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Decaying wood, while an abundant and stable resource, presents considerable nutritional challenges due to its structural rigidity, chemical recalcitrance, and low nitrogen content. Despite these challenges, certain insect lineages have successfully evolved saproxylophagy (consuming and deriving sustenance from decaying wood), impacting nutrient recycling in ecosystems and carbon sequestration dynamics. This study explores the uneven phylogenetic distribution of saproxylophagy across insects and delves into the evolutionary origins of this trait in disparate insect orders. Employing a comprehensive analysis of gut microbiome data, from both saproxylophagous insects and their non-saproxylophagous relatives, including new data from unexplored wood-feeding insects, this Hypothesis paper discusses the broader phylogenetic context and potential adaptations necessary for this dietary specialization. The study proposes the "Detritivore-First Hypothesis," suggesting an evolutionary pathway to saproxylophagy through detritivory, and highlights the critical role of symbiotic gut microbiomes in the digestion of decaying wood.
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Evolução Biológica , Microbioma Gastrointestinal , Insetos , Madeira , Animais , Comportamento Alimentar/fisiologia , Insetos/classificação , Insetos/microbiologia , Insetos/fisiologia , Mastigação , FilogeniaRESUMO
The co-evolution between symbionts and their insect hosts has led to intricate functional interdependencies. Advances in DNA-sequencing technologies have not only reduced the cost of sequencing but, with the advent of highly accurate long-read methods, have also enabled facile genome assembly even using mixed genomic input, thereby allowing us to more easily assess the contribution of symbionts to their insect hosts. In this study, genomic data recently generated from Peregrinus maidis was used to assemble the genome of a bacterial symbiont, Pm Arsenophonus sp. This ~4.9-Mb assembly is one of the largest Arsenophonus genomes reported to date. The Benchmarking Universal Single-Copy Orthologs (BUSCO) result indicates that this Pm Arsenophonus assembly has a high degree of completeness, with 96% of the single-copy Enterobacterales orthologs found. The identity of the Pm Arsenophonus sp. was further confirmed by phylogenetic analysis. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis indicates a major contribution by Pm Arsenophonus sp. to the biosynthesis of B vitamins and essential amino acids in P. maidis, where threonine and lysine production is carried out solely by Pm Arsenophonus sp. This study not only provides deeper insights into the evolutionary relationships between symbionts and their insect hosts, but also adds to our understanding of insect biology, potentially guiding the development of novel pest control methods.
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Laboratory research in Ghana demonstrated the effectiveness of an isolate of Beauveria bassiana (IMI 389521) from the United Kingdom against the larger grain borer Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae), a major pest of stored maize. The minimum effective concentration, following artificial infestation trials on maize, was between 109 and 1010 cfu/kg maize. Before moving out to village-level control, a major requirement was to determine if the product could effect control in artificially infested maize held under real environmental conditions in several locations in Ghana. Therefore, this study investigated the efficacy of formulated conidia of B. bassiana, IMI 389521, at two concentrations (1 × 109 and 3.16 × 109 cfu/kg maize) to control P. truncatus on stored maize kernels under semi-field conditions in Ghana. Maize ('Obatanpa' cultivar) kernels were treated with the formulated B. bassiana product and stored in polypropylene woven bags in cribs in Southern Ghana. After 24 h, one hundred adults of P. truncatus were placed into each bag containing the treated maize. Mortality and the percent of weight loss of kernels were assessed every two weeks for three months. The semi-field trials revealed the possibility of successfully controlling adult P. truncatus on maize kernels treated with B. bassiana at 3.16 × 109 cfu/kg maize. However, due to the minimal protection of kernels after four weeks, re-treating maize kernels after this period is recommended to ensure maximum protection during prolonged storage.
