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Evolutionary Diversification of Methanotrophic Ca. Methanophagales (ANME-1) and Their Expansive Virome

Laso-Pérez, Rafael and Wu, Fabai and Crémière, Antoine and Speth, Daan R. and Magyar, John S. and Krupovic, Mart and Orphan, Victoria J. (2022) Evolutionary Diversification of Methanotrophic Ca. Methanophagales (ANME-1) and Their Expansive Virome. . (Unpublished)

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‘Candidatus Methanophagales’ (ANME-1) is a major order-level clade of archaea responsible for methane removal in deep-sea sediments through anaerobic oxidation of methane. Yet the extent of their diversity and factors which drive their dynamics and evolution remain poorly understood. Here, by sampling hydrothermal rocks and sediments, we expand their phylogenetic diversity and characterize a new deep-branching, thermophilic ANME-1 family, ‘Candidatus Methanoxibalbaceae’ (ANME-1c). They are phylogenetically closest to the short-chain-alkane oxidizers ‘Candidatus Syntrophoarchaeales’ and ‘Candidatus Alkanophagales’, and encode ancestral features including a methyl coenzyme M reductase chaperone McrD and a hydrogenase complex. Global phylogeny and near-complete genomes clarified that the debated hydrogen metabolism within ANME-1 is an ancient trait that was vertically inherited but differentially lost during lineage diversification. Our expanded genomic and metagenomic sampling allowed the discovery of viruses constituting 3 new orders and 16 new families that so far are exclusive to ANME-1 hosts. These viruses represent 4 major archaeal virus assemblages, characterized by tailless icosahedral, head-tailed, rod-shaped, and spindle-shaped virions, but display unique structural and replicative signatures. Exemplified by the analyses of thymidylate synthases that unveiled a virus-mediated ancestral process of host gene displacement, this expansive ANME-1 virome carries a large gene repertoire that can influence their hosts across different timescales. Our study thus puts forth an emerging evolutionary continuum between anaerobic methane and short-chain-alkane oxidizers and opens doors for exploring the impacts of viruses on the dynamics and evolution of the anaerobic methane-driven ecosystems.

Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription Paper Information ItemCode
Laso-Pérez, Rafael0000-0002-6912-7865
Wu, Fabai0000-0001-5812-5621
Crémière, Antoine0000-0001-7382-2097
Speth, Daan R.0000-0002-2361-5935
Magyar, John S.0000-0002-3586-8286
Krupovic, Mart0000-0001-5486-0098
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. We are indebted to the crews from R/V Falkor (cruise FK181031) and E/V Nautilus (cruise NA091) and the pilots of ROVs SuBastian and Hercules. Sample collection permits for FK181031 (25/07/2018) 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 / Dirección General de Cooperación Técnica y Científica. Sample collection permit for cruise NA091 (18/04/2017) 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 Center For Dark Energy Biosphere Investigations (C-DEBI) and the NOMIS foundation (V.J.O.). VJO contribution was supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research under Award Number DE-SC0020373. This work was also supported by the Deutsche Forschungsgemeinschaft (DFG, 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 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. Author contributions. R. L.-P., F.W., A.C., and V.J.O. conceived and designed the study. D.R.S, V.J.O. and J.S.M. retrieved the original samples. A.C. and F.W. carried out rock incubations and FISH 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. R.L.-P., F.W., M.K. and V.J.O wrote the manuscript with contributions from all coauthors. We declare no competing financial interests. Data availability. All MAGs and sequence data can be found in the figshare link (except some large libraries), and will be deposited onto NCBI database prior to peer-reviewed publication. This report was prepared as an account of work sponsored by an agency of the United States Government. Neither the United States Government nor any agency thereof, nor 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 United States Government or any agency thereof. The views and opinions of authors expressed herein do not necessarily state or reflect those of the United States Government or any agency thereof.
Funding AgencyGrant Number
Ocean Exploration TrustUNSPECIFIED
Dalio FoundationUNSPECIFIED
Woods Hole Oceanographic InstitutionUNSPECIFIED
Department of Energy (DOE)DE-SC0020373
Deutsche Forschungsgemeinschaft (DFG)EXC-2077-390741603
Agence Nationale de la Recherche (ANR)ANR-20-CE20-0009-02
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)019.162LW.037
Human Frontier Science ProgramLT000468
Zhejiang UniversityUNSPECIFIED
Record Number:CaltechAUTHORS:20220808-886882000
Persistent URL:
Official Citation:Evolutionary Diversification of Methanotrophic Ca. Methanophagales (ANME-1) and Their Expansive Virome Rafael Laso-Pérez, Fabai Wu, Antoine Crémière, Daan R. Speth, John S. Magyar, Mart Krupovic, Victoria J. Orphan bioRxiv 2022.07.04.498658; doi:
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:116176
Deposited By: George Porter
Deposited On:12 Aug 2022 20:56
Last Modified:12 Aug 2022 20:56

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