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A Clostridium group IV species dominates and suppresses a mixed culture fermentation by tolerance to medium chain fatty acids products

Stephen Andersen UGent, Vicky De Groof, Way Cern Khor, Hugo Roume, Ruben Props UGent, Marta Coma and Korneel Rabaey UGent (2017) FRONTIERS IN BIOENGINEERING AND BIOTECHNOLOGY. 5.
abstract
A microbial community is engaged in a complex economy of cooperation and competition for carbon and energy. In engineered systems such as anaerobic digestion and fermentation, these relationships are exploited for conversion of a broad range of substrates into products, such as biogas, ethanol, and carboxylic acids. Medium chain fatty acids (MCFAs), for example, hexanoic acid, are valuable, energy dense microbial fermentation products, however, MCFA tend to exhibit microbial toxicity to a broad range of microorganisms at low concentrations. Here, we operated continuous mixed population MCFA fermentations on biorefinery thin stillage to investigate the community response associated with the production and toxicity of MCFA. In this study, an uncultured species from the Clostridium group IV (related to Clostridium sp. BS-1) became enriched in two independent reactors that produced hexanoic acid (up to 8.1 g L−1), octanoic acid (up to 3.2 g L−1), and trace concentrations of decanoic acid. Decanoic acid is reported here for the first time as a possible product of a Clostridium group IV species. Other significant species in the community, Lactobacillus spp. and Acetobacterium sp., generate intermediates in MCFA production, and their collapse in relative abundance resulted in an overall production decrease. A strong correlation was present between the community composition and both the hexanoic acid concentration (p = 0.026) and total volatile fatty acid concentration (p = 0.003). MCFA suppressed species related to Clostridium sp. CPB-6 and Lactobacillus spp. to a greater extent than others. The proportion of the species related to Clostridium sp. BS-1 over Clostridium sp. CPB-6 had a strong correlation with the concentration of octanoic acid (p = 0.003). The dominance of this species and the increase in MCFA resulted in an overall toxic effect on the mixed community, most significantly on the Lactobacillus spp., which resulted in a decrease in total hexanoic acid concentration to 32 ± 2% below the steady-state average. As opposed to the current view of MCFA toxicity broadly leading to production collapse, this study demonstrates that varied tolerance to MCFA within the community can lead to the dominance of some species and the suppression of others, which can result in a decreased productivity of the fermentation.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
journal title
FRONTIERS IN BIOENGINEERING AND BIOTECHNOLOGY
Front. Bioeng. Biotechnol.
volume
5
article number
8
pages
10 pages
ISSN
2296-4185
DOI
10.3389/fbioe.2017.00008
language
English
UGent publication?
yes
classification
A2
copyright statement
I have retained and own the full copyright for this publication
id
8508357
handle
http://hdl.handle.net/1854/LU-8508357
date created
2017-02-08 15:42:30
date last changed
2017-09-08 09:14:59
@article{8508357,
  abstract     = {A microbial community is engaged in a complex economy of cooperation and competition for carbon and energy. In engineered systems such as anaerobic digestion and fermentation, these relationships are exploited for conversion of a broad range of substrates into products, such as biogas, ethanol, and carboxylic acids. Medium chain fatty acids (MCFAs), for example, hexanoic acid, are valuable, energy dense microbial fermentation products, however, MCFA tend to exhibit microbial toxicity to a broad range of microorganisms at low concentrations. Here, we operated continuous mixed population MCFA fermentations on biorefinery thin stillage to investigate the community response associated with the production and toxicity of MCFA. In this study, an uncultured species from the Clostridium group IV (related to Clostridium sp. BS-1) became enriched in two independent reactors that produced hexanoic acid (up to 8.1 g L\ensuremath{-}1), octanoic acid (up to 3.2 g L\ensuremath{-}1), and trace concentrations of decanoic acid. Decanoic acid is reported here for the first time as a possible product of a Clostridium group IV species. Other significant species in the community, Lactobacillus spp. and Acetobacterium sp., generate intermediates in MCFA production, and their collapse in relative abundance resulted in an overall production decrease. A strong correlation was present between the community composition and both the hexanoic acid concentration (p = 0.026) and total volatile fatty acid concentration (p = 0.003). MCFA suppressed species related to Clostridium sp. CPB-6 and Lactobacillus spp. to a greater extent than others. The proportion of the species related to Clostridium sp. BS-1 over Clostridium sp. CPB-6 had a strong correlation with the concentration of octanoic acid (p = 0.003). The dominance of this species and the increase in MCFA resulted in an overall toxic effect on the mixed community, most significantly on the Lactobacillus spp., which resulted in a decrease in total hexanoic acid concentration to 32 {\textpm} 2\% below the steady-state average. As opposed to the current view of MCFA toxicity broadly leading to production collapse, this study demonstrates that varied tolerance to MCFA within the community can lead to the dominance of some species and the suppression of others, which can result in a decreased productivity of the fermentation.},
  articleno    = {8},
  author       = {Andersen, Stephen and De Groof, Vicky and Khor, Way Cern and Roume, Hugo and Props, Ruben and Coma, Marta and Rabaey, Korneel},
  issn         = {2296-4185},
  journal      = {FRONTIERS IN BIOENGINEERING AND BIOTECHNOLOGY},
  language     = {eng},
  pages        = {10},
  title        = {A Clostridium group IV species dominates and suppresses a mixed culture fermentation by tolerance to medium chain fatty acids products},
  url          = {http://dx.doi.org/10.3389/fbioe.2017.00008},
  volume       = {5},
  year         = {2017},
}

Chicago
Andersen, Stephen, Vicky De Groof, Way Cern Khor, Hugo Roume, Ruben Props, Marta Coma, and Korneel Rabaey. 2017. “A Clostridium Group IV Species Dominates and Suppresses a Mixed Culture Fermentation by Tolerance to Medium Chain Fatty Acids Products.” Frontiers in Bioengineering and Biotechnology 5.
APA
Andersen, S., De Groof, V., Khor, W. C., Roume, H., Props, R., Coma, M., & Rabaey, K. (2017). A Clostridium group IV species dominates and suppresses a mixed culture fermentation by tolerance to medium chain fatty acids products. FRONTIERS IN BIOENGINEERING AND BIOTECHNOLOGY, 5.
Vancouver
1.
Andersen S, De Groof V, Khor WC, Roume H, Props R, Coma M, et al. A Clostridium group IV species dominates and suppresses a mixed culture fermentation by tolerance to medium chain fatty acids products. FRONTIERS IN BIOENGINEERING AND BIOTECHNOLOGY. 2017;5.
MLA
Andersen, Stephen, Vicky De Groof, Way Cern Khor, et al. “A Clostridium Group IV Species Dominates and Suppresses a Mixed Culture Fermentation by Tolerance to Medium Chain Fatty Acids Products.” FRONTIERS IN BIOENGINEERING AND BIOTECHNOLOGY 5 (2017): n. pag. Print.