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Beauveria , Besouros , Animais , Zea mays , Gana , Grão Comestível , Controle Biológico de VetoresRESUMO
Cockroaches of the subfamily Panesthiinae (family Blaberidae) are among the few major groups of insects feeding on decayed wood. Despite having independently evolved the ability to thrive on this recalcitrant and nitrogen-limited resource, they are among the least studied of all wood-feeding insect groups. In the pursuit of unraveling their unique digestive strategies, we explored cellulase and xylanase activity in the crop, midgut, and hindgut lumens of Panesthia angustipennis and Salganea taiwanensis. Employing Percoll density gradient centrifugation, we further fractionated luminal fluid to elucidate how the activities in the gut lumen are further partitioned. Our findings challenge conventional wisdom, underscoring the significant contribution of the hindgut, which accounts for approximately one-fifth of cellulase and xylanase activity. Particle-associated enzymes, potentially of bacterial origin, dominate hindgut digestion, akin to symbiotic strategies observed in select termites and passalid beetles. Our study sheds new light on the digestive prowess of panesthiine cockroaches, providing invaluable insights into the evolution of wood-feeding insects and their remarkable adaptability to challenging, nutrient-poor substrates.
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Introduction: Wood digestion in insects relies on the maintenance of a mosaic of numerous microhabitats, each colonized by distinct microbiomes. Understanding the division of digestive labor between these microhabitats- is central to understanding the physiology and evolution of symbiotic wood digestion. A microhabitat that has emerged to be of direct relevance to the process of lignocellulose digestion is the surface of ingested plant material. Wood particles in the guts of some termites are colonized by a specialized bacterial fiber-digesting microbiome, but whether this represents a widespread strategy among insect lineages that have independently evolved wood-feeding remains an open question. Methods: In this study, we investigated the bacterial communities specifically associated with wood fibers in the gut of the passalid beetle Odontotaenius disjunctus. We developed a Percoll-based centrifugation method to isolate and enrich the wood particles from the anterior hindgut, allowing us to access the wood fibers and their associated microbiome. We then performed assays of enzyme activity and used short-read and long-read amplicon sequencing of the 16S rRNA gene to identify the composition of the fiber-associated microbiome. Results: Our assays demonstrated that the anterior hindgut, which houses a majority of the bacterial load, is an important site for lignocellulose digestion. Wood particles enriched from the anterior hindgut contribute to a large proportion of the total enzyme activity. The sequencing revealed that O. disjunctus, like termites, harbors a distinct fiber-associated microbiome, but notably, its community is enriched in insect-specific groups of Lactococcus and Turicibacter. Discussion: Our study underscores the importance of microhabitats in fostering the complex symbiotic relationships between wood-feeding insects and their microbiomes. The discovery of distinct fiber-digesting symbionts in O. disjunctus, compared to termites, highlights the diverse evolutionary paths insects have taken to adapt to a challenging diet.
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The ability of a fungal entomopathogen to infect an insect depends on a variety of factors, including strain, host, and environmental conditions. Similarly, an insect's ability to prevent fungal infection is dependent on its biology, environment, and evolutionary history. Synanthropic pests have adapted to thrive in the indoor environment, yet they arose from divergent evolutionary lineages and occupy different feeding guilds. The hematophagous bed bug (Cimex lectularius) and omnivorous German cockroach (Blattella germanica) are highly successful indoors, but have evolved different physiological and behavioral adaptations to cope with the human-built environment, some of which also reduce the efficacy of fungal biopesticides. In order to gain greater insight into the host barriers that prevent or constrain fungal infection in bed bugs and German cockroaches, we tested different doses of Beauveria bassiana GHA through surface contact, topical application, feeding, and injection. Bed bugs were generally more susceptible to infection by B. bassiana with the mode of delivery having a significant impact on infectivity. The German cockroach was highly resilient to infection, requiring high doses of fungal conidia (>8.8 × 104) delivered by injection into the hemocoel to cause mortality. Mortality occurred much faster in both insect species after exposure to surfaces dusted with dry conidia than surfaces treated with conidia suspended in water or oil. These findings highlight the importance of developing innovative delivery techniques to enhance fungal entomopathogens against bed bugs and cockroaches.
