Thanks to visit codestin.com
Credit goes to link.springer.com

Skip to main content
Springer Nature Link
Log in

Viruses and virus satellites of haloarchaea and their nanosized DPANN symbionts reveal intricate nested interactions

  • Article
  • Published:

From Nature Microbiology

View current issue Submit your manuscript

Abstract

Nested symbioses, including hyperparasitism in which parasites exploit other parasites within a host, are common in nature. However, such nested interactions remain poorly studied in archaea. Here we characterize this phenomenon in ultra-small archaea of the candidate phylum Nanohaloarchaeota, members of the DPANN superphylum (named after its first representative phyla: Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota and Nanohaloarchaeota) that form obligate interactions with halophilic archaea of the class Halobacteria. We reconstructed the viromes from geothermally influenced salt lakes in the Danakil Depression, Ethiopia, and find that nanohaloarchaea and haloarchaea are both associated with head-tailed, tailless icosahedral, pleomorphic and spindle-shaped viruses, representing 16 different families. These viruses exhibit convergent adaptation to hypersaline environments, encode diverse auxiliary metabolic genes and exchange genes horizontally with each other. We further characterize plasmid-derived satellites that independently evolved to parasitize spindle-shaped viruses of haloarchaea and nanohaloarchaea, revealing another layer of nested symbiosis. Collectively, our findings highlight the complexity of virus–host and virus–virus interactions in hypersaline environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1: Microbial and viral diversity in the salt lakes of the north Danakil Depression, Ethiopia.
Fig. 2: Genome-wide proteomic trees of the four virus groups.
Fig. 3: Genome maps of HVs and NHVs from the Danakil Depression.
Fig. 4: Phylogenetic analysis and structural modelling of AMGs encoded by DNTV-1.
Fig. 5: Horizontal gene transfer between HVs and NHVs.
Fig. 6: Putative satellites associated with spindle-shaped HVs and NHVs.

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

Data availability

All assembled genomes were deposited to GenBank (viruses: PQ827550–PQ827567; SRCEs and plasmids: PQ766422–PQ766435). Metagenome-assembled genomes are accessible on GenBank through BioProject PRJNA541281. All identified haloarchaeal and nanohaloarchaeal CRISPRs and spacers are available via GitHub at https://github.com/IfanZHOU/DAL-virome. Source data are provided with this paper.

Code availability

All scripts used in this work are available via GitHub at https://github.com/IfanZHOU/DAL-virome.

References

  1. Goker, M. & Oren, A. Valid publication of names of two domains and seven kingdoms of prokaryotes. Int. J. Syst. Evol. Microbiol. https://doi.org/10.1099/ijsem.0.006242 (2024).

  2. Baker, B. J. et al. Diversity, ecology and evolution of Archaea. Nat. Microbiol 5, 887–900 (2020).

    Article  PubMed  CAS  Google Scholar 

  3. Dombrowski, N., Lee, J. H., Williams, T. A., Offre, P. & Spang, A. Genomic diversity, lifestyles and evolutionary origins of DPANN archaea. FEMS Microbiol. Lett. https://doi.org/10.1093/femsle/fnz008 (2019).

  4. Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).

    Article  PubMed  CAS  Google Scholar 

  5. Emerson, J. B. et al. Virus–host and CRISPR dynamics in Archaea-dominated hypersaline Lake Tyrrell, Victoria, Australia. Archaea 2013, 370871 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Martínez-García, M., Santos, F., Moreno-Paz, M., Parro, V. & Anton, J. Unveiling viral–host interactions within the ‘microbial dark matter. Nat. Commun. 5, 4542 (2014).

    Article  PubMed  Google Scholar 

  7. Wu, Z., Liu, S. & Ni, J. Metagenomic characterization of viruses and mobile genetic elements associated with the DPANN archaeal superphylum. Nat. Microbiol. 9, 3362–3375 (2024).

    Article  PubMed  CAS  Google Scholar 

  8. Penades, J. R., Seed, K. D., Chen, J., Bikard, D. & Rocha, E. P. C. Genetics, ecology and evolution of phage satellites. Nat. Rev. Microbiol. https://doi.org/10.1038/s41579-025-01156-z (2025).

    Article  PubMed  Google Scholar 

  9. Arnold, H. P. et al. The genetic element pSSVx of the extremely thermophilic crenarchaeon Sulfolobus is a hybrid between a plasmid and a virus. Mol. Microbiol. 34, 217–226 (1999).

