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Nematode-free agricultural system of a fungus-growing termite.

ABSTRACT: Fungus-growing termites forage dead plant materials from the field to cultivate symbiotic Termitomyces fungi in the nest. Termite foraging behavior and the entry of symbiotic arthropod inquilines may transfer nematodes into a nest and adversely affect fungus production. To test whether nematodes were transferred to fungus gardens by termites and inquilines, we examined the occurrence of nematodes in fungus gardens, five termite castes, and nine species of inquilines of a fungus-growing termite, Odontotermes formosanus. Our results revealed that nematodes were commonly carried by foraging termites and beetle inquilines. Numerous nematodes were found under the beetle elytra. No nematodes were found on termite larvae, eggs, and wingless inquilines. In addition, nematodes rarely occurred in the fungus garden. By observing the response of nematodes to three species of Termitomyces spp. and the fungus gardens, we confirmed that the fungus and fungus gardens are not actually toxic to nematodes. We suggest that nematodes were suppressed through grooming behavior and gut antimicrobial activity in termites, rather than through the antimicrobial activity of the fungus.

SUBMITTER: Kanzaki N

PROVIDER: S-EPMC6586928 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Nematode-free agricultural system of a fungus-growing termite.

Kanzaki Natsumi N Liang Wei-Ren WR Chiu Chun-I CI Yang Ching-Ting CT Hsueh Yen-Ping YP Li Hou-Feng HF

Scientific reports 20190620 1

Fungus-growing termites forage dead plant materials from the field to cultivate symbiotic Termitomyces fungi in the nest. Termite foraging behavior and the entry of symbiotic arthropod inquilines may transfer nematodes into a nest and adversely affect fungus production. To test whether nematodes were transferred to fungus gardens by termites and inquilines, we examined the occurrence of nematodes in fungus gardens, five termite castes, and nine species of inquilines of a fungus-growing termite, ...[more]

PMID: 31222010

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Project description: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.

Project description:BACKGROUND:The metagenomic analysis of gut microbiomes has emerged as a powerful strategy for the identification of biomass-degrading enzymes, which will be no doubt useful for the development of advanced biorefining processes. In the present study, we have performed a functional metagenomic analysis on comb and gut microbiomes associated with the fungus-growing termite, Pseudacanthotermes militaris. RESULTS:Using whole termite abdomens and fungal-comb material respectively, two fosmid-based metagenomic libraries were created and screened for the presence of xylan-degrading enzymes. This revealed 101 positive clones, corresponding to an extremely high global hit rate of 0.49%. Many clones displayed either ?-d-xylosidase (EC 3.2.1.37) or ?-l-arabinofuranosidase (EC 3.2.1.55) activity, while others displayed the ability to degrade AZCL-xylan or AZCL-?-(1,3)-?-(1,4)-glucan. Using secondary screening it was possible to pinpoint clones of interest that were used to prepare fosmid DNA. Sequencing of fosmid DNA generated 1.46 Mbp of sequence data, and bioinformatics analysis revealed 63 sequences encoding putative carbohydrate-active enzymes, with many of these forming parts of sequence clusters, probably having carbohydrate degradation and metabolic functions. Taxonomic assignment of the different sequences revealed that Firmicutes and Bacteroidetes were predominant phyla in the gut sample, while microbial diversity in the comb sample resembled that of typical soil samples. Cloning and expression in E. coli of six enzyme candidates identified in the libraries provided access to individual enzyme activities, which all proved to be coherent with the primary and secondary functional screens. CONCLUSIONS:This study shows that the gut microbiome of P. militaris possesses the potential to degrade biomass components, such as arabinoxylans and arabinans. Moreover, the data presented suggests that prokaryotic microorganisms present in the comb could also play a part in the degradation of biomass within the termite mound, although further investigation will be needed to clarify the complex synergies that might exist between the different microbiomes that constitute the termitosphere of fungus-growing termites. This study exemplifies the power of functional metagenomics for the discovery of biomass-active enzymes and has provided a collection of potentially interesting biocatalysts for further study.

Project description:The eusocial termites are well accomplished in chemical communication, but how they achieve the communication using trace amount of no more than two pheromone components is mostly unknown. In this study, the foraging process and trail pheromones of the fungus-growing termite Odontotermes formosanus (Shiraki) were systematically studied and monitored in real-time using a combination of techniques, including video analysis, solid-phase microextraction, gas chromatography coupled with either mass spectrometry or an electroantennographic detector, and bioassays. The trail pheromone components in foraging workers were (3Z)-dodec-3-en-1-ol and (3Z,6Z)-dodeca-3,6-dien-1-ol secreted by their sternal glands. Interestingly, ratio of the two components changed according to the behaviors that the termites were displaying. This situation only occurs in termites whereas ratios of pheromone components are fixed and species-specific for other insect cuticular glands. Moreover, in bioassays, the active thresholds of the two components ranged from 1 fg/cm to 10 pg/cm according to the behavioral contexts or the pheromonal exposure of tested workers. The two components did not act in synergy. (3Z)-Dodec-3-en-1-ol induced orientation behavior of termites that explore their environment, whereas (3Z,6Z)-dodeca-3,6-dien-1-ol had both an orientation effect and a recruitment effect when food was discovered. The trail pheromone of O. formosanus was regulated both quantitatively by the increasing number of workers involved in the early phases of foraging process, and qualitatively by the change in ratio of the two pheromone components on sternal glandular cuticle in the food-collecting workers. In bioassays, the responses of workers to the pheromone were also affected by the variation in pheromone concentration and component ratio in the microenvironment. Thus, this termite could exchange more information with nestmates using the traces of the two trail pheromone components that can be easily regulated within a limited microenvironment formed by the tunnels or chambers.

Dataset Information

Nematode-free agricultural system of a fungus-growing termite.

Publications

Nematode-free agricultural system of a fungus-growing termite.

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