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Phylosymbiosis is a cross-system trend whereby microbial community relationships recapitulate the host phylogeny. In Nasonia parasitoid wasps, phylosymbiosis occurs throughout development, is distinguishable between sexes, and benefits host development and survival. Moreover, the microbiome shifts in hybrids as a rare Proteus bacterium in the microbiome becomes dominant. The larval hybrids then catastrophically succumb to bacterium-assisted lethality and reproductive isolation between the species. Two important questions for understanding phylosymbiosis and bacterium-assisted lethality in hybrids are (i) do the Nasonia bacterial genomes differ from other animal isolates and (ii) are the hybrid bacterial genomes the same as those in the parental species? Here, we report the cultivation, whole-genome sequencing, and comparative analyses of the most abundant gut bacteria in Nasonia larvae, Providencia rettgeri and Proteus mirabilis Characterization of new isolates shows Proteus mirabilis forms a more robust biofilm than Providencia rettgeri and that, when grown in coculture, Proteus mirabilis significantly outcompetes Providencia rettgeri Providencia rettgeri genomes from Nasonia are similar to each other and more divergent from pathogenic, human associates. Proteus mirabilis from Nasonia vitripennis, Nasonia giraulti, and their hybrid offspring are nearly identical and relatively distinct from human isolates. These results indicate that members of the larval gut microbiome within Nasonia are most similar to each other, and the strain of the dominant Proteus mirabilis in hybrids is resident in parental species. Holobiont interactions between shared, resident members of the wasp microbiome and the host underpin phylosymbiosis and hybrid breakdown.IMPORTANCE Animal and plant hosts often establish intimate relationships with their microbiomes. In varied environments, closely related host species share more similar microbiomes, a pattern termed phylosymbiosis. When phylosymbiosis is functionally significant and beneficial, microbial transplants between host species and host hybridization can have detrimental consequences on host biology. In the Nasonia parasitoid wasp genus, which contains a phylosymbiotic gut community, both effects occur and provide evidence for selective pressures on the holobiont. Here, we show that bacterial genomes in Nasonia differ from other environments and harbor genes with unique functions that may regulate phylosymbiotic relationships. Furthermore, the bacteria in hybrids are identical to those in parental species, thus supporting a hologenomic tenet that the same members of the microbiome and the host genome impact phylosymbiosis, hybrid breakdown, and speciation.
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As vectors of microbial diseases in vertebrates, ticks are excellent at regulating bacterial proliferation in and around them. In a recent issue of Cell, Hayes et al. (2020) reveal acarid toxins of bacterial origin that help eliminate microbes that are pathogenic to black-legged ticks but commensal to their vertebrate hosts.
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Ixodes , Amidoidrolases/genética , Animais , Fatores Imunológicos , Simbiose , VertebradosRESUMO
BACKGROUND: Diet is a major determinant of bacterial community structure in termite guts, but evidence of its importance in the closely related cockroaches is conflicting. Here, we investigated the ecological drivers of the bacterial gut microbiota in cockroaches that feed on lignocellulosic leaf litter. RESULTS: The physicochemical conditions determined with microsensors in the guts of Ergaula capucina, Pycnoscelus surinamensis, and Byrsotria rothi were similar to those reported for both wood-feeding and omnivorous cockroaches. All gut compartments were anoxic at the center and showed a slightly acidic to neutral pH and variable but slightly reducing conditions. Hydrogen accumulated only in the crop of B. rothi. High-throughput amplicon sequencing of bacterial 16S rRNA genes documented that community structure in individual gut compartments correlated strongly with the respective microenvironmental conditions. A comparison of the hindgut microbiota of cockroaches and termites from different feeding groups revealed that the vast majority of the core taxa in cockroaches with a lignocellulosic diet were present also in omnivorous cockroaches but absent in wood-feeding higher termites. CONCLUSION: Our results indicate that diet is not the primary driver of bacterial community structure in the gut of wood- and litter-feeding cockroaches. The high similarity to the gut microbiota of omnivorous cockroaches suggests that the dietary components that are actually digested do not differ fundamentally between feeding groups.
