Species- and Caste-Specific Gut Metabolomes in Fungus-Farming Termites.
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ABSTRACT:
SUBMITTER: Vidkjær NH
PROVIDER: S-EPMC8707012 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Fungus-growing termites engage in an obligate mutualistic relationship with Termitomyces fungi, which they maintain in monocultures on specialised fungus comb structures, without apparent problems with infectious diseases. While other fungi have been reported in the symbiosis, detailed comb fungal community analyses have been lacking. Here we use culture-dependent and -independent methods to characterise fungus comb mycobiotas from three fungus-growing termite species (two genera). Internal Transcribed Spacer (ITS) gene analyses using 454 pyrosequencing and Illumina MiSeq showed that non-Termitomyces fungi were essentially absent in fungus combs, and that Termitomyces fungal crops are maintained in monocultures as heterokaryons with two or three abundant ITS variants in a single fungal strain. To explore whether the essential absence of other fungi within fungus combs is potentially due to the production of antifungal metabolites by Termitomyces or comb bacteria, we performed in vitro assays and found that both Termitomyces and chemical extracts of fungus comb material can inhibit potential fungal antagonists. Chemical analyses of fungus comb material point to a highly complex metabolome, including compounds with the potential to play roles in mediating these contaminant-free farming conditions in the termite symbiosis.
| S-EPMC6584615 | biostudies-literature
Project description:The gut microbiotas of cockroaches and termites play important roles in the symbiotic digestion of dietary components, such as lignocellulose. Diet has been proposed as a primary determinant of community structure within the gut, acting as a selection force to shape the diversity observed within this "bioreactor", and as a key factor for the divergence of the termite gut microbiota from the omnivorous cockroach ancestor. The gut microbiota in most termites supports primarily the breakdown of lignocellulose, but the fungus-farming sub-family of higher termites has become similar in gut microbiota to the ancestral omnivorous cockroaches. To assess the importance of a fungus diet as a driver of community structure, we compare community compositions in the guts of experimentally manipulated Pycnoscelus surinamensis cockroaches fed on fungus cultivated by fungus-farming termites. MiSeq amplicon analysis of gut microbiotas from 49 gut samples showed a step-wise gradient pattern in community similarity that correlated with an increase in the proportion of fungal material provided to the cockroaches. Comparison of the taxonomic composition of manipulated communities to that of gut communities of a fungus-feeding termite species showed that although some bacteria OTUs shared by P. surinamensis and the farming termites increased in the guts of cockroaches on a fungal diet, cockroach communities remained distinct from those of termites. These results demonstrate that a fungal diet can play a role in structuring gut community composition, but at the same time exemplifies how original community compositions constrain the magnitude of such change.
| S-EPMC5626473 | biostudies-literature
Project description:Here, we describe four novel circular single-stranded DNA viruses discovered in fungus-farming termites (Odontotermes sp.). The viruses, named termite-associated circular virus 1 (TaCV-1) through TaCV-4, are most similar to members of the family Genomoviridae and were widely detected in African termite mounds.
| S-EPMC5920188 | biostudies-literature
Project description:BackgroundFungus-cultivating termites make use of an obligate mutualism with fungi from the genus Termitomyces, which are acquired through either vertical transmission via reproductive alates or horizontally transmitted during the formation of new mounds. Termitomyces taxonomy, and thus estimating diversity and host specificity of these fungi, is challenging because fruiting bodies are rarely found. Molecular techniques can be applied but need not necessarily yield the same outcome than morphological identification.MethodologyCulture-dependent and culture-independent methods were used to comprehensively assess host specificity and gut fungal diversity. Termites were identified using mitochondrial cytochrome oxidase II (COII) genes. Twenty-three Termitomyces cultures were isolated from fungal combs. Internal transcribed spacer (ITS) clone libraries were constructed from termite guts. Presence of Termitomyces was confirmed using specific and universal primers. Termitomyces species boundaries were estimated by cross-comparison of macromorphological and sequence features, and ITS clustering parameters accordingly optimized. The overall trends in coverage of Termitomyces diversity and host associations were estimated using Genbank data.Results and conclusionResults indicate a monoculture of Termitomyces in the guts as well as the isolation sources (fungal combs). However, cases of more than one Termitomyces strains per mound were observed since mounds can contain different termite colonies. The newly found cultures, as well as the clustering analysis of GenBank data indicate that there are on average between one and two host genera per Termitomyces species. Saturation does not appear to have been reached, neither for the total number of known Termitomyces species nor for the number of Termitomyces species per host taxon, nor for the number of known hosts per Termitomyces species. Considering the rarity of Termitomyces fruiting bodies, it is suggested to base the future taxonomy of the group mainly on well-characterized and publicly accessible cultures.
