The Antimicrobial Defence and Biomass Decomposition of Fungus-Growing Termites and Microbial Symbionts

Haofu Hu

The Antimicrobial Defence and Biomass Decomposition of Fungus-Growing Termites and Microbial Symbionts

Abstract

Termites are a group of eusocial insects that have tight symbiotic relationships with microbes in their gut. Fungus-growing termites from subfamily Macrotermitinae had engaged in another special obligated symbiosis with basidiomycete fungus Termitomyces, which is a remarkable symbiotic innovation impacted their behaviour and lifestyle. Fungus-growing termites maintain a fungus garden made by harvested plant material from environment for Termitomyces farming and consume the crops as protein-rich diet. Termitomyces in return are benefited from the optimal growth condition maintained by termites and constant inoculation of free substrates. This tripartite symbiosis between termites, fungus and gut bacteria are considered the key to the successful establishment of fungus-growing termites in subtropical and tropical regions of Asia and Africa. We focused our studies on two remarkable aspects of this evolutionary successful symbiosis: defensive symbiosis against pathogens and digestive symbiosis of plant and fungal biomass. First, we used metagenome, genome and transcriptome to systematically predict the defensive potential of termites and gut microbiota. In genome and transcriptome of all termites, we identified the presence of antimicrobial peptides (AMPs) and found signal of positive selection. Challenging the fungus garden of fungus-growing termite with pathogens, we found expressional responds of these AMPs against termite pathogens. In the metagenome, we identified biosynthetic gene clusters (BGCs) encode by the gut bacteria. This indicates gut bacteria of termites have high potential in producing antimicrobial natural products. Isolation of the Actinobacteria from termite gut and fungus comb have identified strains with antimicrobial activity. Chemical analysis has confirmed the production of antimicrobial compounds in these strains. To understand the digestive symbiosis fungus-growing termites, we used metagenome and transcriptome sequencing to identified enzymes for biomass degradation in gut microbiota and Termitomyces. In the metagenome of fungus-growing termites, we identified high composition of mycolytic enzymes that contributed by the most abundant bacteria groups in the gut, while the plant degrading enzymes are under present. This indicates the gut microbiota shifted to mycolytic function for the fungal rich diet of fungus-growing termites. In the transcriptome of Termitomyces, we identified the presence and high expression of plant material degrading enzymes. Using enzyme assays and expression level comparison, we detected enzyme activities and expressions differ throughout the plant biomass breakdown process in the colony and vary between termite species. We demonstrated the efficacy of the digestive symbiosis by the ability to decompose a wide-range of complex plant substrates and suggested specific metabolic adaptations of the symbiont in different species. Collectively, our results demonstrated that fungusgrowing termites, Termitomyces and gut bacteria all contribute to the defensive symbiosis and digestive symbiosis with possible functional complementary between the partners.

Original language	English

Publisher	Department of Biology, Faculty of Science, University of Copenhagen
Publication status	Published - 2019

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title = "The Antimicrobial Defence and Biomass Decomposition of Fungus-Growing Termites and Microbial Symbionts",

abstract = "Termites are a group of eusocial insects that have tight symbiotic relationships with microbes in their gut. Fungus-growing termites from subfamily Macrotermitinae had engaged in another special obligated symbiosis with basidiomycete fungus Termitomyces, which is a remarkable symbiotic innovation impacted their behaviour and lifestyle. Fungus-growing termites maintain a fungus garden made by harvested plant material from environment for Termitomyces farming and consume the crops as protein-rich diet. Termitomyces in return are benefited from the optimal growth condition maintained by termites and constant inoculation of free substrates. This tripartite symbiosis between termites, fungus and gut bacteria are considered the key to the successful establishment of fungus-growing termites in subtropical and tropical regions of Asia and Africa. We focused our studies on two remarkable aspects of this evolutionary successful symbiosis: defensive symbiosis against pathogens and digestive symbiosis of plant and fungal biomass. First, we used metagenome, genome and transcriptome to systematically predict the defensive potential of termites and gut microbiota. In genome and transcriptome of all termites, we identified the presence of antimicrobial peptides (AMPs) and found signal of positive selection. Challenging the fungus garden of fungus-growing termite with pathogens, we found expressional responds of these AMPs against termite pathogens. In the metagenome, we identified biosynthetic gene clusters (BGCs) encode by the gut bacteria. This indicates gut bacteria of termites have high potential in producing antimicrobial natural products. Isolation of the Actinobacteria from termite gut and fungus comb have identified strains with antimicrobial activity. Chemical analysis has confirmed the production of antimicrobial compounds in these strains. To understand the digestive symbiosis fungus-growing termites, we used metagenome and transcriptome sequencing to identified enzymes for biomass degradation in gut microbiota and Termitomyces. In the metagenome of fungus-growing termites, we identified high composition of mycolytic enzymes that contributed by the most abundant bacteria groups in the gut, while the plant degrading enzymes are under present. This indicates the gut microbiota shifted to mycolytic function for the fungal rich diet of fungus-growing termites. In the transcriptome of Termitomyces, we identified the presence and high expression of plant material degrading enzymes. Using enzyme assays and expression level comparison, we detected enzyme activities and expressions differ throughout the plant biomass breakdown process in the colony and vary between termite species. We demonstrated the efficacy of the digestive symbiosis by the ability to decompose a wide-range of complex plant substrates and suggested specific metabolic adaptations of the symbiont in different species. Collectively, our results demonstrated that fungusgrowing termites, Termitomyces and gut bacteria all contribute to the defensive symbiosis and digestive symbiosis with possible functional complementary between the partners.",