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Bactérias/classificação , Baratas/microbiologia , Sequenciamento de Nucleotídeos em Larga Escala/métodos , Isópteros/microbiologia , Folhas de Planta/química , Animais , Bactérias/genética , Bactérias/isolamento & purificação , DNA Bacteriano/genética , DNA Ribossômico/genética , Dieta , Microbioma Gastrointestinal , Concentração de Íons de Hidrogênio , Lignina/metabolismo , Filogenia , RNA Ribossômico 16S/genéticaRESUMO
Social insects owe their ecological success to the division of labour between castes, but associations between microbial community compositions and castes with different tasks and diets have not been extensively explored. Fungus-growing termites associate with fungi to degrade plant material, complemented by diverse gut microbial communities. Here, we explore whether division of labour and accompanying dietary differences between fungus-growing termite castes are linked to gut bacterial community structure. Using amplicon sequencing, we characterize community compositions in sterile (worker and soldier) and reproductive (queen and king) termites and combine this with gut enzyme activities and microscopy to hypothesise sterile caste-specific microbiota roles. Gut bacterial communities are structured primarily according to termite caste and genus and, in contrast to the observed rich and diverse sterile caste microbiotas, royal pair guts are dominated by few bacterial taxa, potentially reflecting their specialized uniform diet and unique lifestyle.
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Comportamento Animal , Dieta , Microbioma Gastrointestinal/fisiologia , Isópteros/microbiologia , Animais , Bactérias/classificação , Bactérias/genética , Biodiversidade , DNA Bacteriano/genética , Especificidade de Hospedeiro , RNA Ribossômico 16S/genética , Análise de Sequência de DNARESUMO
Symbiotic digestion of lignocellulose in wood-feeding higher termites (family Termitidae) is a two-step process that involves endogenous host cellulases secreted in the midgut and a dense bacterial community in the hindgut compartment. The genomes of the bacterial gut microbiota encode diverse cellulolytic and hemicellulolytic enzymes, but the contributions of host and bacterial symbionts to lignocellulose degradation remain ambiguous. Our previous studies of Nasutitermes spp. documented that the wood fibers in the hindgut paunch are consistently colonized not only by uncultured members of Fibrobacteres, which have been implicated in cellulose degradation, but also by unique lineages of Spirochaetes. Here, we demonstrate that the degradation of xylan, the major component of hemicellulose, is restricted to the hindgut compartment, where it is preferentially hydrolyzed over cellulose. Metatranscriptomic analysis documented that the majority of glycoside hydrolase (GH) transcripts expressed by the fiber-associated bacterial community belong to family GH11, which consists exclusively of xylanases. The substrate specificity was further confirmed by heterologous expression of the gene encoding the predominant homolog. Although the most abundant transcripts of GH11 in Nasutitermes takasagoensis were phylogenetically placed among their homologs of Firmicutes, immunofluorescence microscopy, compositional binning of metagenomics contigs, and the genomic context of the homologs indicated that they are encoded by Spirochaetes and were most likely obtained by horizontal gene transfer among the intestinal microbiota. The major role of spirochetes in xylan degradation is unprecedented and assigns the fiber-associated Treponema clades in the hindgut of wood-feeding higher termites a prominent part in the breakdown of hemicelluloses.
