.2023 Feb 18;15(2):564.

doi: 10.3390/v15020564.

An Update on Eukaryotic Viruses Revived from Ancient Permafrost

Jean-Marie Alempic¹, Audrey Lartigue¹, Artemiy E Goncharov², Guido Grosse^{3 4}, Jens Strauss³, Alexey N Tikhonov⁵, Alexander N Fedorov⁶, Olivier Poirot¹, Matthieu Legendre¹, Sébastien Santini¹, Chantal Abergel¹, Jean-Michel Claverie¹

Affiliations

¹ IGS, Information Génomique & Structurale (UMR7256), Institut de Microbiologie de la Méditerranée (FR 3489), Institut Microbiologie, Bioénergies et Biotechnologie, and Institut Origines, CNRS, Aix Marseille University, 13288 Marseille, France.
² Department of Molecular Microbiology, Institute of Experimental Medicine, Department of Epidemiology, Parasitology and Disinfectology, Northwestern State Medical Mechnikov University, Saint Petersburg 195067, Russia.
³ Permafrost Research Section, Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, 14473 Potsdam, Germany.
⁴ Institute of Geosciences, University of Potsdam, 14478 Potsdam, Germany.
⁵ Laboratory of Theriology, Zoological Institute of Russian Academy of Science, Saint Petersburg 199034, Russia.
⁶ Melnikov Permafrost Institute, Yakutsk 677010, Russia.

PMID:36851778
PMCID: PMC9958942
DOI: 10.3390/v15020564

An Update on Eukaryotic Viruses Revived from Ancient Permafrost

Jean-Marie Alempic et al. Viruses.2023.

.2023 Feb 18;15(2):564.

doi: 10.3390/v15020564.

Authors

Affiliations

¹ IGS, Information Génomique & Structurale (UMR7256), Institut de Microbiologie de la Méditerranée (FR 3489), Institut Microbiologie, Bioénergies et Biotechnologie, and Institut Origines, CNRS, Aix Marseille University, 13288 Marseille, France.
² Department of Molecular Microbiology, Institute of Experimental Medicine, Department of Epidemiology, Parasitology and Disinfectology, Northwestern State Medical Mechnikov University, Saint Petersburg 195067, Russia.
³ Permafrost Research Section, Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, 14473 Potsdam, Germany.
⁴ Institute of Geosciences, University of Potsdam, 14478 Potsdam, Germany.
⁵ Laboratory of Theriology, Zoological Institute of Russian Academy of Science, Saint Petersburg 199034, Russia.
⁶ Melnikov Permafrost Institute, Yakutsk 677010, Russia.

PMID:36851778
PMCID: PMC9958942
DOI: 10.3390/v15020564

Abstract

One quarter of the Northern hemisphere is underlain by permanently frozen ground, referred to as permafrost. Due to climate warming, irreversibly thawing permafrost is releasing organic matter frozen for up to a million years, most of which decomposes into carbon dioxide and methane, further enhancing the greenhouse effect. Part of this organic matter also consists of revived cellular microbes (prokaryotes, unicellular eukaryotes) as well as viruses that have remained dormant since prehistorical times. While the literature abounds on descriptions of the rich and diverse prokaryotic microbiomes found in permafrost, no additional report about "live" viruses have been published since the two original studies describing pithovirus (in 2014) and mollivirus (in 2015). This wrongly suggests that such occurrences are rare and that "zombie viruses" are not a public health threat. To restore an appreciation closer to reality, we report the preliminary characterizations of 13 new viruses isolated from seven different ancient Siberian permafrost samples, one from the Lena river and one from Kamchatka cryosol. As expected from the host specificity imposed by our protocol, these viruses belong to five different clades infectingAcanthamoeba spp. but not previously revived from permafrost: Pandoravirus, Cedratvirus, Megavirus, and Pacmanvirus, in addition to a new Pithovirus strain.

Keywords: Acanthamoeba; Kamchatka; Pleistocene; Siberia; giant virus; permafrost.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

**Figure 1**
Morphological features guiding the preliminary identification of newly isolated viruses (negative staining, TEM). (A) The large ovoid particle (1000 nm in length) ofPandoravirus yedoma (strain Y2) (sample #5 in Table 1) showing the apex ostiole (white arrowhead) and the thick tegument characteristic of thePandoraviridae family. (B) A mixture ofPandoravirus mammoth (strain Yana14) oblate particles and ofMegavirus mammoth (strain Yana14) icosahedral particles exhibiting a “stargate” (white starfish-like structure crowning a vertex, white arrowhead) as seen in sample #7 (Table 1). (C) The elongated particle ofCedratvirus lena (strain DY0) (1500 nm in length) exhibits two apex cork-like structures (white arrowheads) (sample #2, Table 1). (D) The elongated particle ofPithovirus mammoth (1800 nm in length) (sample #7, Table 1) exhibiting a single apex cork-like structure (white arrowhead). (E) The large (770 nm in diameter) “hairy” icosahedral particle ofMegavirus mammoth (strain Yana14), showing the “stargate” (white arrowhead) characteristic of theMegavirinae subfamily (sample #7, Table 1). (F) The smaller icosahedral particle (200 nm in diameter) ofPacmanvirus lupus (strain Tums2) (sample #9, Table 1) typical of asfarviruses/pacmanviruses.

**Figure 2**
Maximum-likelihood phylogenetic relationships of the available Pandoravirus isolates. The tree (rooted at midpoint) was built using IQ-TREE (version 1.6.2) [54] from 2067 gap-free sites in the multiple alignment of 17 RNA polymerases (RPB1) protein (best fit model: “JTT + F + I + G4”). The permafrost isolates (in bold) are distributed between the two separatePandoraviridae clades previously documented [55]. Accession numbers are indicated following the isolate name when available.

**Figure 3**
Maximum-likelihood phylogenetic relationships of the closestPacmanvirus lupus relatives (using RPB1 homologs, Table 7). The tree (rooted at midpoint) was built using IQ-TREE (version 1.6.2) [54] (best fit model: “LG + F + I + G4”). The two closestMimiviridae RPB1 sequences are used as an outgroup. The tree was built from 1314 gap-free sites in the multiple alignment of 9 RNA polymerases (RPB1) protein sequences. AlthoughPacmanvirus lupus is well clustered with other pacmanviruses, this clade (together with faustovirus) appears more as a sister group rather thanbona fide members within theAsfarviridae (ASFV) family. Accession numbers are indicated following the isolate name when available.

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References

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An Update on Eukaryotic Viruses Revived from Ancient Permafrost

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An Update on Eukaryotic Viruses Revived from Ancient Permafrost

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Conflict of interest statement

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