| S-EPMC3577893 | biostudies-literature
Project description:Mass-energy transfer across the boundaries of living systems is crucial for the maintenance of homeostasis; however, it is scarcely known how structural strength and integrity is maintained in extended phenotypes while also achieving optimum heat-mass exchange. Here we present data on strength, stability, porosity and permeability of termite mounds of a fungus-farming species, Odontotermes obesus. We demonstrate that the termite mound is a bi-layered structure with a dense, strong core and a porous shell that is constantly remodelled. Its safety factor is extraordinarily high and is orders of magnitude higher than those of human constructions. The porous peripheries are analogous to the mulch layer used in agriculture and help in moisture retention crucial for the survival of fungus gardens, while also allowing adequate wind-induced ventilation of the mounds. We suggest that the architectural solutions offered by these termites have wider implications for natural and industrial building technologies.
| S-EPMC7403385 | biostudies-literature
Project description:The survival and foraging of Coptotermesformosanus Shiraki in a microbe-rich environment reflect the adaptation of an extraordinary, sophisticated defense mechanism by the nest-mates. We aimed to explore the host pathogen interaction by studying caste-specific volatile chemistry and genes encoding the antioxidant defense of winged imagoes, nymphs, soldiers and workers of Formosan subterranean termites. Qualitative analyses of C.formosanus Shiraki performed by HS-SPME/GC-MS showed considerable variations in the chemical composition of volatile organic compounds (VOCs) and their proportions among all the castes. Winged imagoes produced the most important compounds such as naphthalene and n-hexanoic acid. The antifungal activity of these compounds along with nonanal, n-pentadecane, n-tetradecane, n-heptadecane and methyl octanoate against the conidial suspensions of Metarhiziumanisopliae and Beauveriabassiana isolates enable us to suggest that the failure of natural fungal infection in the nest is due to the antiseptic environment of the nest, which is mainly controlled by the VOCs of nest-mates. In addition, conidial germination of M.anisopliae and B.bassiana isolates evaluated on the cuticle of each caste showed significant variations among isolates and different castes. Our results showed that the conidia of M.anisopliae 02049 exhibited the highest germination on the cuticle of all the inoculated castes. Moreover, we recorded the lowest germination of the conidia of B.bassiana 200436. Caste-specific germination variations enabled us to report for the first time that the cuticle of winged imagoes was found to be the most resistant cuticle. The analysis of the transcriptome of C.formosanus Shiraki revealed the identification of 17 genes directly involved in antioxidant defense. Expression patterns of the identified antioxidant genes by quantitative real-time PCR (qPCR) revealed the significantly highest upregulation of CAT, GST, PRXSL, Cu/Zn-SOD2, TXN1, TXN2, TXNL1, TXNL2, TXNL4A and TPx genes among winged imagoes upon infection with the most virulent isolate, M.anisopliae 02049. Furthermore, soldiers showed the least expression of genes encoding antioxidant defense. Our findings indicated that the volatile chemistry of nest-mates and genes encoding antioxidant defense greatly contribute to the survival and foraging of Formosan subterranean termites in a microbe-rich habitat.
| S-EPMC5751295 | biostudies-literature
Project description:The hallmark of social insects is their caste system: reproduction is primarily monopolized by queens, whereas workers specialize in the other tasks required for colony growth and survival. Pheromones produced by reigning queens have long been believed to be the prime factor inhibiting the differentiation of new reproductive individuals. However, there has been very little progress in the chemical identification of such inhibitory pheromones. Here we report the identification of a volatile inhibitory pheromone produced by female neotenics (secondary queens) that acts directly on target individuals to suppress the differentiation of new female neotenics and identify n-butyl-n-butyrate and 2-methyl-1-butanol as the active components of the inhibitory pheromone. An artificial pheromone blend consisting of these two compounds had a strong inhibitory effect similar to live neotenics. Surprisingly, the same two volatiles are also emitted by eggs, playing a role both as an attractant to workers and an inhibitor of reproductive differentiation. This dual production of an inhibitory pheromone by female reproductives and eggs probably reflects the recruitment of an attractant pheromone as an inhibitory pheromone and may provide a mechanism ensuring honest signaling of reproductive status with a tight coupling between fertility and inhibitory power. Identification of a volatile pheromone regulating caste differentiation in a termite provides insights into the functioning of social insect colonies and opens important avenues for elucidating the developmental pathways leading to reproductive and nonreproductive castes.