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Isópteros/microbiologia , Polissacarídeos/metabolismo , Spirochaetales/enzimologia , Spirochaetales/genética , Spirochaetales/metabolismo , Madeira/metabolismo , Animais , Celulases/genética , Celulases/metabolismo , Celulose/metabolismo , Microbioma Gastrointestinal/genética , Trato Gastrointestinal/microbiologia , Regulação Bacteriana da Expressão Gênica/genética , Transferência Genética Horizontal , Genes Bacterianos/genética , Glicosídeo Hidrolases/genética , Glicosídeo Hidrolases/metabolismo , Metagenoma/genética , Metagenômica , Filogenia , Análise de Sequência de DNA , Simbiose , Xilanos/metabolismo , Xilosidases/classificação , Xilosidases/genética , Xilosidases/metabolismoRESUMO
Phylosymbiosis was recently proposed to describe the eco-evolutionary pattern whereby the ecological relatedness (e.g., beta diversity relationships) of host-associated microbial communities parallels the phylogeny of the host species. Representing the most abundant biological entities on the planet and common members of the animal-associated microbiome, viruses can be influential members of host-associated microbial communities that may recapitulate, reinforce, or ablate phylosymbiosis. Here we sequence the metagenomes of purified viral communities from three different parasitic wasp Nasonia species, one cytonuclear introgression line of Nasonia, and the flour moth outgroup Ephestia kuehniella. Results demonstrate complete phylosymbiosis between the viral metagenome and insect phylogeny. Across all Nasonia contigs, 69% of the genes in the viral metagenomes are either new to the databases or uncharacterized, yet over 99% of the contigs have at least one gene with similarity to a known sequence. The core Nasonia virome spans 21% of the total contigs, and the majority of that core is likely derived from induced prophages residing in the genomes of common Nasonia-associated bacterial genera: Proteus, Providencia, and Morganella. We also assemble the first complete viral particle genomes from Nasonia-associated gut bacteria. Taken together, results reveal the first complete evidence for phylosymbiosis in viral metagenomes, new genome sequences of viral particles from Nasonia-associated gut bacteria, and a large set of novel or uncharacterized genes in the Nasonia virome. This work suggests that phylosymbiosis at the host-microbiome level will likely extend to the host-virome level in other systems as well. IMPORTANCE Viruses are the most abundant biological entity on the planet and interact with microbial communities with which they associate. The virome of animals is often dominated by bacterial viruses, known as bacteriophages or phages, which can (re)structure bacterial communities potentially vital to the animal host. Beta diversity relationships of animal-associated bacterial communities in laboratory and wild populations frequently parallel animal phylogenetic relationships, a pattern termed phylosymbiosis. However, little is known about whether viral communities also exhibit this eco-evolutionary pattern. Metagenomics of purified viruses from recently diverged species of Nasonia parasitoid wasps reared in the lab indicates for the first time that the community relationships of the virome can also exhibit complete phylosymbiosis. Therefore, viruses, particularly bacteriophages here, may also be influenced by animal evolutionary changes either directly or indirectly through the tripartite interactions among hosts, bacteria, and phage communities. Moreover, we report several new bacteriophage genomes from the common gut bacteria in Nasonia.
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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.
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Baratas/microbiologia , Fungos , Microbioma Gastrointestinal , Trato Gastrointestinal/microbiologia , Isópteros/microbiologia , Animais , DietaRESUMO
Bacteria of the class Endomicrobia form a deep-branching clade in the Elusimicrobia phylum. They are found almost exclusively in the intestinal tract of animals and are particularly abundant in many termites, where they reside as intracellular symbionts in the cellulolytic gut flagellates. Although small populations of putatively free-living lineages have been detected in faunated and flagellate-free hosts, the evolutionary origin of the endosymbionts is obscured by the limited amount of phylogenetic information provided by the 16S rRNA gene fragment amplified with Endomicrobia-specific primers. Here, we present a robust phylogenetic framework based on the near-full-length 16S-23S rRNA gene region of a diverse set of Endomicrobia from termites and cockroaches, which also allowed us to classify the shorter reads from previous studies. Our data revealed that endosymbionts arose independently at least four times from different free-living lineages, which were already present in ancestral cockroaches but became associated with their respective hosts long after the digestive symbiosis between termites and flagellates had been established. Pyrotag sequencing revealed that the proportion of putatively free-living lineages increased, when all flagellates and their symbionts were removed from the gut of lower termites by starvation, starch feeding or hyperbaric oxygen, but results varied between different methods.
