An archaeal symbiont-host association from the deep terrestrial subsurface

Article metrics


DPANN archaea have reduced metabolic capacities and are diverse and abundant in deep aquifer ecosystems, yet little is known about their interactions with other microorganisms that reside there. Here, we provide evidence for an archaeal host-symbiont association from a deep aquifer system at the Colorado Plateau (Utah, USA). The symbiont, Candidatus Huberiarchaeum crystalense, and its host, Ca. Altiarchaeum hamiconexum, show a highly significant co-occurrence pattern over 65 metagenome samples collected over six years. The physical association of the two organisms was confirmed with genome-informed fluorescence in situ hybridization depicting small cocci of Ca. H. crystalense attached to Ca. A. hamiconexum cells. Based on genomic information, Ca. H. crystalense potentially scavenges vitamins, sugars, nucleotides, and reduced redox-equivalents from its host and thus has a similar metabolism as Nanoarchaeum equitans. These results provide insight into host-symbiont interactions among members of two uncultivated archaeal phyla that thrive in a deep subsurface aquifer.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1
Fig. 2


  1. 1.

    Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng J-F, et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature. 2013;499:431–7.

  2. 2.

    Castelle CJ, Wrighton KC, Thomas BC, Hug LA, Brown CT, Wilkins MJ, et al. Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr Biol. 2015;25:690–701.

  3. 3.

    Huber H, Hohn MJ, Rachel R, Fuchs T, Wimmer VC, Stetter KO. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature. 2002;417:63–7.

  4. 4.

    Jarett JK, Nayfach S, Podar M, Inskeep W, Ivanova NN, Munson-McGee J, et al. Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis. Microbiome. 2018;6:161.

  5. 5.

    Baker BJ, Comolli LR, Dick GJ, Hauser LJ, Hyatt D, Dill BD, et al. Enigmatic, ultrasmall, uncultivated Archaea. Proc Natl Acad Sci. 2010;107:8806–11. 200914470.

  6. 6.

    Krause S, Bremges A, Münch PC, McHardy AC, Gescher J. Characterisation of a stable laboratory co-culture of acidophilic nanoorganisms. Sci Rep. 2017;7:3289.

  7. 7.

    Golyshina OV, Toshchakov SV, Makarova KS, Gavrilov SN, Korzhenkov AA, La Cono V, et al. ‘ARMAN’archaea depend on association with euryarchaeal host in culture and in situ. Nat Commun. 2017;8:60.

  8. 8.

    Probst AJ, Ladd B, Jarett JK, Geller-McGrath DE, Sieber CMK, Emerson JB, et al. Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. Nat Microbiol. 2018;3:328–36.

  9. 9.

    Moissl C, Rudolph C, Rachel R, Koch M, Huber R. In situ growth of the novel SM1 euryarchaeon from a string-of-pearls-like microbial community in its cold biotope, its physical separation and insights into its structure and physiology. Arch Microbiol. 2003;180:211–7.

  10. 10.

    Schimak MP, Kleiner M, Wetzel S, Liebeke M, Dubilier N, Fuchs BM. MiL-FISH: Multilabeled oligonucleotides for fluorescence in situ hybridization improve visualization of bacterial cells. Appl Env Microbiol. 2016;82:62–70.

  11. 11.

    Rudolph C, Wanner G, Huber R. Natural communities of novel archaea and bacteria growing in cold sulfurous springs with a string-of-pearls-like morphology. Appl Environ Microbiol. 2001;67:2336–44.

  12. 12.

    Vallenet D, Labarre L, Rouy Z, Barbe V, Bocs S, Cruveiller S, et al. MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res. 2006;34:53–65.

  13. 13.

    Waters E, Hohn MJ, Ahel I, Graham DE, Adams MD, Barnstead M, et al. The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism. Proc Natl Acad Sci. 2003;100:12984–8.

  14. 14.

    Isobe K, Ogawa T, Hirose K, Yokoi T, Yoshimura T, Hemmi H. Geranylgeranyl reductase and ferredoxin from Methanosarcina acetivorans are required for the synthesis of fully reduced archaeal membrane lipid in Escherichia coli cells. J Bacteriol. 2014;196:417–23.

  15. 15.

    Villanueva L, Schouten S, Damsté JSS. Phylogenomic analysis of lipid biosynthetic genes of Archaea shed light on the ‘lipid divide’. Environ Microbiol. 2017;19:54–69.

  16. 16.

    Probst AJ, Elling FJ, Castelle CJ, Zhu Q, Elvert M, Birarda G, et al. Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria. bioRxiv 2018;465690.

  17. 17.

    Comolli LR, Baker BJ, Downing KH, Siegerist CE, Banfield JF. Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon. ISME J. 2009;3:159.

  18. 18.

    Heimerl T, Flechsler J, Pickl C, Heinz V, Salecker B, Zweck J, et al. A complex endomembrane system in the archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans. Front Microbiol. 2017;8:1072.

  19. 19.

    Probst AJ, Weinmaier T, Raymann K, Perras A, Emerson JB, Rattei T, et al. Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface. Nat Commun. 2014;5:5497.

  20. 20.

    Giannone RJ, Huber H, Karpinets T, Heimerl T, Küper U, Rachel R, et al. Proteomic characterization of cellular and molecular processes that enable the Nanoarchaeum equitans-Ignicoccus hospitalis relationship. PloS ONE. 2011;6:e22942.

Download references


This study was funded by the Ministerium für Kultur und Wissenschaft des Landes Nordrhein-Westfalen (“Nachwuchsgruppe Dr. Alexander Probst”). Parts of this research were carried out under the Sloan Award Deep Life (G-2017-9955, subaward 53588).  A.S. is supported by a grant of the Swedish Research Council (VR starting grant 2016-03559) and the NWO-I foundation of the Netherlands Organisation for Scientific Research (WISE fellowship).

Author information

Correspondence to Alexander J. Probst.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Further reading

  • Unexpected host dependency of Antarctic Nanohaloarchaeota

    • Joshua N. Hamm
    • , Susanne Erdmann
    • , Emiley A. Eloe-Fadrosh
    • , Allegra Angeloni
    • , Ling Zhong
    • , Christopher Brownlee
    • , Timothy J. Williams
    • , Kirston Barton
    • , Shaun Carswell
    • , Martin A. Smith
    • , Sarah Brazendale
    • , Alyce M. Hancock
    • , Michelle A. Allen
    • , Mark J. Raftery
    •  & Ricardo Cavicchioli

    Proceedings of the National Academy of Sciences (2019)