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

Abstract

“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.

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

“…0.69%) is four times higher than that assigned to euryarchaeal MAGs (0.02–0.79%; avg. 0.16%; Table S2 in Hervé et al ., 2020), the population sizes of Bathyarchaeia might be sufficient to contribute significantly to acetogenesis, particularly in soil-feeding species.…”

“…SSU rRNA gene sequences in the MAGs and other bathyarchaeotal bins obtained from the original metagenomes (Hervé et al ., 2020) were identified using the ssu_finder function implemented in CheckM. Sequences were imported into the alignment of rRNA gene sequences in the SILVA SSURef NR database release 132 (https://www.arb-silva.de; Quast et al, 2013) using Arb v6.0.6 (Ludwig et al ., 2004).…”

“…16S rRNA-based phylogeny of subgroup Bathy-6, indicating the placement of the sequences from termite guts among those obtained from other environments. The maximum-likelihood tree is based on a curated alignment (1,424 positions) of all sequences in the SILVA database and their homologs retrieved from the bathyarchaeal MAGs (in bold) and the low-quality bins obtained from the termite gut metagenomes (Hervé et al ., 2020). The tree was rooted using members of Bathy-5 as outgroup.…”

“…Supplementary Table S1 . Taxonomic assignment and characteristics of the bathyarchaeotal MAGs from termite guts (from Hervé et al ., 2020).…”

“…In a large-scale metagenomic study of the gut microbiota of eight higher termites, we obtained 15 metagenome-assembled genomes (MAGs) assigned to Bathyarchaeia (Hervé et al ., 2020). Preliminary analysis revealed that they fell into a cluster comprising mainly termite gut MAGs, with members of Bathy-1 and Bathy-6 as next relatives.…”