptake glucose in the disaccharide form (cellobiose) rather than the monosaccharide (glucose).<br/><br/><b>Results</b>: Interestingly, growth of <i>C. kronotskyensis</i> on glucose and xylose mixtures did not display diauxic-like growth patterns. Closer investigation revealed that, in contrast to <i>C. saccharolyticus</i>, <i>C. kronotskyensis</i> does not possess a second uptake system for glucose. Both <i>C. saccharolyticus</i> and <i>C. kronotskyensis</i> share the characteristics of preferring xylose over glucose. Growth on xylose was twice as fast (<i>μ</i><sub>max</sub>=0.57 h<sup>−1</sup>) as on glucose (<i>μ</i><sub>max</sub>=0.28 h<sup>−1</sup>). A study of the sugar uptake was made with diferent glucose–xylose ratios to fnd a kinetic relationship between the two sugars for transport into the cell. High concentrations of glucose inhibited xylose uptake and vice versa. The inhibition constants were estimated to be <i>K</i><sub>I,glu</sub>=0.01 cmol L<sup>−1</sup> and K<sub>I,xyl</sub>=0.001 cmol L<sup>−1</sup>, hence glucose uptake was more severely <br/>inhibited by xylose uptake. Bioinformatics analysis could not exclude that <i>C. kronotskyensis</i> possesses more than one transporter for glucose. As a next step it was investigated whether glucose uptake by <i>C. kronotskyensis</i> improved in <br/>the form of cellobiose. Indeed, cellobiose is taken up faster than glucose; nevertheless, the growth rate on each sugar remained similar.<br/><br/><b>Conclusions</b>: <i>C. kronotskyensis</i> possesses a xylose transporter that might take up glucose at an inferior rate even in the absence of xylose. Alternatively, glucose can be taken up in the form of cellobiose, but growth performance is still inferior to growth on xylose. Therefore, we propose that the catabolism of <i>C. kronotskyensis</i> has adapted more strongly to pentose rather than hexose, thereby having obtained a specifc survival edge in thermophilic lignocellulosic degradation communities.}},
  author       = {{Vongkampang, Thitiwut and Sreenivas, Krishnan and Engvall, Jonathan and Grey, Carl and van Niel, Ed W. J.}},
  issn         = {{1754-6834}},
  keywords     = {{Caldicellulosiruptor kronotskyensis; non-diauxic; xylose uptake; glucose uptake; cellobiose uptake}},
  language     = {{eng}},
  month        = {{04}},
  publisher    = {{BioMed Central (BMC)}},
  series       = {{Biotechnology for Biofuels}},
  title        = {{Characterization of simultaneous uptake of xylose and glucose in <i>Caldicellulosiruptor kronotskyensis</i> for optimal hydrogen production}},
  url          = {{http://dx.doi.org/10.1186/s13068-021-01938-6}},
  doi          = {{10.1186/s13068-021-01938-6}},
  volume       = {{14}},
  year         = {{2021}},
}