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SCIENCE CHINA Life Sciences, Volume 63 , Issue 6 : 886-897(2020) https://doi.org/10.1007/s11427-020-1679-1

Diverse Asgard archaea including the novel phylum Gerdarchaeota participate in organic matter degradation

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  • ReceivedFeb 27, 2020
  • AcceptedMar 12, 2020
  • PublishedMar 16, 2020

Abstract

Asgard is an archaeal superphylum that might hold the key to understand the origin of eukaryotes, but its diversity and ecological roles remain poorly understood. Here, we reconstructed 15 metagenomic-assembled genomes from coastal sediments covering most known Asgard archaea and a novel group, which is proposed as a new Asgard phylum named as the “Gerdarchaeota”. Genomic analyses predict that Gerdarchaeota are facultative anaerobes in utilizing both organic and inorganic carbon. Unlike their closest relatives Heimdallarchaeota, Gerdarchaeota have genes encoding for cellulase and enzymes involved in the tetrahydromethanopterin-based Wood–Ljungdahl pathway. Transcriptomics showed that most of our identified Asgard archaea are capable of degrading organic matter, including peptides, amino acids and fatty acids, occupying ecological niches in different depths of layers of the sediments. Overall, this study broadens the diversity of the mysterious Asgard archaea and provides evidence for their ecological roles in coastal sediments.


Acknowledgment

We thank Dr. Nidhi Singh for her suggestions in molecular modeling. We thank the captain, crew and scientists of R/V HEINCKE expeditions HE443. This research was financed by the National Natural Science Foundation of China (91851105, 31622002, 31970105, 31600093, and 31700430), the Shenzhen Science and Technology Program (JCYJ20170818091727570 and KQTD20180412181334790), the Key Project of Department of Education of Guangdong Province (2017KZDXM071), the China Postdoctoral Science Foundation (2018M633111), the DFG (Deutsche Forschungsgemeinschaft) Cluster of Excellence EXC 309 “The Ocean in the Earth System - MARUM - Center for Marine Environmental Sciences” (project ID 49926684) and the University of Bremen.


Interest statement

The author(s) declare that they have no conflict of interest.


Supplement

SUPPORTING INFORMATION

Methods

Results

Figure S1 Maximum likelihood tree of Gerdarchaeota MAGs built on a concatenated alignment of 55 archaeal genes.

Figure S2 Average nucleotide identity (ANI) (a) and amino acid identity (AAI) of Asgard (b) archaeal MAGs.

Figure S3 Pan-genome analysis of protein clusters within all Asgard MAGs using the Anvi’o software.

Figure S4 Maximum likelihood phylogenetic analyses of Topoisomerase IB, ribophorin I, and DNA-directed RNA polymerase A.

Figure S5 Key potential metabolic pathways of Asgard archaea.

Figure S6 Phylogenetic position of the Gerdarchaeota cytochrome c oxidases subunit II.

Figure S7 Phylogenetic position of the Gerdarchaeota rhodopsins.

Figure S8 Abundance of (a) peptidases and (b) carbohydrate-active enzymes in Asgard MAGs.

Figure S9 Phylogenetic position of the Gerdarchaeota [NiFe]-hydrogenases.

Figure S10 Phylogenetic maximum likelihood tree of RuBisCO amino acid sequences (large subunit).

Figure S11 Diversity and biotope of Asgard archaea.

Figure S12 Protein tree based on mcrA gene sequences as identified in the scaffolds.

Figure S13 Molecular modelling and dynamics of MCR complex.

Figure S14 Phylogenetic position and evolution of Asgard archaea mcrA genes.

Figure S15 Protein trees of Asgard archaea (a) McrB and (b) McrG.

Figure S16 Phylogenetic position of the Gerdarchaeota nifH.

Table S1 Information of sedimental samples analysed in this study

Table S2 Overview of Asgard archaea genomic bins

Table S3 The 16S rRNA gene identity (%) of Asgard groups Asgard lineage 1 to Asgard lineage 5 with other Asgard groups

Table S4 Accession numbers list of INTERPRO (IPR) domains and UniProtKB protein sequences related to ESPs

Table S5 Expression of ESPs in the novel Asgard archaea

Table S6 Gene annotation of Asgard archaea based on the NCBI-nr database, KEGG database, and InterProScan tool

Table S7 Overview of the transcript abundance (TPM) in surface and subsurface sediments at the phylum level

Table S8 ORFs of the scaffolds with cytochrome c oxidases

Table S9 Carbohydrate active enzymes numbers for each phylum

Table S10 Overview of 170 archaeal libraries that include Asgard archaeal 16S rRNA sequences

Table S11 Amino acid degradation pathways in Asgard archaea MAGs

Table S12 Summary of intracellular and extracellular peptidases from Asgard archaea MAGs.

Table S13 Characteristics of Asgard phyla

Supplementary Data 1 Phylogenetic position of Gerdarchaeota cytochrome c oxidases (newick format)

Supplementary Data 2 Phylogenetic position of Gerdarchaeota rhodopsins (newick format)

The supporting information is available online at http://life.scichina.com and https://link.springer.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.


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  • Figure 1

    Phylogenetic positions and ESPs of Asgard archaea reconstructed from coastal sediments. A, Maximum likelihood tree of Gerdarchaeota MAGs built on a concatenated alignment of 122 archaea-specific protein markers. The tree was inferred with LG+F+R10 mixture mode in IQ-TREE and rooted with DPANN and Euryarchaeota. Asgard archaea MAGs obtained in this study are marked in bold face. B, Phylogenetic position of Asgard archaeal 16S rRNA genes. Red color represents 16S rRNA genes from newly discovered Asgard MAGs, and blue color represents sequences from references. The tree was built using the IQ-TREE software with GTR+I+G4 mixture mode and rooted with Crenarchaeota. C, ESPs identified in Gerdarchaeota and other Asgard archaea. Asgard archaea MAGs obtained in this study are marked bold. Colors indicate phylum-level assignment (see 1A).

  • Figure 2

    Key potential metabolic pathways of Gerdarchaeota. Solid lines represent pathway steps present in 8 MAGs assigned to Gerdarchaeota. Dashed lines represent pathway steps not identified. Circles represent transcripts from surface sediments and rectangles represent transcripts from subsurface samples. The relative abundance of the transcripts (transcripts per million reads, TPM) for each gene is marked with different colors. Pathway abbreviations: PPP, pentose phosphate pathway (archaea); CBB, Calvin–Benson–Bassham cycle; EMP, Embden–Meyerhof–Parnas pathway, THMPT WL, tetrahydromethanopterin-dependent Wood–Ljungdahl pathway; TCA cycle, tricarboxylic acid cycle. Detailed metabolic information for the MAGs is available in Figure S5, ables S6 and S7 in Supporting Information.

  • Figure 3

    Ecological niches of Asgard archaea in coastal sediments. Dashed lines represent pathways with no transcript for the key genes. Detailed information is available in Figure S5, Tables S6 and S7 in Supporting Information.

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