Abstract
Endosymbiosis is a widespread phenomenon in the microbial world and can be based on diverse interactions between endosymbiont and host cell. The vast majority of the known endosymbiotic interactions involve bacteria that have invaded eukaryotic host cells. However, methanogenic archaea have been found to thrive in anaerobic, hydrogenosome-containing protists and it was suggested that this symbiosis is based on the transfer of hydrogen. Here, we used culture-independent genomics approaches to sequence the genomes of two distantly related methanogenic endosymbionts that have been acquired in two independent events by closely related anaerobic ciliate hosts Nyctotherus ovalis and Metopus contortus, respectively. The sequences obtained were then validated as originating from the ciliate endosymbionts by in situ probing experiments. Comparative analyses of these genomes and their closest free-living counterparts reveal that the genomes of both endosymbionts are in an early stage of adaptation towards endosymbiosis as evidenced by the large number of genes undergoing pseudogenization. For instance, the observed loss of genes involved in amino acid biosynthesis in both endosymbiont genomes indicates that the endosymbionts rely on their hosts for obtaining several essential nutrients. Furthermore, the endosymbionts appear to have gained significant amounts of genes of potentially secreted proteins, providing targets for future studies aiming to elucidate possible mechanisms underpinning host-interactions. Altogether, our results provide the first genomic insights into prokaryotic endosymbioses from the archaeal domain of life.
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Acknowledgements
We thank Prof. Genoveva Esteban for help in isolating and identifying cultures of M. contortus, and we are grateful to Dr. Nicole Poulton for the initial evaluation of N. ovalis lysates. We would also like to thank Roel van Eijk and Lina Juzokaite for their help with sequencing library construction and Daniel Lundblad for his help in establishing cockroach cultivation. All sequencing was performed by the National Genomics Infrastructure sequencing platforms at the Science for Life Laboratory at Uppsala University, a national infrastructure supported by the Swedish Research Council (VR-RFI) and the Knut and Alice Wallenberg Foundation. We thank the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) at Uppsala University and the Swedish National Infrastructure for Computing (SNIC) at the PDC Center for High-Performance Computing for providing computational resources. This work was supported by grants of the Swedish Research Council (VR grant 621-2009-4813), the European Research Council (ERC Starting grant 310039-PUZZLE_CELL) and the Swedish Foundation for Strategic Research (SSF-FFL5) to TJGE and to TME (ERC Advanced grant 20100317-EUKORIGINMIT).
Author contributions
TJGE conceived and supervised the study. AEL isolated the endosymbionts and performed genomic sequence assemblies and analysis. AEL performed comparative genomics and phylogenomics analyses with occasional support from LG. WHL and TME isolated and cultured M. contortus samples and performed the fluorescent in situ hybridization experiments, as well as microscopic imaging. AS performed the metabolic analysis. AEL and TJGE wrote the manuscript, which was edited and approved by all authors.
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Lind, A.E., Lewis, W.H., Spang, A. et al. Genomes of two archaeal endosymbionts show convergent adaptations to an intracellular lifestyle. ISME J 12, 2655–2667 (2018). https://doi.org/10.1038/s41396-018-0207-9
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DOI: https://doi.org/10.1038/s41396-018-0207-9
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