Interplay of intracellular and trans‐cellular DNA methylation in natural archaeal consortia

Author:

Reva Oleg N.1ORCID,La Cono Violetta2ORCID,Crisafi Francesca2ORCID,Smedile Francesco2ORCID,Mudaliyar Manasi34ORCID,Ghosal Debnath34ORCID,Giuliano Laura5ORCID,Krupovic Mart6ORCID,Yakimov Michail M.2ORCID

Affiliation:

1. Department of Biochemistry, Genetics and Microbiology, Centre for Bioinformatics and Computational Biology University of Pretoria Pretoria South Africa

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

3. Department of Biochemistry and Pharmacology, Bio21 Molecular Science and Biotechnology Institute The University of Melbourne Melbourne Victoria Australia

4. ARC Centre for Cryo‐electron Microscopy of Membrane Proteins, Bio21 Molecular Science and Biotechnology Institute University of Melbourne Parkville Victoria Australia

5. Mediterranean Science Commission (CIESM) Monaco

6. Istitut Pasteur, Archaeal Virology Unit Université Paris Cité Paris France

Abstract

AbstractDNA methylation serves a variety of functions across all life domains. In this study, we investigated archaeal methylomics within a tripartite xylanolytic halophilic consortium. This consortium includes Haloferax lucertense SVX82, Halorhabdus sp. SVX81, and an ectosymbiotic Candidatus Nanohalococcus occultus SVXNc, a nano‐sized archaeon from the DPANN superphylum. We utilized PacBio SMRT and Illumina cDNA sequencing to analyse samples from consortia of different compositions for methylomics and transcriptomics. Endogenous cTAG methylation, typical of Haloferax, was accompanied in this strain by methylation at four other motifs, including GDGcHC methylation, which is specific to the ectosymbiont. Our analysis of the distribution of methylated and unmethylated motifs suggests that autochthonous cTAG methylation may influence gene regulation. The frequency of GRAGAaG methylation increased in highly expressed genes, while CcTTG and GTCGaGG methylation could be linked to restriction‐modification (RM) activity. Generally, the RM activity might have been reduced during the evolution of this archaeon to balance the protection of cells from intruders, the reduction of DNA damage due to self‐restriction in stressful environments, and the benefits of DNA exchange under extreme conditions. Our methylomics, transcriptomics and complementary electron cryotomography (cryo‐ET) data suggest that the nanohaloarchaeon exports its methyltransferase to methylate the Haloferax genome, unveiling a new aspect of the interaction between the symbiont and its host.

Funder

National Health and Medical Research Council

Agence Nationale de la Recherche

HORIZON EUROPE European Research Council

Publisher

Wiley

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