Large freshwater phages with the potential to augment aerobic methane oxidation

Chen, Lin-Xing; Méheust, Raphaël; Crits-Christoph, Alexander; McMahon, Katherine D.; Nelson, Tara Colenbrander; Slater, Gregory F.; Warren, Lesley A.; Banfield, Jillian F.

doi:10.1038/s41564-020-0779-9

Title: Large freshwater phages with the potential to augment aerobic methane oxidation

Journal Article · Mon Aug 24 00:00:00 EDT 2020 · Nature Microbiology

DOI:https://doi.org/10.1038/s41564-020-0779-9· OSTI ID:1816092

^[1];

^[1]; Crits-Christoph, Alexander ^[2]; McMahon, Katherine D. ^[3]; Nelson, Tara Colenbrander ^[4]; Slater, Gregory F. ^[5]; Warren, Lesley A. ^[6];

^[7]

Univ. of California, Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
Univ. of Wisconsin, Madison, WI (United States). Dept. of Civil and Environmental Engineering, and Bacteriology
Univ. of Toronto, ON (Canada). Dept. of Civil and Mineral Engineering
McMaster Univ., Hamilton, ON (Canada). School of Geography and Earth Science
Univ. of Toronto, ON (Canada). Dept. of Civil and Mineral Engineering; McMaster Univ., Hamilton, ON (Canada). School of Geography and Earth Science
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences

There is growing evidence that phages with unusually large genomes are common across various microbiomes, but little is known about their genetic inventories or potential ecosystem impacts. In the present study, we reconstructed large phage genomes from freshwater lakes known to contain bacteria that oxidize methane. Of manually curated genomes, 22 (18 are complete), ranging from 159 kilobase (kb) to 527 kb in length, were found to encode the pmoC gene, an enzymatically critical subunit of the particulate methane monooxygenase, the predominant methane oxidation catalyst in nature. The phage-associated PmoC sequences show high similarity to (>90%), and affiliate phylogenetically with, those of coexisting bacterial methanotrophs, including members of Methyloparacoccus, Methylocystis and Methylobacter spp. In addition, pmoC-phage abundance patterns correlate with those of the coexisting bacterial methanotrophs, supporting host–phage relationships. Future work is needed to determine whether phage-associated PmoC has similar functions to additional copies of PmoC encoded in bacterial genomes, thus contributing to growth on methane. Transcriptomics data from Lake Rotsee (Switzerland) showed that some phage-associated pmoC genes were highly expressed in situ and, of interest, that the most rapidly growing methanotroph was infected by three pmoC-phages. Thus, augmentation of bacterial methane oxidation by pmoC-phages during infection could modulate the efflux of this potent greenhouse gas into the environment.

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Research Organization:: Univ. of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1816092

Journal Information:: Nature Microbiology, Vol. 5, Issue 12; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (78)

