Phylogenetic diversity of Archaea in the intestinal tract of termites from different lineages

Brune

2020

Preprint

Symbiotic digestion of lignocellulose in the hindgut of higher termites is mediated by a diverse assemblage of bacteria and archaea. During a large-scale metagenomic study, we reconstructed 15 metagenome-assembled genomes (MAGs) of Bathyarchaeia that represent two distinct lineages in subgroup 6 (formerly MCG-6) unique to termite guts. One lineage (TB2; Candidatus Termitimicrobium) encodes all enzymes required for reductive acetogenesis from H2 and CO2 via an archaeal variant of the Wood–Ljungdahl pathway. This includes a novel 11-subunit hydrogenase, which possesses the genomic architecture of the respiratory Fpo-complex of other archaea but whose catalytic subunit is phylogenetically related to and shares the conserved [NiFe] cofactor-binding motif with [NiFe] hydrogenases of subgroup 4g. We propose that this novel Fpo-like hydrogenase provides the reduced ferredoxin required for CO2 reduction and is driven by the electrochemical membrane potential generated from the ATP conserved by substrate-level phosphorylation. Members of the other lineage (TB1; Candidatus Termiticorpusculum) are not capable of lithotrophic acetogenesis because they consistently lack hydrogenases and/or methylene-tetrahydromethanopterin reductase, a key enzyme of the pathway. Both lineages have the genomic capacity to reduce ferredoxin by oxidizing amino acids and might conduct methylotrophic acetogenesis using unidentified methylated compound(s). Our results indicate that Bathyarchaeia of subgroup 6 contribute to acetate formation in the guts of higher termites and substantiate the genomic evidence for reductive acetogenesis from organic substrates, including methylated compounds, in other uncultured representatives of the phylum.

Section: Resultsmentioning

confidence: 99%

Metabolic potential for reductive acetogenesis and a novel energy-converting [NiFe] hydrogenase inBathyarchaeiafrom termite guts – a genome-centric analysis

Loh

Brune

2020

Preprint

“…Several bacterial phyla and one archaeal phylum containing prominent taxa that have been identified in previous 16S rRNA gene surveys of termite guts were not represented among the MAGs recovered in the present study. They include Cyanobacteria (class Melainabacteria; Utami et al, 2018), Lentisphaerae (Köhler et al, 2012;Sabree & Moran, 2014), Verrucomicrobia (Wertz et al, 2012), and Thaumarchaeota (Friedrich et al, 2001;Shi et al, 2015). Also intracellular symbionts of termite tissues, such as Wolbachia (Proteobacteria) (Diouf et al, 2018b) were not recovered.…”

Section: Phyla Not Represented By Magsmentioning

confidence: 99%

Phylogenomic analysis of 589 metagenome-assembled genomes encompassing all major prokaryotic lineages from the gut of higher termites

Liu

Dietrich

et al. 2020

PeerJ

“Higher” termites have been able to colonize all tropical and subtropical regions because of their ability to digest lignocellulose with the aid of their prokaryotic gut microbiota. Over the last decade, numerous studies based on 16S rRNA gene amplicon libraries have largely described both the taxonomy and structure of the prokaryotic communities associated with termite guts. Host diet and microenvironmental conditions have emerged as the main factors structuring the microbial assemblages in the different gut compartments. Additionally, these molecular inventories have revealed the existence of termite-specific clusters that indicate coevolutionary processes in numerous prokaryotic lineages. However, for lack of representative isolates, the functional role of most lineages remains unclear. We reconstructed 589 metagenome-assembled genomes (MAGs) from the different gut compartments of eight higher termite species that encompass 17 prokaryotic phyla. By iteratively building genome trees for each clade, we significantly improved the initial automated assignment, frequently up to the genus level. We recovered MAGs from most of the termite-specific clusters in the radiation of, for example, Planctomycetes, Fibrobacteres, Bacteroidetes, Euryarchaeota, Bathyarchaeota, Spirochaetes, Saccharibacteria, and Firmicutes, which to date contained only few or no representative genomes. Moreover, the MAGs included abundant members of the termite gut microbiota. This dataset represents the largest genomic resource for arthropod-associated microorganisms available to date and contributes substantially to populating the tree of life. More importantly, it provides a backbone for studying the metabolic potential of the termite gut microbiota, including the key members involved in carbon and nitrogen biogeochemical cycles, and important clues that may help cultivating representatives of these understudied clades.

Section: Phyla Not Represented By Magsmentioning

confidence: 99%

Phylogenomic analysis of 589 metagenome-assembled genomes encompassing all major prokaryotic lineages from the gut of higher termites

Liu

Dietrich

et al. 2019

Preprint

“Higher” termites have been able to colonize all tropical and subtropical regions because of their ability to digest lignocellulose with the aid of their prokaryotic gut microbiota. Over the last decade, numerous studies based on 16S rRNA gene amplicon libraries have largely described both the taxonomy and structure of the prokaryotic communities associated with termite guts. Host diet and microenvironmental conditions have emerged as the main factors structuring the microbial assemblages in the different gut compartments. Additionally, these molecular inventories have revealed the existence of termite-specific clusters that indicate coevolutionary processes in numerous prokaryotic lineages. However, for lack of representative isolates, the functional role of most lineages remains unclear. We reconstructed 589 metagenome-assembled genomes (MAGs) from the different gut compartments of eight higher termite species that encompass 17 prokaryotic phyla. By iteratively building genome trees for each clade, we significantly improved the initial automated assignment, frequently up to the genus level. We recovered MAGs from most of the termite-specific clusters in the radiation of, e.g., Planctomycetes, Fibrobacteres, Bacteroidetes, Euryarchaeota, Bathyarchaeota, Spirochaetes, Saccharibacteria, and Firmicutes, which to date contained only few or no representative genomes. Moreover, the MAGs included abundant members of the termite gut microbiota. This dataset represents the largest genomic resource for arthropod-associated microorganisms available to date and contributes substantially to populating the tree of life. More importantly, it provides a backbone for studying the metabolic potential of the termite gut microbiota, including the key members involved in carbon and nitrogen biogeochemical cycles, and important clues that may help cultivating representatives of these understudied clades.