    Article  PubMed  CAS  Google Scholar 

  10. Wang, Y. et al. A novel Sulfolobus non-conjugative extrachromosomal genetic element capable of integration into the host genome and spreading in the presence of a fusellovirus. Virology 363, 124–133 (2007).

    Article  PubMed  CAS  Google Scholar 

  11. Andrade, K. et al. Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem. ISME J. 9, 2697–2711 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Baker, B. A. et al. Expanded phylogeny of extremely halophilic archaea shows multiple independent adaptations to hypersaline environments. Nat. Microbiol 9, 964–975 (2024).

    Article  PubMed  CAS  Google Scholar 

  13. Feng, Y. et al. The evolutionary origins of extreme halophilic archaeal lineages. Genome Biol. Evol. https://doi.org/10.1093/gbe/evab166 (2021).

  14. Zhao, D. et al. Comparative genomic insights into the evolution of Halobacteria-associated “Candidatus Nanohaloarchaeota”. mSystems 7, e0066922 (2022).

    Article  PubMed  Google Scholar 

  15. Hamm, J. N. et al. Unexpected host dependency of Antarctic Nanohaloarchaeota. Proc. Natl Acad. Sci. USA 116, 14661–14670 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. La Cono, V. et al. Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea. Microb. Biotechnol. 16, 1803–1822 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  17. La Cono, V. et al. Symbiosis between nanohaloarchaeon and haloarchaeon is based on utilization of different polysaccharides. Proc. Natl Acad. Sci. USA 117, 20223–20234 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Reva, O. et al. Functional diversity of nanohaloarchaea within xylan-degrading consortia. Front. Microbiol. 14, 1182464 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Puxty, R. J. & Millard, A. D. Functional ecology of bacteriophages in the environment. Curr. Opin. Microbiol. 71, 102245 (2023).

    Article  PubMed  CAS  Google Scholar 

  20. Breitbart, M., Bonnain, C., Malki, K. & Sawaya, N. A. Phage puppet masters of the marine microbial realm. Nat. Microbiol. 3, 754–766 (2018).

    Article  PubMed  CAS  Google Scholar 

  21. López-García, P. et al. Metagenome-derived virus–microbe ratios across ecosystems. ISME J. 17, 1552–1563 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Santos, F. et al. Culture-independent approaches for studying viruses from hypersaline environments. Appl. Environ. Microbiol. 78, 1635–1643 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Liu, Y. et al. Diversity, taxonomy, and evolution of archaeal viruses of the class Caudoviricetes. PLoS Biol. 19, e3001442 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Atanasova, N. S., Bamford, D. H. & Oksanen, H. M. Haloarchaeal virus morphotypes. Biochimie 118, 333–343 (2015).

    Article  PubMed  CAS  Google Scholar 

  25. Luk, A. W., Williams, T. J., Erdmann, S., Papke, R. T. & Cavicchioli, R. Viruses of haloarchaea. Life 4, 681–715 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Dyall-Smith, M., Tang, S. L. & Bath, C. Haloarchaeal viruses: how diverse are they?. Res. Microbiol. 154, 309–313 (2003).

    Article  PubMed  Google Scholar 

  27. Crits-Christoph, A. et al. Functional interactions of archaea, bacteria and viruses in a hypersaline endolithic community. Environ. Microbiol. 18, 2064–2077 (2016).

    Article  PubMed  CAS  Google Scholar 

  28. Emerson, J. B. et al. Dynamic viral populations in hypersaline systems as revealed by metagenomic assembly. Appl. Environ. Microbiol. 78, 6309–6320 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Garcia-Heredia, I. et al. Reconstructing viral genomes from the environment using fosmid clones: the case of haloviruses. PLoS ONE 7, e33802 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Belilla, J. et al. Archaeal overdominance close to life-limiting conditions in geothermally influenced hypersaline lakes at the Danakil Depression, Ethiopia. Environ. Microbiol. 23, 7168–7182 (2021).

    Article  PubMed  CAS  Google Scholar 

  31. Gutiérrez-Preciado, A. et al. Extremely acidic proteomes and metabolic flexibility in bacteria and highly diversified archaea thriving in geothermal chaotropic brines. Nat. Ecol. Evol. 8, 1856–1869 (2024).