Particulate methane monooxygenase contains only mononuclear copper centers Ross, Matthew O.; MacMillan, Fraser; Wang, Jingzhou Science, Vol. 364, Issue 6440 https://doi.org/10.1126/science.aav2572	journal	May 2019
Bacterial photosynthesis genes in a virus Mann, Nicholas H.; Cook, Annabel; Millard, Andrew Nature, Vol. 424, Issue 6950 https://doi.org/10.1038/424741a	journal	August 2003
Sulfur Oxidation Genes in Diverse Deep-Sea Viruses Anantharaman, K.; Duhaime, M. B.; Breier, J. A. Science, Vol. 344, Issue 6185 https://doi.org/10.1126/science.1252229	journal	May 2014
Methanotrophs and copper Semrau, Jeremy D.; DiSpirito, Alan A.; Yoon, Sukhwan FEMS Microbiology Reviews, Vol. 34, Issue 4 https://doi.org/10.1111/j.1574-6976.2010.00212.x	journal	July 2010
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data Kearse, M.; Moir, R.; Wilson, A. Bioinformatics, Vol. 28, Issue 12 https://doi.org/10.1093/bioinformatics/bts199	journal	April 2012
Benzene and Naphthalene Degrading Bacterial Communities in an Oil Sands Tailings Pond Rochman, Fauziah F.; Sheremet, Andriy; Tamas, Ivica Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01845	journal	September 2017
A century of the phage: past, present and future Salmond, George P. C.; Fineran, Peter C. Nature Reviews Microbiology, Vol. 13, Issue 12 https://doi.org/10.1038/nrmicro3564	journal	November 2015
Expression of Individual Copies of Methylococcus capsulatus Bath Particulate Methane Monooxygenase Genes Stolyar, S.; Franke, M.; Lidstrom, M. E. Journal of Bacteriology, Vol. 183, Issue 5 https://doi.org/10.1128/JB.183.5.1810-1812.2001	journal	March 2001
Host-linked soil viral ecology along a permafrost thaw gradient Emerson, Joanne B.; Roux, Simon; Brum, Jennifer R. Nature Microbiology, Vol. 3, Issue 8 https://doi.org/10.1038/s41564-018-0190-y	journal	July 2018
Accurate and complete genomes from metagenomes Chen, Lin-Xing; Anantharaman, Karthik; Shaiber, Alon Genome Research, Vol. 30, Issue 3 https://doi.org/10.1101/gr.258640.119	journal	March 2020
KEGG: new perspectives on genomes, pathways, diseases and drugs Kanehisa, Minoru; Furumichi, Miho; Tanabe, Mao Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw1092	journal	November 2016
The distinction of CPR bacteria from other bacteria based on protein family content Méheust, Raphaël; Burstein, David; Castelle, Cindy J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12171-z	journal	September 2019
Biological Methane Oxidation: Regulation, Biochemistry, and Active Site Structure of Particulate Methane Monooxygenase Lieberman, Raquel L.; Rosenzweig, Amy C. Critical Reviews in Biochemistry and Molecular Biology, Vol. 39, Issue 3 https://doi.org/10.1080/10409230490475507	journal	January 2004
Biogeochemical aspects of atmospheric methane Cicerone, R. J.; Oremland, R. S. Global Biogeochemical Cycles, Vol. 2, Issue 4 https://doi.org/10.1029/GB002i004p00299	journal	December 1988
Contribution of oxic methane production to surface methane emission in lakes and its global importance Günthel, Marco; Donis, Daphne; Kirillin, Georgiy Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13320-0	journal	December 2019
Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes Ahlgren, Nathan A.; Fuchsman, Clara A.; Rocap, Gabrielle The ISME Journal, Vol. 13, Issue 3 https://doi.org/10.1038/s41396-018-0289-4	journal	October 2018
UniRef: comprehensive and non-redundant UniProt reference clusters Suzek, B. E.; Huang, H.; McGarvey, P. Bioinformatics, Vol. 23, Issue 10 https://doi.org/10.1093/bioinformatics/btm098	journal	March 2007
Bacteriophages of methanotrophs isolated from fish Tyutikov, F. M.; Yesipova, V. V.; Rebentish, B. A. Applied and Environmental Microbiology, Vol. 46, Issue 4 https://doi.org/10.1128/aem.46.4.917-924.1983	journal	October 1983
The Potential Role of Halothiobacillus spp. in Sulfur Oxidation and Acid Generation in Circum-Neutral Mine Tailings Reservoirs Whaley-Martin, Kelly; Jessen, Gerdhard L.; Nelson, Tara Colenbrander Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00297	journal	March 2019
Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake Mori, Jiro F.; Chen, Lin-Xing; Jessen, Gerdhard L. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02435	journal	October 2019
