Diversity and taxonomic revision of methanogens and other archaea in the intestinal tract of terrestrial arthropods

Protasov, Evgenii; Nonoh, James O.; Kästle Silva, Joana M.; Mies, Undine S.; Hervé, Vincent; Dietrich, Carsten; Lang, Kristina; Mikulski, Lena; Platt, Katja; Poehlein, Anja; Köhler-Ramm, Tim; Miambi, Edouard; Boga, Hamadi I.; Feldewert, Christopher; Ngugi, David K.; Plarre, Rudy; Sillam-Dussès, David; Šobotník, Jan; Daniel, Rolf; Brune, Andreas

doi:10.3389/fmicb.2023.1281628

Cited by 5 publications

(7 citation statements)

References 119 publications

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“…Together with the 589 MAGs from our previous study ( 30 ), they comprise 2,228 MAGs from the bacterial domain and 84 MAGs from the archaeal domain. The archaeal MAGs comprised members of the euryarchaeal phyla Thermoplasmatota (33 MAGs), Methanobacteriota (15 MAGs), and Halobacterota (10 MAGs), and the crenarchaeal phylum Thermoproteota (26 MAGs); these have been covered in a separate study ( 36 ). The bacterial MAGs were classified into 30 phyla.…”

Section: Resultsmentioning

confidence: 99%

Genome reduction and horizontal gene transfer in the evolution of Endomicrobia—rise and fall of an intracellular symbiosis with termite gut flagellates

Mies,

Hervé,

Kropp

et al. 2024

mBio

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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. IMPORTANCE Unicellular 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.

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Section: Resultsmentioning

confidence: 99%

Genome reduction and horizontal gene transfer in the evolution of Endomicrobia—rise and fall of an intracellular symbiosis with termite gut flagellates

Mies,

Hervé,

Kropp

et al. 2024

mBio

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“…The assignment is based on the 16S rRNA gene (LC802674). The draft genome sequence CfCl-M3 showed 96.2% average nucleotide identity to Methanovirga procula, which has been named under SeqCode on the basis of a MAG (GCA_031280375) obtained from the gut of Prorhinotermes canalifrons [5].…”

Section: Discussionmentioning

confidence: 99%

Facultative endosymbiosis between cellulolytic protists and methanogenic archaea in the gut of the Formosan termiteCoptotermes formosanus

Kaneko,

Omori,

Igai

et al. 2024

Preprint

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Anaerobic protists frequently harbour methanogenic archaea, which apparently contribute to the hosts' fermentative metabolism by consuming excess H2. However, the ecological properties of endosymbiotic methanogens remain elusive in many cases. Here we investigated the ecology and genome of the endosymbiotic methanogen of the cellulolytic Cononympha protists in the hindgut of the Formosan termite Coptotermes formosanus. Microscopic and 16S rRNA amplicon sequencing analyses revealed that a single species, designated here 'Candidatus Methanobrevibacter cononymphae', is associated with both Cononympha leidyi and Cononympha koidzumii and that its infection rate in Cononympha cells greatly varied from 0.0 to 99.8% among termite colonies. Fine-scale network analysis indicated that multiple 16S rRNA sequence variants coexisted within a single host cell and that identical variants were present in both Cononympha species and also on the gut wall; 'Ca. Methanobrevibacter cononymphae' is facultatively associated with Cononympha and horizontally taken up. Indeed, transmission electron microscopy showed escape or uptake of methanogens from/by a Cononympha cell. The genome of 'Ca. Methanobrevibacter cononymphae' showed features consistent with its facultative lifestyle: i.e., the genome size (2.7 Mbp) comparable to those of free-living relatives; the pseudogenization of the formate dehydrogenase gene fdhA, unnecessary within the non-formate-producing host cell; the dependence on acetate as an essential carbon source, which is abundant within the host cell; and the presence of a catalase gene, required for colonization on the microoxic gut wall. Our study revealed a versatile endosymbiosis between the methanogen and protists, which may be a strategy responding to changing conditions in the termite gut.

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“…To construct a phylogenomic tree, we retrieved genome sequences of Methanobacteriaceae as references from GTDB r202 [ 52 ] and metagenome-assembled genomes (MAGs) assigned to Methanobacteriaceae recently obtained from termite guts [ 5 , 53 ]. Gene prediction, extraction, and alignment are described in Supplemental Methods.…”

Section: Methodsmentioning

confidence: 99%

“…In the guts of termites, for example, which are keystone animals in the terrestrial carbon cycle, methanogens accounted for 0%–10% of the prokaryotic gut community and possibly produce 1%–3% of the global methane [ 2 , 3 ]. Methanogens are present in the guts of diverse termite lineages [ 4 , 5 ] and are considered to contribute to the gut ecosystem as H 2 -sinks by producing methane from H 2 and CO 2 [ 6 , 7 ]. Methanogens are found on the hindgut epithelium [ 4 , 8 , 9 ] or within the cells of certain gut protist species [ 10 ].…”

Section: Introductionmentioning

confidence: 99%

Facultative endosymbiosis between cellulolytic protists and methanogenic archaea in the gut of the Formosan termite Coptotermes formosanus

Kaneko,

Omori,

Igai

et al. 2024

ISME Communications

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Anaerobic protists frequently harbour methanogenic archaea, which apparently contribute to the hosts’ fermentative metabolism by consuming excess H2. However, the ecological properties of endosymbiotic methanogens remain elusive in many cases. Here we investigated the ecology and genome of the endosymbiotic methanogen of the Cononympha protists in the hindgut of the termite Coptotermes formosanus. Microscopic and 16S rRNA amplicon sequencing analyses revealed that a single species, designated here “Candidatus Methanobrevibacter cononymphae”, is associated with both Cononympha leidyi and Cononympha koidzumii and that its infection rate in Cononympha cells varied from 0.0 to 99.8% among termite colonies. Fine-scale network analysis indicated that multiple 16S rRNA sequence variants coexisted within a single host cell and that identical variants were present in both Cononympha species and also on the gut wall. Thus, “Ca. Methanobrevibacter cononymphae” is a facultative endosymbiont, transmitted vertically with frequent exchanges with the gut environment. Indeed, transmission electron microscopy showed escape or uptake of methanogens from/by a Cononympha cell. The genome of “Ca. Methanobrevibacter cononymphae” showed features consistent with its facultative lifestyle: i.e., the genome size (2.7 Mbp) comparable to those of free-living relatives; the pseudogenization of the formate dehydrogenase gene fdhA, unnecessary within the non-formate-producing host cell; the dependence on abundant acetate in the host cell as an essential carbon source; and the presence of a catalase gene, required for colonization on the microoxic gut wall. Our study revealed a versatile endosymbiosis between the methanogen and protists, which may be a strategy responding to changing conditions in the termite gut.

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Diversity and taxonomic revision of methanogens and other archaea in the intestinal tract of terrestrial arthropods

Cited by 5 publications

References 119 publications

Genome reduction and horizontal gene transfer in the evolution of Endomicrobia—rise and fall of an intracellular symbiosis with termite gut flagellates

Genome reduction and horizontal gene transfer in the evolution of Endomicrobia—rise and fall of an intracellular symbiosis with termite gut flagellates

Facultative endosymbiosis between cellulolytic protists and methanogenic archaea in the gut of the Formosan termiteCoptotermes formosanus

Facultative endosymbiosis between cellulolytic protists and methanogenic archaea in the gut of the Formosan termite Coptotermes formosanus

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