Cited by 232Microbial Community Ecology and PhysiologyGenomics and Phylogenetic StudiesProtist diversity and phylogeny

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Genomic diversity, lifestyles and evolutionary origins of DPANN archaea

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Dombrowski, Nina, Lee, Jun-Hoe, Williams, Tom A, Offre, Pierre, Spang, Anja·2019·FEMS Microbiology Letters

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Abstract

Archaea-a primary domain of life besides Bacteria-have for a long time been regarded as peculiar organisms that play marginal roles in biogeochemical cycles. However, this picture changed with the discovery of a large diversity of archaea in non-extreme environments enabled by the use of cultivation-independent methods. These approaches have allowed the reconstruction of genomes of uncultivated microorganisms and revealed that archaea are diverse and broadly distributed in the biosphere and seemingly include a large diversity of putative symbiotic organisms, most of which belong to the tentative archaeal superphylum referred to as DPANN. This archaeal group encompasses at least 10 different lineages and includes organisms with extremely small cell and genome sizes and limited metabolic capabilities. Therefore, many members of DPANN may be obligately dependent on symbiotic interactions with other organisms and may even include novel parasites. In this contribution, we review the current knowledge of the gene repertoires and lifestyles of members of this group and discuss their placement in the tree of life, which is the basis for our understanding of the deep microbial roots and the role of symbiosis in the evolution of life on Earth.

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Figure 1. Phylogenetic tree displaying currently available taxonomic diversity of DPANN genomes. Tree was generated using the RP15 pipeline published previously in Zaremba-Niedzwiedzka et al. (2017) and is based on maximum-likelihood analyses in IQ-tree using the LG + C60 + F model of evolution. SH-values and bootstraps were calculated using a SH-like approximate likelihood ratio test (Guindon et al.2010) and ultrafast bootstrap support values (Minh et al.2013), respectively. Black and white circles indicate support values of 100/100 and 99.9–90/90–99.9, respectively. Scale bars indicate the average number of substitutions per site. The phylogeny represents bins available at NCBI before 23 March 2018 and indicates the genome size (for closed genomes), the bin completeness and contamination (for MAGs). The stars highlight genomes from DPANN members existing in co-cultures. Corresponding information for these genomic bins is available in Supplementary Table S1 (Supporting Information), the tree including taxa names is available as Supplementary Fig. S1 (Supporting Information) and the tree file is provided in Supplementary Data 1 (Supporting Information).CC BY · PubMed Central

Figure 2. General genome characteristics of DPANN archaea. Dot plots displaying total protein numbers (A) and GC content (B) versus genome size for DPANN genomes as compared to other archaeal representatives as well as selected endosymbiotic bacteria (see also Supplementary Table S1, Supporting Information). (C) Average amino acid frequencies of members of the DPANN archaea compared to their hosts, other archaea and bacterial endosymbionts (see also Supplementary Table S2, Supporting Information). Frequencies are shown for each individual amino acid, which are listed in their single letter code. Boxplot shows the median, the first and third quartiles, the upper/lower whiskers that extend from the hinge to the largest/smallest value no further than 1.5× of the interquartile range from the hinge as well as outliers, which are represented as dots. Boxplots were generated with R v3.5.0 using the package ggplot2.CC BY · PubMed Central

Figure 3. Transmission electron micrographs (TEM) of I. hospitalis and N. equitans interaction. This TEM of ultrathin sections of I. hospitalis and N. equitans display the interactions between this host–symbiont system and are based on a slightly modified and updated version of Fig. 4 originally published in Jahn et al. (2008) and kindly provided by Harald Huber. OCM: outer cellular membrane, IMC: intermembrane compartment, IM: inner membrane. Bars: 1 μm.CC BY · PubMed Central

Figure 4. Illustration of controversially discussed placements of DPANN lineages in the archaeal part of the tree of life. While most studies indicate that DPANN represent a deep-branching archaeal superphylum (A), few studies have suggested that some (B) or all DPANN lineages (C) could represent fast-evolving archaeal taxa, which are artificially attracted to the base of the archaeal tree while in fact affiliating with other archaeal lineages.CC BY · PubMed Central

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Authors: Dombrowski, N., Lee, J.-H., Williams, T. A., Offre, P., & Spang, A.
Affiliations: Utrecht University (NL)
Uppsala University (SE)
University of Bristol (GB)
Corresponding author: Spang, Anja
ORCID: Dombrowski, Nina
Lee, Jun-Hoe
Williams, Tom A
Offre, Pierre
Spang, Anja
Venue: FEMS Microbiology Letters
Publisher: Oxford University Press (OUP)
Published: 2019-01-01
Volume: 366
Issue: 2
ISSN: 0378-1097 (ISSN-L)
1574-6968
DOI: 10.1093/femsle/fnz008
PMC: PMC6349945
OpenAlex: W2910961041
Cited by: 230
References: 110
Citations by year: 2026: 20 · 2025: 25 · 2024: 34 · 2023: 30 · 2022: 43 · 2021: 39 · 2020: 28 · 2019: 11
FWCI: 2.19
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor, 9 d)
Locations: FEMS Microbiology Letters (publishedVersion, cc-by)
NIOZ Publications (Royal Netherlands Institute for Sea Research) (publishedVersion, other-oa)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Bristol Research (University of Bristol) (publishedVersion, cc-by)
Flanders Marine Institute (Flanders Marine Institute) (submittedVersion, other-oa)
KTH Publication Database DiVA (KTH Royal Institute of Technology) (submittedVersion, other-oa)
Explore Bristol Research (submittedVersion, cc-by)
Funders: Swedish Research Council (2016-03559)
Netherlands Organisation for Scientific Research
Royal Society University Research
Topics: Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
Keywords: DPANN archaea, genomic diversity, symbiosis, obligate symbionts, gene repertoire, tree of life, unculturable microorganisms
MeSH terms: Archaea, Phylogeny, Genetic Variation, Evolution, Molecular, Genome, Archaeal

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Genomic diversity, lifestyles and evolutionary origins of DPANN archaea

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