| S-EPMC2919916 | biostudies-literature
Project description:BackgroundTermites are an important food resource for many human populations around the world, and are a good supply of nutrients. The fungus-farming 'higher' termite members of Macrotermitinae are also consumed by modern great apes and are implicated as critical dietary resources for early hominins. While the chemical nutritional composition of edible termites is well known, their microbiomes are unexplored in the context of human health. Here we sequenced the V4 region of the 16S rRNA gene of gut microbiota extracted from the whole intestinal tract of two Macrotermes sp. soldiers collected from the Limpopo region of South Africa.ResultsMajor and minor soldier subcastes of M. falciger exhibit consistent differences in taxonomic representation, and are variable in microbial presence and abundance patterns when compared to another edible but less preferred species, M. natalensis. Subcaste differences include alternate patterns in sulfate-reducing bacteria and methanogenic Euryarchaeota abundance, and differences in abundance between Alistipes and Ruminococcaceae. M. falciger minor soldiers and M. natalensis soldiers have similar microbial profiles, likely from close proximity to the termite worker castes, particularly during foraging and fungus garden cultivation. Compared with previously published termite and cockroach gut microbiome data, the taxonomic representation was generally split between termites that directly digest lignocellulose and humic substrates and those that consume a more distilled form of nutrition as with the omnivorous cockroaches and fungus-farming termites. Lastly, to determine if edible termites may point to a shared reservoir for rare bacterial taxa found in the gut microbiome of humans, we focused on the genus Treponema. The majority of Treponema sequences from edible termite gut microbiota most closely relate to species recovered from other termites or from environmental samples, except for one novel OTU strain, which clustered separately with Treponema found in hunter-gatherer human groups.ConclusionsMacrotermes consumed by humans display special gut microbial arrangements that are atypical for a lignocellulose digesting invertebrate, but are instead suited to the simplified nutrition in the fungus-farmer diet. Our work brings to light the particular termite microbiome features that should be explored further as avenues in human health, agricultural sustainability, and evolutionary research.
| S-EPMC6637627 | biostudies-literature
Project description:Several fungal genera and species occurring in the fungus-growing termite fungus combs Raw sequence reads
| PRJNA438656 | ENA
Project description:Fungus-growing termites are eusocial insects that represent one of the most efficient and unique systems for lignocellulose bioconversion, evolved from a sophisticated symbiosis with lignocellulolytic fungi and gut bacterial communities. Despite a plethora of information generated during the last century, some essential information on gut bacterial profiles and their unique contributions to wood digestion in some fungus-growing termites is still inadequate. Hence, using the culture-dependent approach, the present study aims to assess and compare the diversity of lignocellulose-degrading bacterial symbionts within the gut systems of three fungus-growing termites: Ancistrotermes pakistanicus, Odontotermes longignathus, and Macrotermes sp. A total of 32 bacterial species, belonging to 18 genera and 10 different families, were successfully isolated and identified from three fungus-growing termites using Avicel or xylan as the sole source of carbon. Enterobacteriaceae was the most dominant family represented by 68.1% of the total bacteria, followed by Yersiniaceae (10.6%) and Moraxellaceae (9%). Interestingly, five bacterial genera such as Enterobacter, Citrobacter, Acinetobacter, Trabulsiella, and Kluyvera were common among the tested termites, while the other bacteria demonstrated a termite-specific distribution. Further, the lignocellulolytic potential of selected bacterial strains was tested on agricultural waste to evaluate their capability for lignocellulose bioconversion. The highest substrate degradation was achieved with E. chengduensis MA11 which degraded 45.52% of rice straw. All of the potential strains showed endoglucanase, exoglucanase, and xylanase activities depicting a symbiotic role towards the lignocellulose digestion within the termite gut. The above results indicated that fungus-growing termites harbor a diverse array of bacterial symbionts that differ from species to species, which may play an inevitable role to enhance the degradation efficacy in lignocellulose decomposition. The present study further elaborates our knowledge about the termite-bacteria symbiosis for lignocellulose bioconversion which could be helpful to design a future biorefinery.
| S-EPMC10146277 | biostudies-literature