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year = "2019",

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T1 - The Antimicrobial Defence and Biomass Decomposition of Fungus-Growing Termites and Microbial Symbionts

AU - Hu, Haofu

PY - 2019

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N2 - Termites are a group of eusocial insects that have tight symbiotic relationships with microbes in their gut. Fungus-growing termites from subfamily Macrotermitinae had engaged in another special obligated symbiosis with basidiomycete fungus Termitomyces, which is a remarkable symbiotic innovation impacted their behaviour and lifestyle. Fungus-growing termites maintain a fungus garden made by harvested plant material from environment for Termitomyces farming and consume the crops as protein-rich diet. Termitomyces in return are benefited from the optimal growth condition maintained by termites and constant inoculation of free substrates. This tripartite symbiosis between termites, fungus and gut bacteria are considered the key to the successful establishment of fungus-growing termites in subtropical and tropical regions of Asia and Africa. We focused our studies on two remarkable aspects of this evolutionary successful symbiosis: defensive symbiosis against pathogens and digestive symbiosis of plant and fungal biomass. First, we used metagenome, genome and transcriptome to systematically predict the defensive potential of termites and gut microbiota. In genome and transcriptome of all termites, we identified the presence of antimicrobial peptides (AMPs) and found signal of positive selection. Challenging the fungus garden of fungus-growing termite with pathogens, we found expressional responds of these AMPs against termite pathogens. In the metagenome, we identified biosynthetic gene clusters (BGCs) encode by the gut bacteria. This indicates gut bacteria of termites have high potential in producing antimicrobial natural products. Isolation of the Actinobacteria from termite gut and fungus comb have identified strains with antimicrobial activity. Chemical analysis has confirmed the production of antimicrobial compounds in these strains. To understand the digestive symbiosis fungus-growing termites, we used metagenome and transcriptome sequencing to identified enzymes for biomass degradation in gut microbiota and Termitomyces. In the metagenome of fungus-growing termites, we identified high composition of mycolytic enzymes that contributed by the most abundant bacteria groups in the gut, while the plant degrading enzymes are under present. This indicates the gut microbiota shifted to mycolytic function for the fungal rich diet of fungus-growing termites. In the transcriptome of Termitomyces, we identified the presence and high expression of plant material degrading enzymes. Using enzyme assays and expression level comparison, we detected enzyme activities and expressions differ throughout the plant biomass breakdown process in the colony and vary between termite species. We demonstrated the efficacy of the digestive symbiosis by the ability to decompose a wide-range of complex plant substrates and suggested specific metabolic adaptations of the symbiont in different species. Collectively, our results demonstrated that fungusgrowing termites, Termitomyces and gut bacteria all contribute to the defensive symbiosis and digestive symbiosis with possible functional complementary between the partners.

AB - Termites are a group of eusocial insects that have tight symbiotic relationships with microbes in their gut. Fungus-growing termites from subfamily Macrotermitinae had engaged in another special obligated symbiosis with basidiomycete fungus Termitomyces, which is a remarkable symbiotic innovation impacted their behaviour and lifestyle. Fungus-growing termites maintain a fungus garden made by harvested plant material from environment for Termitomyces farming and consume the crops as protein-rich diet. Termitomyces in return are benefited from the optimal growth condition maintained by termites and constant inoculation of free substrates. This tripartite symbiosis between termites, fungus and gut bacteria are considered the key to the successful establishment of fungus-growing termites in subtropical and tropical regions of Asia and Africa. We focused our studies on two remarkable aspects of this evolutionary successful symbiosis: defensive symbiosis against pathogens and digestive symbiosis of plant and fungal biomass. First, we used metagenome, genome and transcriptome to systematically predict the defensive potential of termites and gut microbiota. In genome and transcriptome of all termites, we identified the presence of antimicrobial peptides (AMPs) and found signal of positive selection. Challenging the fungus garden of fungus-growing termite with pathogens, we found expressional responds of these AMPs against termite pathogens. In the metagenome, we identified biosynthetic gene clusters (BGCs) encode by the gut bacteria. This indicates gut bacteria of termites have high potential in producing antimicrobial natural products. Isolation of the Actinobacteria from termite gut and fungus comb have identified strains with antimicrobial activity. Chemical analysis has confirmed the production of antimicrobial compounds in these strains. To understand the digestive symbiosis fungus-growing termites, we used metagenome and transcriptome sequencing to identified enzymes for biomass degradation in gut microbiota and Termitomyces. In the metagenome of fungus-growing termites, we identified high composition of mycolytic enzymes that contributed by the most abundant bacteria groups in the gut, while the plant degrading enzymes are under present. This indicates the gut microbiota shifted to mycolytic function for the fungal rich diet of fungus-growing termites. In the transcriptome of Termitomyces, we identified the presence and high expression of plant material degrading enzymes. Using enzyme assays and expression level comparison, we detected enzyme activities and expressions differ throughout the plant biomass breakdown process in the colony and vary between termite species. We demonstrated the efficacy of the digestive symbiosis by the ability to decompose a wide-range of complex plant substrates and suggested specific metabolic adaptations of the symbiont in different species. Collectively, our results demonstrated that fungusgrowing termites, Termitomyces and gut bacteria all contribute to the defensive symbiosis and digestive symbiosis with possible functional complementary between the partners.

UR - https://rex.kb.dk/permalink/f/h35n6k/KGL01012062439

M3 - Ph.D. thesis

BT - The Antimicrobial Defence and Biomass Decomposition of Fungus-Growing Termites and Microbial Symbionts

PB - Department of Biology, Faculty of Science, University of Copenhagen

ER -

The Antimicrobial Defence and Biomass Decomposition of Fungus-Growing Termites and Microbial Symbionts

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