    Article  PubMed  Google Scholar 

  32. Maier, L. K. et al. The nuts and bolts of the Haloferax CRISPR–Cas system I-B. RNA Biol. 16, 469–480 (2019).

    Article  PubMed  Google Scholar 

  33. Nayfach, S. et al. A genomic catalog of Earth’s microbiomes. Nat. Biotechnol. 39, 499–509 (2021).

    Article  PubMed  CAS  Google Scholar 

  34. Camargo, A. P. et al. Identification of mobile genetic elements with geNomad. Nat. Biotechnol. 42, 1303–1312 (2024).

    Article  PubMed  CAS  Google Scholar 

  35. Guo, J. et al. VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses. Microbiome 9, 37 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Esser, S. P. et al. A predicted CRISPR-mediated symbiosis between uncultivated archaea. Nat. Microbiol. 8, 1619–1633 (2023).

    Article  PubMed  CAS  Google Scholar 

  37. Reed, C. J., Lewis, H., Trejo, E., Winston, V. & Evilia, C. Protein adaptations in archaeal extremophiles. Archaea 2013, 373275 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Simon, D., Cristina, J. & Musto, H. Nucleotide composition and codon usage across viruses and their respective hosts. Front Microbiol. 12, 646300 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Hurwitz, B. L. & U’Ren, J. M. Viral metabolic reprogramming in marine ecosystems. Curr. Opin. Microbiol. 31, 161–168 (2016).

    Article  PubMed  CAS  Google Scholar 

  40. Enav, H., Mandel-Gutfreund, Y. & Beja, O. Comparative metagenomic analyses reveal viral-induced shifts of host metabolism towards nucleotide biosynthesis. Microbiome 2, 9 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Krupovic, M., Gribaldo, S., Bamford, D. H. & Forterre, P. The evolutionary history of archaeal MCM helicases: a case study of vertical evolution combined with hitchhiking of mobile genetic elements. Mol. Biol. Evol. 27, 2716–2732 (2010).

    Article  PubMed  CAS  Google Scholar 

  42. Chevallereau, A. et al. Next-generation “-omics” approaches reveal a massive alteration of host RNA metabolism during bacteriophage infection of Pseudomonas aeruginosa. PLoS Genet. 12, e1006134 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Oakley, A. J., Coggan, M. & Board, P. G. Identification and characterization of gamma-glutamylamine cyclotransferase, an enzyme responsible for gamma-glutamyl-epsilon-lysine catabolism. J. Biol. Chem. 285, 9642–9648 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Milewski, S. Glucosamine-6-phosphate synthase—the multi-facets enzyme. Biochim. Biophys. Acta 1597, 173–192 (2002).

    Article  PubMed  CAS  Google Scholar 

  45. Isupov, M. N. et al. Substrate binding is required for assembly of the active conformation of the catalytic site in Ntn amidotransferases: evidence from the 1.8 A crystal structure of the glutaminase domain of glucosamine 6-phosphate synthase. Structure 4, 801–810 (1996).

    Article  PubMed  CAS  Google Scholar 

  46. Reva, O. N. et al. DPANN symbiont of Haloferax volcanii accelerates xylan degradation by the non-host haloarchaeon Halorhabdus sp. iScience 28, 111749 (2025).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Reva, O. N. et al. Interplay of intracellular and trans-cellular DNA methylation in natural archaeal consortia. Environ. Microbiol. Rep. 16, e13258 (2024).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Krupovic, M., Quemin, E. R., Bamford, D. H., Forterre, P. & Prangishvili, D. Unification of the globally distributed spindle-shaped viruses of the Archaea. J. Virol. 88, 2354–2358 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Wang, F. et al. Spindle-shaped archaeal viruses evolved from rod-shaped ancestors to package a larger genome. Cell 185, 1297–1307 (2022).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Roux, S. et al. Analysis of metagenomic data reveals common features of halophilic viral communities across continents. Environ. Microbiol. 18, 889–903 (2016).

    Article  PubMed  Google Scholar 

  51. Guyot, V. et al. A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids. PLoS Pathog. 18, e1010448 (2022).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Boyd, C. M. & Seed, K. D. A phage satellite manipulates the viral DNA packaging motor to inhibit phage and promote satellite spread. Nucleic Acids Res. 52, 10431–10446 (2024).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. de Sousa, J. A. M., Fillol-Salom, A., Penades, J. R. & Rocha, E. P. C. Identification and characterization of thousands of bacteriophage satellites across bacteria. Nucleic Acids Res. 51, 2759–2777 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Alqurainy, N. et al. A widespread family of phage-inducible chromosomal islands only steals bacteriophage tails to spread in nature. Cell Host Microbe 31, 69–82 (2023).