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Microbioma Gastrointestinal , Metagenoma , Metagenômica , Filogenia , Simbiose , Animais , Bactérias/classificação , Bactérias/genética , DNA Intergênico , Insetos/microbiologia , Metagenômica/métodos , RNA Ribossômico 16S/genética , RNA Ribossômico 23S/genéticaRESUMO
Symbiotic digestion of lignocellulose in higher termites (family Termitidae) is accomplished by an exclusively prokaryotic gut microbiota. By deep sequencing of amplified 16S rRNA genes, we had identified diet as the primary determinant of bacterial community structure in a broad selection of termites specialized on lignocellulose in different stages of humification. Here, we increased the resolution of our approach to account for the pronounced heterogeneity in microenvironmental conditions and microbial activities in the major hindgut compartments. The community structure of consecutive gut compartments in each species strongly differed, but that of homologous compartments clearly converged, even among unrelated termites. While the alkaline P1 compartments of all termites investigated contained specific lineages of Clostridiales, the posterior hindgut compartments (P3, P4) differed between feeding groups and were predominantly colonized by putatively fiber-associated lineages of Spirochaetes, Fibrobacteres and the TG3 phylum (wood and grass feeders) or diverse assemblages of Clostridiales and Bacteroidetes (humus and soil feeders). The results underscore that bacterial community structure in termite guts is driven by microenvironmental factors, such as pH, available substrates and gradients of O2 and H2, and inspire investigations on the functional roles of specific bacterial taxa in lignocellulose and humus digestion.
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Bactérias/isolamento & purificação , Microbioma Gastrointestinal , Isópteros/microbiologia , Madeira/microbiologia , Animais , Bactérias/classificação , Bactérias/genética , Bactérias/metabolismo , Sistema Digestório/microbiologia , Comportamento Alimentar , Sequenciamento de Nucleotídeos em Larga Escala , Isópteros/fisiologia , Lignina/metabolismo , Filogenia , Análise de Sequência de DNA , Solo/químicaRESUMO
The flagellate protists in the hindgut of lower termites play an essential role in the digestion of lignocellulose. Most flagellate species are associated with host-specific symbionts from various bacterial lineages, which typically lack cultured representatives. In this study, we analyzed the genome of 'Candidatus Ancillula trichonymphae', an endosymbiont of Trichonympha flagellates from dry-wood termites, which represents a novel, family-level lineage of uncultured Actinobacteria encountered so far only in termite guts. The draft genome of 'Ca. A. trichonymphae' (ca. 1.48 Mbp; 95% complete) revealed a purely fermentative metabolism that is probably fueled by xylose, N-acetyl-glucosamine and glycerol 3-phosphate acquired from the flagellate host. The absence of fructose bisphosphate aldolase and the presence of a complete gene set encoding the phosphoketolase pathway underscore the sister position of the new lineage to Bifidobacteriaceae. The preservation of the pathways for the assimilation of ammonia and the synthesis of 18 amino acids and several cofactors and vitamins suggests that 'Ca. A. trichonymphae' - like other endosymbionts of termite gut flagellates - provides essential amino acids and vitamins to its host. Our findings corroborate the emerging concept that numerous lineages of unrelated flagellate endosymbionts have convergently evolved to fill similar ecological niches.
