Insight into the symbiotic lifestyle of DPANN archaea revealed by culture and genome analyzes

Importance

The superphylum DPANN is a grouping of symbiotic microorganisms classified according to their genomic content and some examples of culture experiments. Although information on the genome of DPANN archaea is increasing year by year, most of it has remained uncultivated, limiting our knowledge of these organisms. Here, a thermoacidophilic symbiotic archaeon (ARM-1) of the superphylum DPANN has been cultured and characterized successfully. We have determined in detail its physiological, morphological and genomic characteristics and obtained experimental evidence of the symbiotic way of life of this archaeon. Notably, ARM-1 is a symbiotic strain of archaea which has shown dependence on a range of host species in laboratory culture. The results contribute significantly to the true understanding of the physiology and ecology of DPANN archaea.

Summary

Decades of independent culture analyzes have resulted in proposals for many phyla of provisional archaea without any cultivable representative. Members of DPANN (an acronym for the names of early phylum including Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanohaloarchaeota, and Nanoarchaeota), an archaeal superphylum composed of at least 10 of these provisional phylum, are generally considered obligate symbionts dependent on other micro -organisms. While numerous provisional / complete genome sequences of DPANN archaea are available and their biological functions have been significantly predicted, only a few examples of their successful laboratory culture have been reported, limiting our knowledge of their symbiotic lifestyles. Here we have studied the physiology, morphology and host specificity of an archaeon of the phylum “Candidatus Micrarchaeota ”(ARM-1) belonging to the superphylum DPANN by culture. We have built a stable coculture system composed of ARM-1 and its original host Metallospheres sp. AS-7 belonging to the order Sulfolobales. Further host-change experiments confirmed that ARM-1 developed in five different species of archaea from three genera—Metallospheres, Acidianus, and Saccharolobus—From geologically distinct hot and acidic environments. The results suggest the existence of DPANN arches which can grow by relying on a range of hosts. Genomic analyzes showed inferred metabolic capabilities, common / unique genetic content of ARM-1 among representatives of cultured micro-strings, and the possibility of horizontal gene transfer between ARM-1 and members of the order. Sulfolobales. Our report sheds light on the symbiotic lifestyles of DPANN archaea and will contribute to the elucidation of their biological / ecological functions.

Footnotes

    • Accepted November 12, 2021.
  • Author contributions: research designed by HDS, AS and NK; HDS, NN, AS and NK carried out research; NN and NK carried out field sampling; HDS, MY and MS provided new reagents / analytical tools; HDS, SK, TI and MO analyzed the data; and HDS and NK wrote the paper.

  • The authors declare no competing interests.

  • This article is a direct PNAS submission.

  • This article contains additional information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2115449119/-/DCSupplemental.

Data availability

The 16S rRNA gene sequence data to support the results of this study have been deposited in GenBank under the accession numbers. LC490573 – LC490578. ARM-1 genomic sequences and Metallospheres sp. AS-7 with raw read data has been filed under the following accession numbers: AP024486 (ARM-1 genome), AP024487 (AS-7 genome), DRR248897 (PacBio RS II long reads) and DRR248898 (Illumina short reads) MiSeq). All study data is included in the article and / or additional information.

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