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Potential of enriched and stabilized anaerobic lignocellulolytic fungi coexisting with bacteria and methanogens for enhanced methane production from rice straw

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Abstract

Anaerobic lignocellulosic microbial consortia are known to be prodigiously efficient at converting lignocellulosic biomass to methane. In this study, the efficacy of anaerobic fungal consortia (AFC) from five different inocula, including Bubalus bubalis rumen fluid (RU), in degrading filter paper, microcrystalline cellulose, and rice straw (RS), was screened. The AFC from RU performed best in lignocellulosic material degradation and methane production; thus, RU was selected for further experiments. Consecutive batch subculturing (CBS) was performed in RU to enrich and stabilize the dominant and key microorganisms categorized as anaerobic fungi, using the addition of antibacterial agents to suppress the growth of untargeted bacteria. After the CBS, subculture E19 proved the most efficient, with RS degradation of 84% and a methane yield of 310 mL/g VSadded, representing 1.83- and 2.25-fold increases compared to the initial seed, respectively. The microbial community of E19 consisted of anaerobic fungi (uncultured Neocallimastigales, Anaeromyces sp., Orpinomyces sp., and Feramyces sp.) coexisting with anaerobic bacteria (streptomycin resistant Proteiniphilum acetatigenes), and methanogens. The E19 consortium was able to use various carbon sources (87.5%) and contained potential genes encoding enzymes involved in RS degradation. The microbial community of E19 was highly stable, making it a promising inoculum for biomass degradation, especially for anaerobic digestion to produce biogas.

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Abbreviations

16S rRNA:

16S ribosomal RNA is the RNA component of the 30S subunit of a prokaryotic ribosome

AB:

Anaerobic bacteria

AD:

Anaerobic digestion

AF:

Anaerobic fungi

AFC:

Efficacy of anaerobic fungal consortia

ALMC:

Anaerobic lignocellulosic microbial consortium

AMT:

Acetoclastic methanogens

ANOVA:

One-way analysis of variance

AOAC:

Association of Official Agricultural Chemists

APHA:

American Public Health Association

B-ARISA:

Automated method of ribosomal intergenic spacer analysis for bacteria

BMP:

Biochemical methane potential

BUSCO:

Benchmarking Universal Single-Copy Orthologs

CAZy:

Carbohydrate-active enzymes

CBS:

Consecutive batch subculturing

CM:

Cow manure

COD:

Chemical oxygen demand

CSTR:

Continuously stirred tank reactor

E1 − E19:

Serial number of subculture during enrichment and stabilization

F-ARISA:

Automated method of ribosomal intergenic spacer analysis for fungi

FP:

Filter paper

GC:

Gas chromatography

GH:

Glycoside hydrolase

GM:

Goat manure

HMT:

Hydrogenotrophic methanogens

ISR:

The inoculum (I) to substrate (S) ratio

ITS:

Internal transcribed spacer

MCC:

Microcrystalline cellulose

MT:

Methanigens

MS:

Microbial sludge from anaerobic wastewater treatment system of a palm oil mill factory

PCR:

Polymerase chain reaction

PM:

Pig manure

qPCR:

Quantitative real-time PCR

RS:

Rice straw

RU:

Rumen fluid

SSU:

Small subunit

TS:

Total solids, defined as mass remaining after drying at 105 °C

VFAs:

Volatile fatty acids

VS:

Volatile solids, determined as weight loss from heating in air at 550 °C

°C:

Degree celsius (temperature unit)

bp:

Base pairs (nucleic acid unit)

g :

Gram (mass unit)

h :

Hour (time unit)

L :

Liter (volume unit)

m :

Meter (length unit)

μm:

Micrometer (length unit)

mL:

Milliliter (volume unit)

mg:

Milligram (mass unit)

mm:

Millimeter (length unit)

mM:

Millimolar (concentration unit)

min:

Minute (time unit)

M:

Molar (concentration unit)

s:

Second (time unit)

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Acknowledgements

The authors acknowledge Prof. Dr. Anna Schnürer for the support of barcode preparation and the 16s and ITS1 sequencing at the Department of Molecular Sciences, Swedish University of Agricultural Sciences, Sweden; the Freiburg Galaxy Team: Person X and Prof. Dr. Rolf Backofen for the website of metagenomic data analysis, Bioinformatics, University of Freiburg, Germany, funded by Collaborative Research Centre 992 Medical Epigenetics (DFG grant SFB 992/1 2012) and German Federal Ministry of Education and Research (BMBF grant 031 A538A de. NBI-RBC); the laboratory facility from Excellent Center of Waste Utilization and Management (ECoWaste) at King Mongkut’s University of Technology Thonburi, Thailand.

Funding

The authors gratefully acknowledge the financial support by the Petchra Pra Jom Klao Doctoral Scholarship from King Mongkut’s University of Technology Thonburi (KMUTT) awarded to Ms. Nitiya Thongbunrod. Research funding was supported by the Fundamental Fund (FF) of Thailand Science Research and Innovation (TSRI) and Ministry of Higher Education, Science, Research, and Innovation (MHESI).

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  1. Biotechnology Program, School of Bioresources and Technology, King Mongkut’s University of Technology Thonburi, Bangkok, 10150, Thailand

    Nitiya Thongbunrod & Pawinee Chaiprasert

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  1. Nitiya Thongbunrod
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Pawinee Chaiprasert: conceptualization, project administration, funding acquisition, resources, supervision, and writing—reviewing and editing. Nitiya Thongbunrod: methodology, data curation, formal analysis, visualization, investigation, and writing—original draft preparation.

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Correspondence to Pawinee Chaiprasert.

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Thongbunrod, N., Chaiprasert, P. Potential of enriched and stabilized anaerobic lignocellulolytic fungi coexisting with bacteria and methanogens for enhanced methane production from rice straw. Biomass Conv. Bioref. 14, 8229–8250 (2024). https://doi.org/10.1007/s13399-022-03129-1

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