Undinarchaeota Illuminate DPANN Phylogeny and the Impact of Gene Transfer on Archaeal Evolution

Overview

Journal Nat Commun

Specialty Biology

Date 2020 Aug 10

PMID 32770105

Citations 58

Authors

Nina Dombrowski

Tom A Williams

Jiarui Sun

Benjamin J Woodcroft

Jun-Hoe Lee

Bui Quang Minh

Christian Rinke

Anja Spang

Affiliations

Soon will be listed here.

Abstract

The recently discovered DPANN archaea are a potentially deep-branching, monophyletic radiation of organisms with small cells and genomes. However, the monophyly and early emergence of the various DPANN clades and their role in life's evolution are debated. Here, we reconstructed and analysed genomes of an uncharacterized archaeal phylum (Candidatus Undinarchaeota), revealing that its members have small genomes and, while potentially being able to conserve energy through fermentation, likely depend on partner organisms for the acquisition of certain metabolites. Our phylogenomic analyses robustly place Undinarchaeota as an independent lineage between two highly supported 'DPANN' clans. Further, our analyses suggest that DPANN have exchanged core genes with their hosts, adding to the difficulty of placing DPANN in the tree of life. This pattern can be sufficiently dominant to allow identifying known symbiont-host clades based on routes of gene transfer. Together, our work provides insights into the origins and evolution of DPANN and their hosts.

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References

Silva F, Santos-Garcia D . Slow and Fast Evolving Endosymbiont Lineages: Positive Correlation between the Rates of Synonymous and Non-Synonymous Substitution. Front Microbiol. 2015; 6:1279. PMC: 4643148. DOI: 10.3389/fmicb.2015.01279. View

Li D, Liu C, Luo R, Sadakane K, Lam T . MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015; 31(10):1674-6. DOI: 10.1093/bioinformatics/btv033. View

Probst A, Moissl-Eichinger C . "Altiarchaeales": uncultivated archaea from the subsurface. Life (Basel). 2015; 5(2):1381-95. PMC: 4500143. DOI: 10.3390/life5021381. View

Moran N . Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A. 1996; 93(7):2873-8. PMC: 39726. DOI: 10.1073/pnas.93.7.2873. View

Golyshina O, Toshchakov S, Makarova K, Gavrilov S, Korzhenkov A, La Cono V . 'ARMAN' archaea depend on association with euryarchaeal host in culture and in situ. Nat Commun. 2017; 8(1):60. PMC: 5498576. DOI: 10.1038/s41467-017-00104-7. View

Spang A, Caceres E, Ettema T . Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science. 2017; 357(6351). DOI: 10.1126/science.aaf3883. View

Bateman A, Coin L, Durbin R, Finn R, Hollich V, Griffiths-Jones S . The Pfam protein families database. Nucleic Acids Res. 2003; 32(Database issue):D138-41. PMC: 308855. DOI: 10.1093/nar/gkh121. View

Tully B, Graham E, Heidelberg J . The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans. Sci Data. 2018; 5:170203. PMC: 5769542. DOI: 10.1038/sdata.2017.203. View

Narasingarao P, Podell S, Ugalde J, Brochier-Armanet C, Emerson J, Brocks J . De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J. 2011; 6(1):81-93. PMC: 3246234. DOI: 10.1038/ismej.2011.78. View

10.

Prokofeva M, Kostrikina N, Kolganova T, Tourova T, Lysenko A, Lebedinsky A . Isolation of the anaerobic thermoacidophilic crenarchaeote Acidilobus saccharovorans sp. nov. and proposal of Acidilobales ord. nov., including Acidilobaceae fam. nov. and Caldisphaeraceae fam. nov. Int J Syst Evol Microbiol. 2009; 59(Pt 12):3116-22. DOI: 10.1099/ijs.0.010355-0. View

11.

Kelley L, Mezulis S, Yates C, Wass M, Sternberg M . The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 2015; 10(6):845-58. PMC: 5298202. DOI: 10.1038/nprot.2015.053. View

12.

Williams T, Foster P, Cox C, Embley T . An archaeal origin of eukaryotes supports only two primary domains of life. Nature. 2013; 504(7479):231-6. DOI: 10.1038/nature12779. View

13.

Dombrowski N, Williams T, Sun J, Woodcroft B, Lee J, Minh B . Undinarchaeota illuminate DPANN phylogeny and the impact of gene transfer on archaeal evolution. Nat Commun. 2020; 11(1):3939. PMC: 7414124. DOI: 10.1038/s41467-020-17408-w. View

14.

Katoh K, Misawa K, Kuma K, Miyata T . MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002; 30(14):3059-66. PMC: 135756. DOI: 10.1093/nar/gkf436. View

15.

Steinegger M, Meier M, Mirdita M, Vohringer H, Haunsberger S, Soding J . HH-suite3 for fast remote homology detection and deep protein annotation. BMC Bioinformatics. 2019; 20(1):473. PMC: 6744700. DOI: 10.1186/s12859-019-3019-7. View

16.

Haro-Moreno J, Lopez-Perez M, de la Torre J, Picazo A, Camacho A, Rodriguez-Valera F . Fine metagenomic profile of the Mediterranean stratified and mixed water columns revealed by assembly and recruitment. Microbiome. 2018; 6(1):128. PMC: 6040077. DOI: 10.1186/s40168-018-0513-5. View

17.

Parks D, Chuvochina M, Waite D, Rinke C, Skarshewski A, Chaumeil P . A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018; 36(10):996-1004. DOI: 10.1038/nbt.4229. View

18.

Munson-McGee J, Field E, Bateson M, Rooney C, Stepanauskas R, Young M . Nanoarchaeota, Their Sulfolobales Host, and Nanoarchaeota Virus Distribution across Yellowstone National Park Hot Springs. Appl Environ Microbiol. 2015; 81(22):7860-8. PMC: 4616950. DOI: 10.1128/AEM.01539-15. View

19.

Brochier C, Philippe H . Phylogeny: a non-hyperthermophilic ancestor for bacteria. Nature. 2002; 417(6886):244. DOI: 10.1038/417244a. View

20.

Dombrowski N, Lee J, Williams T, Offre P, Spang A . Genomic diversity, lifestyles and evolutionary origins of DPANN archaea. FEMS Microbiol Lett. 2019; 366(2). PMC: 6349945. DOI: 10.1093/femsle/fnz008. View