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Research Article | Ecological and Evolutionary Science

Heterotrophic Thaumarchaea with Small Genomes Are Widespread in the Dark Ocean

Frank O. Aylward, Alyson E. Santoro
Nick Bouskill, Editor
Frank O. Aylward
aDepartment of Biological Sciences, Virginia Tech, Blacksburg, Virginia, USA
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Alyson E. Santoro
bDepartment of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, California, USA
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Nick Bouskill
Lawrence Berkeley National Laboratory
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DOI: 10.1128/mSystems.00415-20
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  • FIG 1
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    FIG 1

    (A) Relative abundance of the HMT lineage in metagenomic data collected from across the global ocean at depths ranging from 250 to 1,000 m (blue) and >2,000 m (red). HMT relative abundances were calculated by mapping metagenomic reads against a nonredundant set of HMT proteins and are presented in units of reads per million. (B) Relative abundances of HMT versus AOA in different metagenomic samples. Values are the ratio of HMT to AOA, calculated by mapping reads to single-copy marker genes (see Materials and Methods for details). Bars in red denote metagenomic samples taken at depths of >2,000 m, while blue bars denote depths of <1,000 m.

  • FIG 2
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    FIG 2

    Abundance of HMT at Station ALOHA from 25 to 1,000 m. Metagenomic reads from samples collected from 2010 to 2011 were mapped against a nonredundant set of HMT proteins (see Materials and Methods for details). Relative abundance units are given in reads mapped per million.

  • FIG 3
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    FIG 3

    Phylogeny and gene loss analysis. (A) Maximum-likelihood phylogeny of high-quality reference genomes based on a concatenation of 30 marker genes. The phylogeny was generated in IQ-TREE with the C60 substitution model (see Materials and Methods for details). HMT genome sizes are colored purple. Complete genome sizes were estimated for incomplete genomes using completeness and contamination estimates (see Materials and Methods). Circles at the nodes provide the number of estimated gains and losses of orthologous groups. (B) COG composition of two HMT genomes and select high-quality reference genomes. Only genes annotated to select categories are provided; full annotations for all genomes are available in Data Set S3. (C) Functional analysis of the OGs gained and lost on the branch leading to the HMT (star in panel A).

  • FIG 4
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    FIG 4

    Hypothesized central carbon metabolism, electron transport chain, and selected transport capabilities in HMT. Dashed arrows indicate pathways with uncertain enzymology. Pathways: 1, branched-chain alpha-ketoacid dehydrogenase complex; 2, beta oxidation; 3, glycolysis; 4, nonoxidative pentose phosphate pathway; 5, ribose 1,5 bisphosphate isomerase; 6, ribulose bisphosphate carboxylase (RuBisCO); 7, tricarboxylic acid cycle. Annotations for all genes hypothesized to encode proteins in the numbered pathways and all depicted respiratory complexes are included in Data Set S4. Abbreviations: AAs, amino acids; ETF-QO, electron transfer flavoprotein-quinol oxidase; Ile, isoleucine; pcy, plastocyanin; PQQ-DH, pyrroloquinoline-quinone-dependent dehydrogenase; PRPP, phosphoribosyl pyrophosphate; Leu, leucine; Q, quinone pool; R15P, ribose 1,5-bisphosphate; Ru5P, ribose 5-phosphate; RuBP, ribulose 1,5-bisphosphate; SDH, succinate:fumarate dehydrogenase; TCA, tricarboxylic acid cycle; Val, valine. Figure design is modeled after figures from reference 9.

  • FIG 5
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    FIG 5

    Maximum-likelihood phylogeny of 21 HMT PQQ-dependent dehydrogenase families identified in the nonredundant set of HMT proteins (blue) together with reference sequences in the NCBI NR database. Colors symbols indicate the presence of transmembrane domains, signal peptides, and binding motifs in the HMT enzymes. Enzymes that were among the top 40 most highly expressed genes in the DeepDOM metatranscriptomes are denoted with a purple triangle. Black circles denote nodes with >80% bootstrap support (see Materials and Methods for details).

  • FIG 6
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    FIG 6

    Top 40 HMT genes with highest median RPKM in 10 DeepDOM metatranscriptomes. Protein names refer to a nonredundant set of HMT proteins collectively present in the HMT MAGs. Full annotations for these proteins can be found in Data Set S3.