Metagenomics of Hydrocarbon Resource Environments Indicates Aerobic Taxa and Genes to be Unexpectedly Common An, Dongshan; Caffrey, Sean M.; Soh, Jung Environmental Science & Technology, Vol. 47, Issue 18 https://doi.org/10.1021/es4020184	journal	September 2013
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence Lowe, Todd M.; Eddy, Sean R. Nucleic Acids Research, Vol. 25, Issue 5 https://doi.org/10.1093/nar/25.5.955	journal	March 1997
NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins Pruitt, K. D.; Tatusova, T.; Maglott, D. R. Nucleic Acids Research, Vol. 35, Issue Database https://doi.org/10.1093/nar/gkl842	journal	January 2007
Hidden Markov model speed heuristic and iterative HMM search procedure Johnson, L. Steven; Eddy, Sean R.; Portugaly, Elon BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-431	journal	August 2010
Candidate Phyla Radiation Roizmanbacteria From Hot Springs Have Novel and Unexpectedly Abundant CRISPR-Cas Systems Chen, Lin-Xing; Al-Shayeb, Basem; Méheust, Raphaël Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00928	journal	May 2019
From micelles to bicelles: Effect of the membrane on particulate methane monooxygenase activity Ro, Soo Y.; Ross, Matthew O.; Deng, Yue Wen Journal of Biological Chemistry, Vol. 293, Issue 27 https://doi.org/10.1074/jbc.RA118.003348	journal	May 2018
Vertical Distribution of Methanogens in the Anoxic Sediment of Rotsee (Switzerland) Zepp Falz, K.; Holliger, C.; Großkopf, R. Applied and Environmental Microbiology, Vol. 65, Issue 6 https://doi.org/10.1128/AEM.65.6.2402-2408.1999	journal	June 1999
Enzymatic Oxidation of Methane Sirajuddin, Sarah; Rosenzweig, Amy C. Biochemistry, Vol. 54, Issue 14 https://doi.org/10.1021/acs.biochem.5b00198	journal	March 2015
Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses Roux, Simon; Brum, Jennifer R.; Dutilh, Bas E. Nature, Vol. 537, Issue 7622 https://doi.org/10.1038/nature19366	journal	September 2016
Methanotrophic bacteria in oilsands tailings ponds of northern Alberta Saidi-Mehrabad, Alireza; He, Zhiguo; Tamas, Ivica The ISME Journal, Vol. 7, Issue 5 https://doi.org/10.1038/ismej.2012.163	journal	December 2012
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities Kang, Dongwan D.; Froula, Jeff; Egan, Rob PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1165	journal	January 2015
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments: Comparative genomics of T4-like myoviruses Sullivan, Matthew B.; Huang, Katherine H.; Ignacio-Espinoza, Julio C. Environmental Microbiology, Vol. 12, Issue 11 https://doi.org/10.1111/j.1462-2920.2010.02280.x	journal	November 2010
Bacteriophages of methanotrophic bacteria Tyutikov, F. M.; Bespalova, I. A.; Rebentish, B. A. Journal of Bacteriology, Vol. 144, Issue 1 https://doi.org/10.1128/jb.144.1.375-381.1980	journal	October 1980
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
The HHpred interactive server for protein homology detection and structure prediction Soding, J.; Biegert, A.; Lupas, A. N. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki408	journal	July 2005
Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia Dunfield, Peter F.; Yuryev, Anton; Senin, Pavel Nature, Vol. 450, Issue 7171 https://doi.org/10.1038/nature06411	journal	November 2007
Photosynthesis genes in marine viruses yield proteins during host infection Lindell, Debbie; Jaffe, Jacob D.; Johnson, Zackary I. Nature, Vol. 438, Issue 7064 https://doi.org/10.1038/nature04111	journal	October 2005
Differential expression of particulate methane monooxygenase genes in the verrucomicrobial methanotroph ‘Methylacidiphilum kamchatkense’ Kam1 Erikstad, Helge-André; Jensen, Sigmund; Keen, T. Jeffrey Extremophiles, Vol. 16, Issue 3 https://doi.org/10.1007/s00792-012-0439-y	journal	April 2012
Comparative analysis of metagenomes from three methanogenic hydrocarbon-degrading enrichment cultures with 41 environmental samples Tan, Boonfei; Jane Fowler, S.; Laban, Nidal Abu The ISME Journal, Vol. 9, Issue 9 https://doi.org/10.1038/ismej.2015.22	journal	March 2015
Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia : Perspectives on methanotrophic Op den Camp, Huub J. M.; Islam, Tajul; Stott, Matthew B. Environmental Microbiology Reports, Vol. 1, Issue 5 https://doi.org/10.1111/j.1758-2229.2009.00022.x	journal	March 2009
Methyloparacoccus murrellii gen. nov., sp. nov., a methanotroph isolated from pond water Hoefman, S.; van der Ha, D.; Iguchi, H. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 6 https://doi.org/10.1099/ijs.0.057760-0	journal	March 2014
