Nejvíce citovaný článek - PubMed ID 32095380
Phylogenomic analysis of 589 metagenome-assembled genomes encompassing all major prokaryotic lineages from the gut of higher termites
Bacterial endosymbionts of eukaryotic hosts typically experience massive genome reduction, but the underlying evolutionary processes are often obscured by the lack of free-living relatives. Endomicrobia, a family-level lineage of host-associated bacteria in the phylum Elusimicrobiota that comprises both free-living representatives and endosymbionts of termite gut flagellates, are an excellent model to study evolution of intracellular symbionts. We reconstructed 67 metagenome-assembled genomes (MAGs) of Endomicrobiaceae among more than 1,700 MAGs from the gut microbiota of a wide range of termites. Phylogenomic analysis confirmed a sister position of representatives from termites and ruminants, and allowed to propose eight new genera in the radiation of Endomicrobiaceae. Comparative genome analysis documented progressive genome erosion in the new genus Endomicrobiellum, which comprises all flagellate endosymbionts characterized to date. Massive gene losses were accompanied by the acquisition of new functions by horizontal gene transfer, which led to a shift from a glucose-based energy metabolism to one based on sugar phosphates. The breakdown of glycolysis and many anabolic pathways for amino acids and cofactors in several subgroups was compensated by the independent acquisition of new uptake systems, including an ATP/ADP antiporter, from other gut microbiota. The putative donors are mostly flagellate endosymbionts from other bacterial phyla, including several, hitherto unknown lineages of uncultured Alphaproteobacteria, documenting the importance of horizontal gene transfer in the convergent evolution of these intracellular symbioses. The loss of almost all biosynthetic capacities in some lineages of Endomicrobiellum suggests that their originally mutualistic relationship with flagellates is on its decline.IMPORTANCEUnicellular eukaryotes are frequently colonized by bacterial and archaeal symbionts. A prominent example are the cellulolytic gut flagellates of termites, which harbor diverse but host-specific bacterial symbionts that occur exclusively in termite guts. One of these lineages, the so-called Endomicrobia, comprises both free-living and endosymbiotic representatives, which offers the unique opportunity to study the evolutionary processes underpinning the transition from a free-living to an intracellular lifestyle. Our results revealed a progressive gene loss in energy metabolism and biosynthetic pathways, compensated by the acquisition of new functions via horizontal gene transfer from other gut bacteria, and suggest the eventual breakdown of an initially mutualistic symbiosis. Evidence for convergent evolution of unrelated endosymbionts reflects adaptations to the intracellular environment of termite gut flagellates.
- Klíčová slova
- Endomicrobiaceae, Parabasalia, convergent evolution, endosymbionts, lateral gene transfer, termites,
- MeSH
- Bacteria * genetika klasifikace MeSH
- fylogeneze * MeSH
- genom bakteriální * MeSH
- Isoptera * mikrobiologie parazitologie MeSH
- metagenom MeSH
- molekulární evoluce MeSH
- přenos genů horizontální * MeSH
- střevní mikroflóra * MeSH
- symbióza * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Methane emission by terrestrial invertebrates is restricted to millipedes, termites, cockroaches, and scarab beetles. The arthropod-associated archaea known to date belong to the orders Methanobacteriales, Methanomassiliicoccales, Methanomicrobiales, and Methanosarcinales, and in a few cases also to non-methanogenic Nitrososphaerales and Bathyarchaeales. However, all major host groups are severely undersampled, and the taxonomy of existing lineages is not well developed. Full-length 16S rRNA gene sequences and genomes of arthropod-associated archaea are scarce, reference databases lack resolution, and the names of many taxa are either not validly published or under-classified and require revision. Here, we investigated the diversity of archaea in a wide range of methane-emitting arthropods, combining phylogenomic analysis of isolates and metagenome-assembled genomes (MAGs) with amplicon sequencing of full-length 16S rRNA genes. Our results allowed us to describe numerous new species in hitherto undescribed taxa among the orders Methanobacteriales (Methanacia, Methanarmilla, Methanobaculum, Methanobinarius, Methanocatella, Methanoflexus, Methanorudis, and Methanovirga, all gen. nova), Methanomicrobiales (Methanofilum and Methanorbis, both gen. nova), Methanosarcinales (Methanofrustulum and Methanolapillus, both gen. nova), Methanomassiliicoccales (Methanomethylophilaceae fam. nov., Methanarcanum, Methanogranum, Methanomethylophilus, Methanomicula, Methanoplasma, Methanoprimaticola, all gen. nova), and the new family Bathycorpusculaceae (Bathycorpusculum gen. nov.). Reclassification of amplicon libraries from this and previous studies using this new taxonomic framework revealed that arthropods harbor only CO2 and methyl-reducing hydrogenotrophic methanogens. Numerous genus-level lineages appear to be present exclusively in arthropods, suggesting long evolutionary trajectories with their termite, cockroach, and millipede hosts, and a radiation into various microhabitats and ecological niches provided by their digestive tracts (e.g., hindgut compartments, gut wall, or anaerobic protists). The distribution patterns among the different host groups are often complex, indicating a mixed mode of transmission and a parallel evolution of invertebrate and vertebrate-associated lineages.