Tables

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  • TABLE 1

    HMT Thaumarchaeota MAG statistics

    TABLE 1
    • ↵a Estimates made using the Rinke et al. (38) marker set (see Materials and Methods for details).

Supplemental Material

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  • FIG S1

    Concatenated maximum-likelihood phylogeny based on 30 highly conserved marker genes including Thaumarchaeota genomes with completeness of >50% (referred to as the full genome set; see Materials and Methods for details). The HMT clade is shown in blue. Black circles denote nodes with >80% bootstrap support, inferred using 1,000 ultrafast bootstraps in IQ-TREE. The collapsed node contains 147 genomes of ammonia-oxidizing archaea (AOA). Download FIG S1, PDF file, 0.03 MB.

    Copyright © 2020 Aylward and Santoro.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S2

    Maximum-likelihood tree of the HMT using 16S rRNA genes and references available in NCBI and the Ribosomal Database Project. Black circles denote nodes with >80% bootstrap support, inferred using 1,000 ultrafast bootstraps in IQ-TREE. 16S rRNA gene sequences from the 5 MAGs generated in this study are colored blue. Download FIG S2, PDF file, 0.03 MB.

    Copyright © 2020 Aylward and Santoro.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • DATA SET S1

    Raw results from metagenome and metatranscriptome read-mapping analyses. Download Data Set S1, XLSX file, 0.09 MB.

    Copyright © 2020 Aylward and Santoro.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S3

    Depth profile comparisons of HMT (red) and AOA (blue) at Station ALOHA based on marker gene mapping (top) and whole-genome mapping (bottom). The line in the boxplot denotes the median value. Details regarding the mapping can be found in Materials and Methods. Raw data can be found in Data Set S1. Download FIG S3, PDF file, 0.07 MB.

    Copyright © 2020 Aylward and Santoro.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • DATA SET S2

    Statistics for the HMT and reference genomes used in this study. Download Data Set S2, XLSX file, 0.1 MB.

    Copyright © 2020 Aylward and Santoro.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • DATA SET S3

    Annotations for the orthologous groups, HMT nonredundant protein set, and individual MAGs. Results are for the homology searches of HMT PQQ-dependent dehydrogenases when queried against NCBI databases. Download Data Set S3, XLSX file, 3.6 MB.

    Copyright © 2020 Aylward and Santoro.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • DATA SET S4

    Curated metabolic reconstruction of HMT pathways. Download Data Set S4, XLSX file, 0.06 MB.

    Copyright © 2020 Aylward and Santoro.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S4

    Maximum-likelihood phylogeny of the ATPase subunits present in the HMT genomes and available Thaumarchaeota references. The phylogeny is based on a concatenated alignment of ATPase subunits A and B. Black circles denote nodes with >80% bootstrap support, inferred using 1,000 ultrafast bootstraps in IQ-TREE (see Materials and Methods for details). Download FIG S4, PDF file, 0.04 MB.

    Copyright © 2020 Aylward and Santoro.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S5

    (A) Maximum-likelihood phylogeny of RuBisCo large subunits. Reference sequences and RuBisCO form classifications were obtained from Jaffe and Banfield (70) (see Materials and Methods for details). (B) Sample alignment including different forms of RuBisCo, with arrows indicating 19 conserved residues shown to be important for enzymatic activity (see the main text). The two unfilled arrows indicate residues that differ between HMT RuBisCo and other forms. Download FIG S5, PDF file, 0.4 MB.

    Copyright © 2020 Aylward and Santoro.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Heterotrophic Thaumarchaea with Small Genomes Are Widespread in the Dark Ocean
Frank O. Aylward, Alyson E. Santoro
mSystems Jun 2020, 5 (3) e00415-20; DOI: 10.1128/mSystems.00415-20

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Heterotrophic Thaumarchaea with Small Genomes Are Widespread in the Dark Ocean
Frank O. Aylward, Alyson E. Santoro
mSystems Jun 2020, 5 (3) e00415-20; DOI: 10.1128/mSystems.00415-20
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    • ABSTRACT
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KEYWORDS

Thaumarchaeota
marine archaea
TACK
PQQ-dehydrogenase
RuBisCO

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