Tripartite Symbiotic Digestion of Lignocellulose in the Digestive System of a Fungus-Growing Termite
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Tripartite Symbiotic Digestion of Lignocellulose in the Digestive System of a Fungus-Growing Termite. / Ahmad, Farhan; Yang, Guiying; Zhu, Yaning; Poulsen, Michael; Li, Wuhan; Yu, Ting; Mo, Jianchu.
I: Microbiology Spectrum, Bind 10, Nr. 6, e01234-22, 2022.Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › fagfællebedømt
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TY - JOUR
T1 - Tripartite Symbiotic Digestion of Lignocellulose in the Digestive System of a Fungus-Growing Termite
AU - Ahmad, Farhan
AU - Yang, Guiying
AU - Zhu, Yaning
AU - Poulsen, Michael
AU - Li, Wuhan
AU - Yu, Ting
AU - Mo, Jianchu
PY - 2022
Y1 - 2022
N2 - Fungus-farming termites have a mutualist association with fungi of the genus Termitomyces and gut microbiota to support the nearly complete decomposition of lignocellulose to gain access to nutrients. This elaborate strategy of plant biomass digestion makes them ecologically successful dominant decomposers in (sub)tropical Old World ecosystems.Fungus-growing termites are efficient in degrading and digesting plant substrates, achieved through the engagement of symbiotic gut microbiota and lignocellulolytic Termitomyces fungi cultivated for protein-rich food. Insights into where specific plant biomass components are targeted during the decomposition process are sparse. In this study, we performed several analytical approaches on the fate of plant biomass components and did amplicon sequencing of the 16S rRNA gene to investigate the lignocellulose digestion in the symbiotic system of the fungus-growing termite Odontotermes formosanus (Shiraki) and to compare bacterial communities across the different stages in the degradation process. We observed a gradual reduction of lignocellulose components throughout the process. Our findings support that the digestive tract of young workers initiates the degradation of lignocellulose but leaves most of the lignin, hemicellulose, and cellulose, which enters the fresh fungus comb, where decomposition primarily occurs. We found a high diversity and quantity of monomeric sugars in older parts of the fungus comb, indicating that the decomposition of lignocellulose enriches the old comb with sugars that can be utilized by Termitomyces and termite workers. Amplicon sequencing of the 16S rRNA gene showed clear differences in community composition associated with the different stages of plant biomass decomposition which could work synergistically with Termitomyces to shape the digestion process. IMPORTANCE Fungus-farming termites have a mutualist association with fungi of the genus Termitomyces and gut microbiota to support the nearly complete decomposition of lignocellulose to gain access to nutrients. This elaborate strategy of plant biomass digestion makes them ecologically successful dominant decomposers in (sub)tropical Old World ecosystems. We employed acid detergent fiber analysis, high-performance anion-exchange chromatography (HPAEC), high-performance liquid chromatography (HPLC), scanning electron microscopy (SEM), Fourier transform infrared spectroscopy (FTIR), X-ray diffraction (XRD), pyrolysis gas chromatography-mass spectrometry (Py-GC-MS), and amplicon sequencing of the 16S rRNA gene to examine which lignocellulose components were digested and which bacteria were abundant throughout the decomposition process. Our findings suggest that although the first gut passage initiates lignocellulose digestion, the most prominent decomposition occurs within the fungus comb. Moreover, distinct bacterial communities were associated with different stages of decomposition, potentially contributing to the breakdown of particular plant components.
AB - Fungus-farming termites have a mutualist association with fungi of the genus Termitomyces and gut microbiota to support the nearly complete decomposition of lignocellulose to gain access to nutrients. This elaborate strategy of plant biomass digestion makes them ecologically successful dominant decomposers in (sub)tropical Old World ecosystems.Fungus-growing termites are efficient in degrading and digesting plant substrates, achieved through the engagement of symbiotic gut microbiota and lignocellulolytic Termitomyces fungi cultivated for protein-rich food. Insights into where specific plant biomass components are targeted during the decomposition process are sparse. In this study, we performed several analytical approaches on the fate of plant biomass components and did amplicon sequencing of the 16S rRNA gene to investigate the lignocellulose digestion in the symbiotic system of the fungus-growing termite Odontotermes formosanus (Shiraki) and to compare bacterial communities across the different stages in the degradation process. We observed a gradual reduction of lignocellulose components throughout the process. Our findings support that the digestive tract of young workers initiates the degradation of lignocellulose but leaves most of the lignin, hemicellulose, and cellulose, which enters the fresh fungus comb, where decomposition primarily occurs. We found a high diversity and quantity of monomeric sugars in older parts of the fungus comb, indicating that the decomposition of lignocellulose enriches the old comb with sugars that can be utilized by Termitomyces and termite workers. Amplicon sequencing of the 16S rRNA gene showed clear differences in community composition associated with the different stages of plant biomass decomposition which could work synergistically with Termitomyces to shape the digestion process. IMPORTANCE Fungus-farming termites have a mutualist association with fungi of the genus Termitomyces and gut microbiota to support the nearly complete decomposition of lignocellulose to gain access to nutrients. This elaborate strategy of plant biomass digestion makes them ecologically successful dominant decomposers in (sub)tropical Old World ecosystems. We employed acid detergent fiber analysis, high-performance anion-exchange chromatography (HPAEC), high-performance liquid chromatography (HPLC), scanning electron microscopy (SEM), Fourier transform infrared spectroscopy (FTIR), X-ray diffraction (XRD), pyrolysis gas chromatography-mass spectrometry (Py-GC-MS), and amplicon sequencing of the 16S rRNA gene to examine which lignocellulose components were digested and which bacteria were abundant throughout the decomposition process. Our findings suggest that although the first gut passage initiates lignocellulose digestion, the most prominent decomposition occurs within the fungus comb. Moreover, distinct bacterial communities were associated with different stages of decomposition, potentially contributing to the breakdown of particular plant components.
KW - Odontotermes formosanus
KW - bioconversion
KW - lignocellulose
KW - bacteria
KW - Termitomyces
KW - symbiosis
KW - GUT MICROBIOTA
KW - FUNCTIONAL-ANALYSIS
KW - STRUCTURAL-CHANGES
KW - COMMUNITY
KW - DEGRADATION
KW - ISOPTERA
KW - BACTERIA
KW - BIOMASS
KW - TERMITOMYCES
KW - POLYETHISM
U2 - 10.1128/spectrum.01234-22
DO - 10.1128/spectrum.01234-22
M3 - Journal article
C2 - 36250871
VL - 10
JO - Microbiology spectrum
JF - Microbiology spectrum
SN - 2165-0497
IS - 6
M1 - e01234-22
ER -
ID: 325449929