    Article  PubMed  CAS  Google Scholar 

  55. Hadidi, A., Czosnek, H. H., Kalantidis, K. & Palukaitis, P. Viroids and satellites and their vector interactions. Viruses https://doi.org/10.3390/v16101598 (2024).

  56. Dyall-Smith, M. & Pfeiffer, F. Global distribution and diversity of haloarchaeal pL6-family plasmids. Genes https://doi.org/10.3390/genes15091123 (2024).

  57. Dyall-Smith, M. & Pfeiffer, F. The PL6-family plasmids of haloquadratum are virus-related. Front. Microbiol. 9, 1070 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Koonin, E. V. & Krupovic, M. Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity. Curr. Opin. Virol. 25, 7–15 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Belilla, J. et al. Hyperdiverse archaea near life limits at the polyextreme geothermal Dallol area. Nat. Ecol. Evol. 3, 1552–1561 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Allers, T., Ngo, H. P., Mevarech, M. & Lloyd, R. G. Development of additional selectable markers for the halophilic archaeon Haloferax volcanii based on the leuB and trpA genes. Appl. Environ. Microbiol. 70, 943–953 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Zhou, Y., Wang, Y., Prangishvili, D. & Krupovic, M. Exploring the archaeal virosphere by metagenomics. Methods Mol. Biol. 2732, 1–22 (2024).

    Article  PubMed  CAS  Google Scholar 

  62. Nayfach, S. et al. CheckV assesses the quality and completeness of metagenome-assembled viral genomes. Nat. Biotechnol. 39, 578–585 (2021).

    Article  PubMed  CAS  Google Scholar 

  63. Bin Jang, H. et al. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat. Biotechnol. 37, 632–639 (2019).

    Article  Google Scholar 

  64. Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504 (2003).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Couvin, D. et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res. 46, W246–W251 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).

    Article  PubMed  CAS  Google Scholar 

  67. Zhou, Y. et al. Diverse viruses of marine archaea discovered using metagenomics. Environ. Microbiol. 25, 367–382 (2023).

    Article  PubMed  CAS  Google Scholar 

  68. Edwards, R. A., McNair, K., Faust, K., Raes, J. & Dutilh, B. E. Computational approaches to predict bacteriophage-host relationships. FEMS Microbiol. Rev. 40, 258–272 (2016).

    Article  PubMed  CAS  Google Scholar 

  69. Gong, C. et al. Novel virophages discovered in a freshwater lake in China. Front. Microbiol 7, 5 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  70. Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).

    Article  PubMed  CAS  Google Scholar 

  71. Steinegger, M. et al. HH-suite3 for fast remote homology detection and deep protein annotation. BMC Bioinf. 20, 473 (2019).

    Article  Google Scholar 

  72. Gabler, F. et al. Protein sequence analysis using the MPI Bioinformatics Toolkit. Curr. Protoc. Bioinform. 72, e108 (2020).

    Article  CAS  Google Scholar 

  73. Nishimura, Y. et al. ViPTree: the viral proteomic tree server. Bioinformatics 33, 2379–2380 (2017).

    Article  PubMed  CAS  Google Scholar 

  74. Aroney, S. T. et al. CoverM: read alignment statistics for metagenomics. Bioinformatics 41, btaf147 (2025).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Edgar, R. C. Muscle5: high-accuracy alignment ensembles enable unbiased assessments of sequence homology and phylogeny. Nat. Commun. 13, 6968 (2022).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldon, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  77. Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Letunic, I. & Bork, P. Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Res. 52, W78–W82 (2024).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Kazlauskas, D., Varsani, A., Koonin, E. V. & Krupovic, M. Multiple origins of prokaryotic and eukaryotic single-stranded DNA viruses from bacterial and archaeal plasmids. Nat. Commun. 10, 3425 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from Ville de Paris (Emergence(s) project MEMREMA) and Agence Nationale de la Recherche (ANR-23-CE13-022 and ANR-21-CE11-0001) to M.K., and the Moore Foundation (https://doi.org/10.37807/GBMF9739), the ANR (ANR-23-CE02-0016-01) and the European Research Council (ERC-2023-AdG 101141745) to P.L.-G. We thank X. Wang, T. Xu and A. Zhou for their help with configuration of software and scripts.

