Stable coexistence between an archaeal virus and the dominant methanogen of the human gut

Diana P. Baquero, Sofia Medvedeva, Camille Martin-Gallausiaux, Nika Pende, Anna Sartori-Rupp, Stéphane Tachon, Thierry Pedron, Laurent Debarbieux, Guillaume Borrel, Simonetta Gribaldo () and Mart Krupovic ()
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Diana P. Baquero: Archaeal Virology Unit
Sofia Medvedeva: Unit Evolutionary Biology of the Microbial Cell
Camille Martin-Gallausiaux: Unit Evolutionary Biology of the Microbial Cell
Nika Pende: Unit Evolutionary Biology of the Microbial Cell
Anna Sartori-Rupp: Centre de Ressources et Recherches Technologiques (C2RT)
Stéphane Tachon: Centre de Ressources et Recherches Technologiques (C2RT)
Thierry Pedron: Bacteriophage Bacterium Host
Laurent Debarbieux: Bacteriophage Bacterium Host
Guillaume Borrel: Unit Evolutionary Biology of the Microbial Cell
Simonetta Gribaldo: Unit Evolutionary Biology of the Microbial Cell
Mart Krupovic: Archaeal Virology Unit

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: Abstract The human gut virome, which is mainly composed of bacteriophages, also includes viruses infecting archaea, yet their role remains poorly understood due to lack of isolates. Here, we characterize a temperate archaeal virus (MSTV1) infecting Methanobrevibacter smithii, the dominant methanogenic archaeon of the human gut. The MSTV1 genome is integrated in the host chromosome as a provirus which is sporadically induced, resulting in virion release. Using cryo-electron tomography, we capture several intracellular virion assembly intermediates and confirm that only a small fraction of the host population actively produces virions in vitro. Similar low frequency of induction is observed in a mouse colonization model, using mice harboring a stable consortium of 12 bacterial species (OMM12). Transcriptomic analysis suggests a regulatory lysogeny-lysis switch involving an interplay between viral proteins to maintain virus-host equilibrium, ensuring host survival and viral persistence. Thus, our study sheds light on archaeal virus-host interactions and highlights similarities with bacteriophages in establishing stable coexistence with their hosts in the gut.

Date: 2024
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DOI: 10.1038/s41467-024-51946-x

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