- Klíčová slova
- Bathyarchaeia, Nitrososphaerales, archaea, cockroaches, gut microbiota, methanogens, millipedes, termites,
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Termites primarily feed on lignocellulose or soil in association with specific gut microbes. The functioning of the termite gut microbiota is partly understood in a handful of wood-feeding pest species but remains largely unknown in other taxa. We intend to fill this gap and provide a global understanding of the functional evolution of termite gut microbiota. RESULTS: We sequenced the gut metagenomes of 145 samples representative of the termite diversity. We show that the prokaryotic fraction of the gut microbiota of all termites possesses similar genes for carbohydrate and nitrogen metabolisms, in proportions varying with termite phylogenetic position and diet. The presence of a conserved set of gut prokaryotic genes implies that essential nutritional functions were present in the ancestor of modern termites. Furthermore, the abundance of these genes largely correlated with the host phylogeny. Finally, we found that the adaptation to a diet of soil by some termite lineages was accompanied by a change in the stoichiometry of genes involved in important nutritional functions rather than by the acquisition of new genes and pathways. CONCLUSIONS: Our results reveal that the composition and function of termite gut prokaryotic communities have been remarkably conserved since termites first appeared ~ 150 million years ago. Therefore, the "world's smallest bioreactor" has been operating as a multipartite symbiosis composed of termites, archaea, bacteria, and cellulolytic flagellates since its inception. Video Abstract.
- Klíčová slova
- Endosymbionts, Isoptera, Metagenomics, Vertical inheritance,
- MeSH
- fylogeneze MeSH
- Isoptera * MeSH
- metagenom MeSH
- půda MeSH
- střevní mikroflóra * genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- audiovizuální média MeSH
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- půda MeSH
Deadwood represents significant carbon (C) stock in a temperate forests. Its decomposition and C mobilization is accomplished by decomposer microorganisms - fungi and bacteria - who also supply the foodweb of commensalist microbes. Due to the ecosystem-level importance of deadwood habitat as a C and nutrient stock with significant nitrogen fixation, the deadwood microbiome composition and function are critical to understanding the microbial processes related to its decomposition. We present a comprehensive suite of data packages obtained through environmental DNA and RNA sequencing from natural deadwood. Data provide a complex picture of the composition and function of microbiome on decomposing trunks of European beech (Fagus sylvatica L.) in a natural forest. Packages include deadwood metagenomes, metatranscriptomes, sequences of total RNA, bacterial genomes resolved from metagenomic data and the 16S rRNA gene and ITS2 metabarcoding markers to characterize the bacterial and fungal communities. This project will be of use to microbiologists, environmental biologists and biogeochemists interested in the microbial processes associated with the transformation of recalcitrant plant biomass.
- MeSH
- Bacteria klasifikace MeSH
- buk (rod) mikrobiologie MeSH
- dřevo mikrobiologie MeSH
- ekosystém MeSH
- houby klasifikace MeSH
- lesy MeSH
- metagenom * MeSH
- mezerníky ribozomální DNA genetika MeSH
- mikrobiota * MeSH
- RNA ribozomální 16S genetika MeSH
- stromy mikrobiologie MeSH
- taxonomické DNA čárové kódování MeSH
- Publikační typ
- časopisecké články MeSH
- dataset MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Česká republika MeSH
- Názvy látek
- mezerníky ribozomální DNA MeSH
- RNA ribozomální 16S MeSH