Evolutionary diversification of methanotrophic ANME-1 archaea and their expansive virome

Creators: Laso-Pérez, Rafael; Wu, Fabai; Crémière, Antoine; Speth, Daan R.; Magyar, John S.; Zhao, Kehan; Krupovic, Mart; Orphan, Victoria J.

Abstract

'Candidatus Methanophagales' (ANME-1) is an order-level clade of archaea responsible for anaerobic methane oxidation in deep-sea sediments. The diversity, ecology and evolution of ANME-1 remain poorly understood. In this study, we use metagenomics on deep-sea hydrothermal samples to expand ANME-1 diversity and uncover the effect of virus–host dynamics. Phylogenetic analyses reveal a deep-branching, thermophilic family, 'Candidatus Methanospirareceae', closely related to short-chain alkane oxidizers. Global phylogeny and near-complete genomes show that hydrogen metabolism within ANME-1 is an ancient trait that was vertically inherited but differentially lost during lineage diversification. Metagenomics also uncovered 16 undescribed virus families so far exclusively targeting ANME-1 archaea, showing unique structural and replicative signatures. The expansive ANME-1 virome contains a metabolic gene repertoire that can influence host ecology and evolution through virus-mediated gene displacement. Our results suggest an evolutionary continuum between anaerobic methane and short-chain alkane oxidizers and underscore the effects of viruses on the dynamics and evolution of methane-driven ecosystems.

Additional Information

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. We thank G. Chadwick, H. Yu, R. Murali and A. Philosof for discussion, A. Narayanan for sequencing library preparation, S. Connon for technical support and S. Roux and A. Teske for IMG/VR-related data submission. We are indebted to the science parties and cochief scientists D. Caress (MBARI), R. Zierenberg (UC Davis), the crews from R/V Falkor (cruise FK181031) and E/V Nautilus (cruise NA091) and the pilots of ROVs SuBastian and Hercules. We also thank R. Speltz (Universidad Autónoma de Baja California) for consultation on species naming from the Kiliwa language. Sample collection permits for FK181031 (25 July 2018) were granted by la Dirección General de Ordenamiento Pesquero y Acuícola, Comisión Nacional de Acuacultura y Pesca (CONAPESCA: Permiso de Pesca de Fomento No. PPFE/DGOPA-200/18) and la Dirección General de Geografía y Medio Ambiente, Instituto Nacional de Estadística y Geografía (INEGI: Autorización EG0122018), with the associated Diplomatic Note number 18-2083 (CTC/07345/18) from la Secretaría de Relaciones Exteriores Agencia Mexicana de Cooperación Internacional para el Desarrollo and Dirección General de Cooperación Técnica y Científica. Sample collection permit for cruise NA091 (18 April 2017) was obtained by the Ocean Exploration Trust under permit number EG0072017. This research used samples provided by the Ocean Exploration Trust's Nautilus Exploration Program, cruise NA091. E/V Nautlius operated by the Ocean Exploration Trust, with cruise NA091 supported by the Dalio Foundation and Woods Hole Oceanographic Institute, and R/V Falkor operated by the Schmidt Ocean Institute. Funding for this work was provided by grants from the National Science Foundation STC Center For Dark Energy Biosphere Investigations, the NOMIS foundation and by the US Department of Energy, Office of Science, Office of Biological and Environmental Research under Award Number DE-SC0020373 to V.J.O. This work was also supported by the Deutsche Forschungsgemeinschaft (German Research Foundation) under Germany's Excellence Initiative/Strategy through the Cluster of Excellence 'The Ocean Floor-Earth's Uncharted Interface' (EXC-2077-390741603 R.L.-P. and V.J.O). M.K. was supported by l'Agence Nationale de la Recherche grant ANR-20-CE20-0009-02. F.W. was supported in part by the Dutch Research Council Rubicon Award 019.162LW.037, the Human Frontiers Science Program Long-term fellowship LT000468/2017 and a ZJU-HIC Independent PI Startup Grant. This report was prepared as an account of work sponsored by an agency of the US Government. Neither the US Government, any agency thereof, or any of their employees, makes any warranty, express or implied, or assumes any legal liability or responsibility for the accuracy, completeness or usefulness of any information, apparatus, product or process disclosed, or represents that its use would not infringe privately owned rights. Reference herein to any specific commercial product, process or service by trade name, trademark, manufacturer or otherwise does not necessarily constitute or imply its endorsement, recommendation, or favoring by the US Government or any agency thereof. The views and opinions of authors expressed herein do not necessarily state or reflect those of the US Government or any agency thereof. Open access funding provided by Staats- und Universitätsbibliothek Bremen. These authors contributed equally: Rafael Laso-Pérez, Fabai Wu. Contributions. R.L.-P., F.W., A.C. and V.J.O. conceptualized and designed the study. D.R.S., V.J.O. and J.S.M. participated in the oceanographic expedition and recovered and processed the original samples. A.C. and F.W. carried out rock incubations and fluorescence in situ hybridization microscopy. R.L.-P., F.W. and A.C. performed DNA extraction. R.L.-P. and F.W. performed metagenomic assembly and analysis. F.W. performed CRISPR-based mobilome discovery. M.K. and F.W. performed analyses of viruses. K.Z. organized and catalogued virus data. R.L.-P., F.W., M.K. and V.J.O wrote the manuscript with contributions from all coauthors. Data availability. Raw metagenome reads, assembled metagenome bins and virus sequence data are available in the NCBI database under BioProject accession numbers PRJNA875076 and PRJNA721962. Complete ANME-1 virus genomes representing new viral taxa can be found on GenBank under accession numbers OP413838, OP413839, OP413840, OP413841, OP548099, OP548100, OP880252, OP880253 and OP880254. CRISPR spacer sequences of ANME-1 and all genomic sequences of ANME-1 MGEs are also provided as supplementary data. For virus genomic analysis the following databases were used in this study: Protein Data Bank (namely, the major capsid protein of phage PM2, PDB id: 2vvf; https://www.rcsb.org/structure/2vvf), CDD v3.18, PHROG (https://phrogs.lmge.uca.fr/) and uniprot_sprot_vir70 (09/02/2021). The authors declare no competing interests.

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