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

Research Group Insect Gut Microbiology and Symbiosis, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
Laboratory of Experimental and Comparative Ethology EA 4443, Université Paris 13, Villetaneuse, France
Faculty of Forestry and Wood Sciences, Czech University of Life Sciences, Prague, Czech Republic
DOI
10.7287/peerj.preprints.27929v1
Subject Areas
Bioinformatics, Ecology, Genomics, Microbiology
Keywords
metagenome-assembled genomes, gut microbiology, higher termites, bacteria, archaea, phylogenomics, metagenomics
Copyright
© 2019 Hervé et al.
Licence
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ Preprints) and either DOI or URL of the article must be cited.
Cite this article
Hervé V, Liu P, Dietrich C, Sillam-Dussès D, Stiblik P, Šobotník J, Brune A. 2019. Phylogenomic analysis of 589 metagenome-assembled genomes encompassing all major prokaryotic lineages from the gut of higher termites. PeerJ Preprints 7:e27929v1

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, 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.

Author Comment

This is a submission to PeerJ for review.

Supplemental Information

Phylogenomic distribution of the MAGs according to the host diet

The outer rings show the occurrence of MAGs in termites with different diets. The maximum likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I model of amino-acid evolution.

DOI: 10.7287/peerj.preprints.27929v1/supp-1

Phylogenomic distribution of the MAGs according to the gut compartment of the host

The outer rings show the occurrence of MAGs in the different termite gut compartments: C crop (foregut), M midgut, P1–P5 proctodeal compartments (hindgut). The maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I model of amino-acid evolution.

DOI: 10.7287/peerj.preprints.27929v1/supp-2

Phylogenomic tree of the Archaea

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I+F model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Asgard group was used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-3

Phylogenomic tree of the Ruminococcaceae family (Firmicutes)

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Dorea and Butyrivibrio (Lachnospiraceae) species were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-4

Phylogenomic tree of the Actinobacteria

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I+F model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Chloroflexi species were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-5

Phylogenomic tree of the Spirochaetes

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I+F model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Elusimicrobia and Cyanobacteria were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-6

Phylogenomic tree of the Fibrobacteres

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I+F model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Bacteroidetes were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-7

Phylogenomic tree of the Desulfovibrionaceae family (Deltaproteobacteria)

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Desulfonatronum species were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-8

Phylogenomic tree of the Bacteroidetes

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Chlorobi species were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-9

Phylogenomic tree of the Chloroflexi, Saccharibacteria and Microgenomates

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I+F model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Actinobacteria species were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-10

Phylogenomic tree of the Synergistetes

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I+F model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Elusimicrobia species were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-11

Phylogenomic tree of the Planctomycetes

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I+F model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Verrucomicrobia species were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-12

Phylogenomic tree of the Elusimicrobia

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I+F model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Spirochaetes species were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-13

Phylogenomic tree of the Cloacimonetes

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I+F model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Fibrobacteres species were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-14

Phylogenomic tree of the Kiritimatiellaeota

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Chlamydiae species were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-15

Phylogenomic tree of the Acidobacteria

This maximum-likelihood tree was inferred from a concatenated alignment of 43 proteins using the LG+G+I+F model of amino-acid evolution. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test. Proteobacteria species were used as outgroup. Names in bold included MAGs recovered in the present study.

DOI: 10.7287/peerj.preprints.27929v1/supp-16

Final taxonomic assignment and characteristics of the MAGs

DOI: 10.7287/peerj.preprints.27929v1/supp-18

Initial taxonomic assignment of the MAGs

DOI: 10.7287/peerj.preprints.27929v1/supp-19