Author information

Authors and Affiliations

  1. Institut Pasteur, Université Paris Cité, CNRS UMR6047, Cell Biology and Virology of Archaea Unit, Paris, France

    Yifan Zhou, Ying Liu & Mart Krupovic

  2. Collège Doctoral, Sorbonne Université, Paris, France

    Yifan Zhou

  3. Ecologie Systématique Evolution, CNRS, Université Paris-Saclay, AgroParisTech, Gif-sur-Yvette, France

    Ana Gutiérrez-Preciado, David Moreira & Purificación López-García

  4. Extreme Microbiology, Biotechnology and Astrobiology Group, Institute of Polar Sciences, ISP-CNR, Messina, Italy

    Michail M. Yakimov

Authors
  1. Yifan Zhou
    View author publications

    Search author on:PubMed Google Scholar

  2. Ana Gutiérrez-Preciado
    View author publications

    Search author on:PubMed Google Scholar

  3. Ying Liu
    View author publications

    Search author on:PubMed Google Scholar

  4. David Moreira
    View author publications

    Search author on:PubMed Google Scholar

  5. Michail M. Yakimov
    View author publications

    Search author on:PubMed Google Scholar

  6. Purificación López-García
    View author publications

    Search author on:PubMed Google Scholar

  7. Mart Krupovic
    View author publications

    Search author on:PubMed Google Scholar

Contributions

M.K. and Y.Z. conceived the study; Y.Z. assembled and analysed the viral genomes; M.K. annotated the viral genomes and performed structural modelling; Y.L. established enrichment cultures and performed electron microscopy; A.G.-P. analysed the distribution and abundance of viruses and satellites in salt lake metagenomes; D.M. and P.L.-G. collected the environmental samples and provided access to metagenomes; M.M.Y. advised on cultivation of haloarchaeal and nanohaloarchaeal communities. All authors contributed to the conceptualization of the results; Y.Z. and M.K. wrote the paper, which was revised and approved by all coauthors.

Corresponding author

Correspondence to Mart Krupovic.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Microbiology thanks Shingo Kato and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

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

Extended data

Extended Data Fig. 1 CRISPR diversity in the genomes of Halobacteriota (Halo) and Nanohaloarchaeota (Nanohalo).

Similarity networks of CRISPR sequences. Each node represents a CRISPR sequence and the links between nodes represent the degree of sequence similarity between CRISPR sequences.

Extended Data Fig. 2 The vConTACT2 gene-sharing networks of viruses from Danakil Depression and reference prokaryotic DNA viruses.

Each node represents a viral sequence and the edges between nodes represent the degree of connectivity based on the fraction of shared proteins. Nodes for reference bacteriophages are colored cyan, reference archaeal viruses are in yellow, and Danakil viruses are in red. The Danakil viral contigs formed three clusters (outlined) with previously described archaeal viruses: I, head-tailed HVs (class Caudoviricetes, n = 382); II, tailless icosahedral HVs (families Simuloviridae and Sphaerolipoviridae, n = 26); III, pleomorphic HVs (family Pleolipoviridae, n = 9).

Extended Data Fig. 3 Genome maps showing the relationship among spindle-shaped viruses.

a. Spindle-shaped NHVs. b. Spindle-shaped HVs.

Extended Data Fig. 4 Genome maps showing the relationships among head-tailed NHVs.

a. Gulliviridae. b. Lilliviridae. c. Saladoviridae. d. Graaviviridae; e. Madisaviridae; f. Pyrstoviridae.

Extended Data Fig. 5 The heatmap of orthologous fraction among archaeal tailed viruses.

HVs and NHVs described in this work are shown in red. Family-level groups of viruses including representatives from the Danakil Depression are boxed. Orthologous fraction values > 0.08 are shown.

Source data

Extended Data Fig. 6 Genome maps showing the relationships among pleomorphic and tailless icosahedral viruses.

a. Pleolipoviridae HVs. b. Nanopleoviridae NHVs. c. Nanicoviridae NHVs.

