Chromosome-scale assemblies of Acanthamoeba castellanii genomes provide insights into Legionella pneumophila infection-related chromatin reorganization [RESEARCH]

Cyril Matthey-Doret1,2,6, Morgan J. Colp3,6, Pedro Escoll4, Agnès Thierry1, Pierrick Moreau1, Bruce Curtis3, Tobias Sahr4, Matt Sarrasin5, Michael W. Gray3, B. Franz Lang5, John M. Archibald3, Carmen Buchrieser4 and Romain Koszul1 1Institut Pasteur, CNRS UMR 3525, Université de Paris, Unité Régulation Spatiale des Génomes, F-75015 Paris, France; 2Collège Doctoral, Sorbonne Université, F-75005 Paris, France; 3Department of Biochemistry and Molecular Biology and Institute for Comparative Genomics, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada; 4Institut Pasteur, Université de Paris, Biologie des Bactéries Intracellulaires and CNRS UMR 6047, F-75015 Paris, France; 5Robert Cedergren Centre for Bioinformatics and Genomics, Département de Biochimie, Université de Montréal, Montréal, Quebec H3C 3J7, Canada

6 These authors contributed equally to this work.

Corresponding authors: john.archibalddal.ca, cbuchpasteur.fr, romain.koszulpasteur.fr Abstract

The unicellular amoeba Acanthamoeba castellanii is ubiquitous in aquatic environments, where it preys on bacteria. The organism also hosts bacterial endosymbionts, some of which are parasitic, including human pathogens such as Chlamydia and Legionella spp. Here we report complete, high-quality genome sequences for two extensively studied A. castellanii strains, Neff and C3. Combining long- and short-read data with Hi-C, we generated near chromosome-level assemblies for both strains with 90% of the genome contained in 29 scaffolds for the Neff strain and 31 for the C3 strain. Comparative genomics revealed strain-specific functional enrichment, most notably genes related to signal transduction in the C3 strain and to viral replication in Neff. Furthermore, we characterized the spatial organization of the A. castellanii genome and showed that it is reorganized during infection by Legionella pneumophila. Infection-dependent chromatin loops were found to be enriched in genes for signal transduction and phosphorylation processes. In genomic regions where chromatin organization changed during Legionella infection, we found functional enrichment for genes associated with metabolism, organelle assembly, and cytoskeleton organization. Given Legionella infection is known to alter its host's cell cycle, to exploit the host's organelles, and to modulate the host's metabolism in its favor, these changes in chromatin organization may partly be related to mechanisms of host control during Legionella infection.

Received November 8, 2021. Accepted July 25, 2022.

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