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Termite gut flagellates are typically colonized by specific bacterial symbionts. Here we describe the phylogeny, ultrastructure and subcellular location of 'Candidatus Adiutrix intracellularis', an intracellular symbiont of Trichonympha collaris in the termite Zootermopsis nevadensis. It represents a novel, deep-branching clade of uncultured Deltaproteobacteria widely distributed in intestinal tracts of termites and cockroaches. Fluorescence in situ hybridization and transmission electron microscopy localized the endosymbiont near hydrogenosomes in the posterior part and near the ectosymbiont 'Candidatus Desulfovibrio trichonymphae' in the anterior part of the host cell. The draft genome of 'Ca. Adiutrix intracellularis' obtained from a metagenomic library revealed the presence of a complete gene set encoding the Wood-Ljungdahl pathway, including two homologs of fdhF encoding hydrogenase-linked formate dehydrogenases (FDHH ) and all other components of the recently described hydrogen-dependent carbon dioxide reductase (HDCR) complex, which substantiates previous claims that the symbiont is capable of reductive acetogenesis from CO2 and H2 . The close phylogenetic relationship between the HDCR components and their homologs in homoacetogenic Firmicutes and Spirochaetes suggests that the deltaproteobacterium acquired the capacity for homoacetogenesis via lateral gene transfer. The presence of genes for nitrogen fixation and the biosynthesis of amino acids and cofactors indicate the nutritional nature of the symbiosis.
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Deltaproteobacteria/classificação , Deltaproteobacteria/isolamento & purificação , Hypermastigia/microbiologia , Intestinos/microbiologia , Isópteros/parasitologia , Animais , Deltaproteobacteria/genética , Desulfovibrio/genética , Formiato Desidrogenases/genética , Transferência Genética Horizontal/genética , Hibridização in Situ Fluorescente , Fixação de Nitrogênio/genética , Filogenia , SimbioseRESUMO
Fungus-cultivating termites (Macrotermitinae) possess an elaborate strategy of lignocellulose digestion. It involves a lignocellulose-degrading fungal symbiont (genus Termitomyces), a diverse gut microbiota and a characteristic labour division in food processing. In this study, using pyrotag sequencing and electron microscopy, we analysed the bacterial microbiota in the hindgut of Odontotermes formosanus and its fungus comb to investigate the spatial organization, establishment and temporal succession of the bacterial communities colonizing specific microhabitats. Our results document strong differences between the communities at the hindgut epithelium and the luminal fluid of newly moulted, young and old worker termites. The differences in community structure were consistent with the density, morphology and spatial distribution of bacterial cells and the pools of microbial metabolites in the hindgut compartment, underlining that both gut development and the age-specific changes in diet affect the composition and functional role of their gut microbiota. These findings provide strong support for the concept that changes in diet and gut environment are important determinants of community structure because they create new niches for microbial symbionts.
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Envelhecimento/fisiologia , Bactérias/classificação , Sistema Digestório/microbiologia , Microbioma Gastrointestinal/fisiologia , Isópteros/microbiologia , Animais , Fungos/classificação , Isópteros/fisiologiaRESUMO
The gut microbiota of termites plays important roles in the symbiotic digestion of lignocellulose. However, the factors shaping the microbial community structure remain poorly understood. Because termites cannot be raised under axenic conditions, we established the closely related cockroach Shelfordella lateralis as a germ-free model to study microbial community assembly and host-microbe interactions. In this study, we determined the composition of the bacterial assemblages in cockroaches inoculated with the gut microbiota of termites and mice using pyrosequencing analysis of their 16S rRNA genes. Although the composition of the xenobiotic communities was influenced by the lineages present in the foreign inocula, their structure resembled that of conventional cockroaches. Bacterial taxa abundant in conventional cockroaches but rare in the foreign inocula, such as Dysgonomonas and Parabacteroides spp., were selectively enriched in the xenobiotic communities. Donor-specific taxa, such as endomicrobia or spirochete lineages restricted to the gut microbiota of termites, however, either were unable to colonize germ-free cockroaches or formed only small populations. The exposure of xenobiotic cockroaches to conventional adults restored their normal microbiota, which indicated that autochthonous lineages outcompete foreign ones. Our results provide experimental proof that the assembly of a complex gut microbiota in insects is deterministic.