Extended Data Fig. 7 Adaptation of HVs and NHVs to hypersaline environments.

a. Heatmap of amino acid usage patterns. Amino acid frequencies were calculated using proteins encoded by haloarchaea (n = 10), nanohaloarchaea (n = 10) and their viruses (HVs and NHVs) from the Danakil Depression. Genomes of two head-tailed HVs (CGphi46 and HRTV-28) and their hosts as well as two complete genomes of nanohaloarchaea were used for comparison. Genomes of two Sulfolobus species and their viruses SPV1 and SPV2 were also used for comparison. b. Distribution of isoelectric point (pI) values inferred for proteins encoded by the Danakil haloarchaea, nanohaloarchaea and their viruses (HVs and NHVs) in comparison with representative archaeal genomes from seawater (Nitrosopumilus, n = 2) and hot springs (Sulfolobus, n = 2). c. Box plots show GC content (%) of genomes of Halobacteriales (n = 749), Nanohaloarchaeota (n = 49) and head-tailed viruses (HVs, n = 62 and NHVs, n = 9). The center line represents the median; the box limits, the first and third quartiles; whiskers extend 1.5 times the interquartile range; data beyond the whiskers are outliers represented as points.

Source data

Extended Data Fig. 8 Maximum likelihood phylogenies of the hallmark proteins of head-tailed viruses.

a. Major capsid protein (MCP) of head-tailed HVs and NHVs. b. Portal protein of head-tailed HVs and NHVs. c. Terminase large subunit (TerL) of head-tailed HVs and NHVs. NHVs are indicated with pink branches.

Extended Data Fig. 9 Heatmap showing the distribution and abundance of haloarchaeal and nanohaloarchaeal spindle-shaped viruses and SRCEs (mean coverage, rows) in Danakil salt lakes (columns).

Intensity of the blue color represents relative abundance. The accompanying histogram (upper left) displays the distribution of abundance values across all virus–site combinations.

Source data

Extended Data Fig. 10 The complexity of interactions between haloarchaea, nanohaloarchaea, their respective viruses and virus satellites.

1: Viruses infect a haloarchaeal host; 2: A spacer is acquired from viral DNA by the haloarchaeal CRISPR-Cas system; 3: CRISPR spacers are transcribed, matured, and matched with target viral DNA with the help of Cas proteins, leading to the cleavage of the invading viral DNA; 4: Similar CRISPR-Cas immunity processes (1, 2, 3) are happening in nanohaloarchaea; 5: A gene transfer from an icosahedral HV to an icosahedral NHV; 6: A gene transfer from a head-tailed NHV to a head-tailed HV; 7: A gene transfer from a nanohaloarchaeal host to a head-tailed virus; 8: Spindle-shaped HVs infect a haloarchaeal host without interference of virus satellites (SRCEs); 9: Spindle-shaped HVs and SRCEs co-infect a haloarchaeal host. SRCEs replicate and consume the virion components of HVs, which lead to a decrease in HV production; 10: Similar phenomenon (9) is also happening in nanohaloarchaea; 11: the archaeal host carries a CRISPR array with spacers targeting both viruses and virus satellites. Created in BioRender. Krupovic, M. (2025) https://BioRender.com/ptoya59.

Supplementary information

Supplementary Information

Supplementary Text.

Reporting Summary

Peer Review File

Supplementary Tables 1–8

Supplementary Table 1. General genomic characteristics of HVs and NHVs from the salt lakes of the Danakil Depression. Supplementary Table 2. General genomic characteristics of HVs and NHVs related to viruses from the Danakil Depression. Supplementary Table 3. Functional annotations of proteins encoded by HVs and NHVs and their relatives from the salt lakes of the Danakil Depression. Supplementary Table 4. The tRNA genes encoded by DNTV-1. Supplementary Table 5. Results of the BLASTp search against the NCBI nr database for all protein sequences of Danakil Depression viruses. Supplementary Table 6. The BLASTp results showing candidates of horizontal gene transfers between HVs and NHVs. Supplementary Table 7. Protospacer-spacer matching information. Supplementary Table 8. CRISPR arrays targeting multiple mobile genetic elements, shown as BLASTs hits. Spacers from the same CRISPR array are highlighted with the same colour.

Source data

Source Data Fig. 1

Statistical source data.

Source Data Extended Data Fig. 5

Statistical source data.

Source Data Extended Data Fig. 7

Statistical source data.

Source Data Extended Data Fig. 9

Statistical source data.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, Y., Gutiérrez-Preciado, A., Liu, Y. et al. Viruses and virus satellites of haloarchaea and their nanosized DPANN symbionts reveal intricate nested interactions. Nat Microbiol (2025). https://doi.org/10.1038/s41564-025-02149-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41564-025-02149-7

  • Springer Nature Limited

Profiles

  1. Mart Krupovic View author profile