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

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.

doi:10.1186/s13068-018-1238-1

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

Journal Article · Thu Sep 06 00:00:00 EDT 2018 · Biotechnology for Biofuels

DOI:https://doi.org/10.1186/s13068-018-1238-1· OSTI ID:1618731

; 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.

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-C₀f_r), where C represents the concentration of unutilized carbohydrate, C₀ 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 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.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725; AC02-05CH11231

OSTI ID:: 1618731

Alternate ID(s):: OSTI ID: 1471931

Journal Information:: Biotechnology for Biofuels, Journal Name: Biotechnology for Biofuels Vol. 11 Journal Issue: 1; ISSN 1754-6834

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: Netherlands

Language:: English

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Cited by: 22 works

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Journal Article · Tue Jul 05 00:00:00 EDT 2022 · Nature Communications · OSTI ID:1618731

Chirania, Payal; Holwerda, Evert K.; Giannone, Richard J.; +6 more

Co‑cultivation of the anaerobic fungus Caecomyces churrovis with Methanobacterium bryantii enhances transcription of carbohydrate binding modules, dockerins, and pyruvate formate lyases on specific substrates

Journal Article · Fri Dec 10 00:00:00 EST 2021 · Biotechnology for Biofuels · OSTI ID:1618731

Brown, Jennifer L.; Swift, Candice L.; Mondo, Stephen J.; +13 more

Related Subjects

09 BIOMASS FUELS
Lignocellulose
Anaerobic
Methanogenic
Thermophilic
Solubilization
Microbial communities
Metagenomics
Clostridium clariflavum

MOESM10 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7056971 The current record is supplemented by this figure	figure	September 2018
MOESM10 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7056971.v1 The current record is supplemented by this figure	figure	September 2018
MOESM11 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7056986 The current record is supplemented by this figure	figure	September 2018
MOESM11 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7056986.v1 The current record is supplemented by this figure	figure	September 2018
MOESM12 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057010 The current record is supplemented by this dataset	dataset	September 2018
MOESM12 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057010.v1 The current record is supplemented by this dataset	dataset	September 2018
MOESM13 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057025 The current record is supplemented by this dataset	dataset	September 2018
MOESM13 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057025.v1 The current record is supplemented by this dataset	dataset	September 2018
MOESM1 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057046 The current record is supplemented by this figure	figure	September 2018
MOESM1 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057046.v1 The current record is supplemented by this figure	figure	September 2018
MOESM2 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057064 The current record is supplemented by this figure	figure	September 2018
MOESM2 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057064.v1 The current record is supplemented by this figure	figure	September 2018
MOESM3 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057073 The current record is supplemented by this figure	figure	September 2018
MOESM3 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057073.v1 The current record is supplemented by this figure	figure	September 2018
MOESM4 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057082 The current record is supplemented by this figure	figure	September 2018
MOESM4 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057082.v1 The current record is supplemented by this figure	figure	September 2018
MOESM5 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057094 The current record is supplemented by this figure	figure	September 2018
MOESM5 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057094.v1 The current record is supplemented by this figure	figure	September 2018
MOESM6 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057106 The current record is supplemented by this figure	figure	September 2018
MOESM6 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057106.v1 The current record is supplemented by this figure	figure	September 2018
MOESM7 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057109 The current record is supplemented by this dataset	dataset	September 2018
MOESM7 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057109.v1 The current record is supplemented by this dataset	dataset	September 2018
MOESM8 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057112 The current record is supplemented by this figure	figure	September 2018
MOESM8 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057112.v1 The current record is supplemented by this figure	figure	September 2018
MOESM9 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057115 The current record is supplemented by this figure	figure	September 2018
MOESM9 of Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.7057115.v1 The current record is supplemented by this figure	figure	September 2018
Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times [Supplemental Data] Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.c.4224131 The current record is supplemented by this collection	collection	September 2018
Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times [Supplemental Data] Whitham, Jason; Holwerda, Evert; Tian, Liang https://doi.org/10.6084/m9.figshare.c.4224131.v1 The current record is supplemented by this collection	collection	September 2018