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Title: Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times

Abstract

Background: Anaerobic fermentation of lignocellulose occurs in both natural and managed environments, and is an essential part of the carbon cycle as well as a promising route to sustainable production of fuels and chemicals. Lignocellulose solubilization by mixed microbiomes is important in these contexts.Results: Here in this paper, we report the development of stable switchgrass-fermenting enrichment cultures maintained at various residence times and moderately high (55 °C) temperatures. Anaerobic microbiomes derived from a digester inoculum were incubated at 55 °C and fed semi-continuously with medium containing 30 g/L mid-season harvested switchgrass to achieve residence times (RT) of 20, 10, 5, and 3.3 days. Stable, time-invariant cellulolytic methanogenic cultures with minimal accumulation of organic acids were achieved for all RTs. Fractional carbohydrate solubilization was 0.711, 0.654, 0.581 and 0.538 at RT = 20, 10, 5 and 3.3 days, respectively, and glucan solubilization was proportional to xylan solubilization at all RTs. The rate of solubilization was described well by the equation r = k(C-C 0f r), where C represents the concentration of unutilized carbohydrate, C 0 is the concentration of carbohydrate (cellulose and hemicellulose) entering the bioreactor and f r is the extrapolated fraction of entering carbohydrate that is recalcitrant at infinitemore » residence time. The 3.3 day RT is among the shortest RT reported for stable thermophilic, methanogenic digestion of a lignocellulosic feedstock. 16S rDNA phylotyping and metagenomic analyses were conducted to characterize the effect of RT on community dynamics and to infer functional roles in the switchgrass to biogas conversion to the various microbial taxa. Firmicutes were the dominant phylum, increasing in relative abundance from 54 to 96% as RT decreased. A Clostridium clariflavum strain with genetic markers for xylose metabolism was the most abundant lignocellulose-solubilizing bacterium. A Thermotogae (Defluviitoga tunisiensis) was the most abundant bacterium in switchgrass digesters at RT = 20 days but decreased in abundance at lower RTs as did multiple Chloroflexi. Synergistetes and Euryarchaeota were present at roughly constant levels over the range of RTs examined.Conclusions: A system was developed in which stable methanogenic steady-states were readily obtained with a particulate biomass feedstock, mid-season switchgrass, at laboratory (1 L) scale. Characterization of the extent and rate of carbohydrate solubilization in combination with 16S rDNA and metagenomic sequencing provides a multi-dimensional view of performance, species composition, glycoside hydrolases, and metabolic function with varying residence time. These results provide a point of reference and guidance for future studies and organism development efforts involving defined cultures.« less

Authors:
ORCiD logo; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1618731
Alternate Identifier(s):
OSTI ID: 1471931
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Name: Biotechnology for Biofuels Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
Springer Science + Business Media
Country of Publication:
Netherlands
Language:
English
Subject:
09 BIOMASS FUELS; Lignocellulose; Anaerobic; Methanogenic; Thermophilic; Solubilization; Microbial communities; Metagenomics; Clostridium clariflavum

Citation Formats

Liang, Xiaoyu, Whitham, Jason M., Holwerda, Evert K., Shao, Xiongjun, Tian, Liang, Wu, Yu-Wei, Lombard, Vincent, Henrissat, Bernard, Klingeman, Dawn M., Yang, Zamin K., Podar, Mircea, Richard, Tom L., Elkins, James G., Brown, Steven D., and Lynd, Lee R. Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times. Netherlands: N. p., 2018. Web. doi:10.1186/s13068-018-1238-1.
Liang, Xiaoyu, Whitham, Jason M., Holwerda, Evert K., Shao, Xiongjun, Tian, Liang, Wu, Yu-Wei, Lombard, Vincent, Henrissat, Bernard, Klingeman, Dawn M., Yang, Zamin K., Podar, Mircea, Richard, Tom L., Elkins, James G., Brown, Steven D., & Lynd, Lee R. Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times. Netherlands. doi:10.1186/s13068-018-1238-1.
Liang, Xiaoyu, Whitham, Jason M., Holwerda, Evert K., Shao, Xiongjun, Tian, Liang, Wu, Yu-Wei, Lombard, Vincent, Henrissat, Bernard, Klingeman, Dawn M., Yang, Zamin K., Podar, Mircea, Richard, Tom L., Elkins, James G., Brown, Steven D., and Lynd, Lee R. Thu . "Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times". Netherlands. doi:10.1186/s13068-018-1238-1.
@article{osti_1618731,
title = {Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times},
author = {Liang, Xiaoyu and Whitham, Jason M. and Holwerda, Evert K. and Shao, Xiongjun and Tian, Liang and Wu, Yu-Wei and Lombard, Vincent and Henrissat, Bernard and Klingeman, Dawn M. and Yang, Zamin K. and Podar, Mircea and Richard, Tom L. and Elkins, James G. and Brown, Steven D. and Lynd, Lee R.},
abstractNote = {Background: Anaerobic fermentation of lignocellulose occurs in both natural and managed environments, and is an essential part of the carbon cycle as well as a promising route to sustainable production of fuels and chemicals. Lignocellulose solubilization by mixed microbiomes is important in these contexts.Results: Here in this paper, we report the development of stable switchgrass-fermenting enrichment cultures maintained at various residence times and moderately high (55 °C) temperatures. Anaerobic microbiomes derived from a digester inoculum were incubated at 55 °C and fed semi-continuously with medium containing 30 g/L mid-season harvested switchgrass to achieve residence times (RT) of 20, 10, 5, and 3.3 days. Stable, time-invariant cellulolytic methanogenic cultures with minimal accumulation of organic acids were achieved for all RTs. Fractional carbohydrate solubilization was 0.711, 0.654, 0.581 and 0.538 at RT = 20, 10, 5 and 3.3 days, respectively, and glucan solubilization was proportional to xylan solubilization at all RTs. The rate of solubilization was described well by the equation r = k(C-C0fr), where C represents the concentration of unutilized carbohydrate, C0 is the concentration of carbohydrate (cellulose and hemicellulose) entering the bioreactor and fr is the extrapolated fraction of entering carbohydrate that is recalcitrant at infinite residence time. The 3.3 day RT is among the shortest RT reported for stable thermophilic, methanogenic digestion of a lignocellulosic feedstock. 16S rDNA phylotyping and metagenomic analyses were conducted to characterize the effect of RT on community dynamics and to infer functional roles in the switchgrass to biogas conversion to the various microbial taxa. Firmicutes were the dominant phylum, increasing in relative abundance from 54 to 96% as RT decreased. A Clostridium clariflavum strain with genetic markers for xylose metabolism was the most abundant lignocellulose-solubilizing bacterium. A Thermotogae (Defluviitoga tunisiensis) was the most abundant bacterium in switchgrass digesters at RT = 20 days but decreased in abundance at lower RTs as did multiple Chloroflexi. Synergistetes and Euryarchaeota were present at roughly constant levels over the range of RTs examined.Conclusions: A system was developed in which stable methanogenic steady-states were readily obtained with a particulate biomass feedstock, mid-season switchgrass, at laboratory (1 L) scale. Characterization of the extent and rate of carbohydrate solubilization in combination with 16S rDNA and metagenomic sequencing provides a multi-dimensional view of performance, species composition, glycoside hydrolases, and metabolic function with varying residence time. These results provide a point of reference and guidance for future studies and organism development efforts involving defined cultures.},
doi = {10.1186/s13068-018-1238-1},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 11,
place = {Netherlands},
year = {2018},
month = {9}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1186/s13068-018-1238-1

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