Uncovering Earth’s virome Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A. Nature, Vol. 536, Issue 7617 https://doi.org/10.1038/nature19094	journal	August 2016
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes Pruesse, Elmar; Peplies, Jörg; Glöckner, Frank Oliver Bioinformatics, Vol. 28, Issue 14 https://doi.org/10.1093/bioinformatics/bts252	journal	May 2012
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
The TIGRFAMs database of protein families Haft, D. H. Nucleic Acids Research, Vol. 31, Issue 1 https://doi.org/10.1093/nar/gkg128	journal	January 2003
CRISPR Recognition Tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats Bland, Charles; Ramsey, Teresa L.; Sabree, Fareedah BMC Bioinformatics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2105-8-209	journal	June 2007
Freshwater carbon and nutrient cycles revealed through reconstructed population genomes Linz, Alexandra M.; He, Shaomei; Stevens, Sarah L. R. PeerJ, Vol. 6 https://doi.org/10.7717/peerj.6075	journal	January 2018
UniProt: the Universal Protein knowledgebase Apweiler, R. Nucleic Acids Research, Vol. 32, Issue 90001 https://doi.org/10.1093/nar/gkh131	journal	January 2004
Unusual biology across a group comprising more than 15% of domain Bacteria Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C. Nature, Vol. 523, Issue 7559 https://doi.org/10.1038/nature14486	journal	June 2015
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism Thompson, L. R.; Zeng, Q.; Kelly, L. Proceedings of the National Academy of Sciences, Vol. 108, Issue 39 https://doi.org/10.1073/pnas.1102164108	journal	August 2011
MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets Steinegger, Martin; Söding, Johannes Nature Biotechnology, Vol. 35, Issue 11 https://doi.org/10.1038/nbt.3988	journal	October 2017
Photosystem I gene cassettes are present in marine virus genomes Sharon, Itai; Alperovitch, Ariella; Rohwer, Forest Nature, Vol. 461, Issue 7261 https://doi.org/10.1038/nature08284	journal	August 2009
The co-importance of physical mixing and biogeochemical consumption in controlling water cap oxygen levels in Base Mine Lake Arriaga, Daniel; Nelson, Tara Colenbrander; Risacher, Florent F. Applied Geochemistry, Vol. 111 https://doi.org/10.1016/j.apgeochem.2019.104442	journal	December 2019
Measurement of bacterial replication rates in microbial communities Brown, Christopher T.; Olm, Matthew R.; Thomas, Brian C. Nature Biotechnology, Vol. 34, Issue 12 https://doi.org/10.1038/nbt.3704	journal	November 2016
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
The interplay of methane and ammonia as key oxygen consuming constituents in early stage development of Base Mine Lake, the first demonstration oil sands pit lake Risacher, Florent F.; Morris, Patrick K.; Arriaga, Daniel Applied Geochemistry, Vol. 93 https://doi.org/10.1016/j.apgeochem.2018.03.013	journal	June 2018
A new view of the tree of life Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.48	journal	April 2016
Linking Virus Genomes with Host Taxonomy Mihara, Tomoko; Nishimura, Yosuke; Shimizu, Yugo Viruses, Vol. 8, Issue 3 https://doi.org/10.3390/v8030066	journal	March 2016
Clades of huge phages from across Earth’s ecosystems Al-Shayeb, Basem; Sachdeva, Rohan; Chen, Lin-Xing Nature, Vol. 578, Issue 7795 https://doi.org/10.1038/s41586-020-2007-4	journal	February 2020
Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane Lieberman, Raquel L.; Rosenzweig, Amy C. Nature, Vol. 434, Issue 7030 https://doi.org/10.1038/nature03311	journal	January 2005
ViPTree: the viral proteomic tree server Nishimura, Yosuke; Yoshida, Takashi; Kuronishi, Megumi Bioinformatics, Vol. 33, Issue 15 https://doi.org/10.1093/bioinformatics/btx157	journal	March 2017
HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment Remmert, Michael; Biegert, Andreas; Hauser, Andreas Nature Methods, Vol. 9, Issue 2 https://doi.org/10.1038/nmeth.1818	journal	December 2011
Aquatic and terrestrial cyanobacteria produce methane Bižić, M.; Klintzsch, T.; Ionescu, D. Science Advances, Vol. 6, Issue 3 https://doi.org/10.1126/sciadv.aax5343	journal	January 2020
A large-scale evaluation of algorithms to calculate average nucleotide identity Yoon, Seok-Hwan; Ha, Sung-min; Lim, Jeongmin Antonie van Leeuwenhoek, Vol. 110, Issue 10 https://doi.org/10.1007/s10482-017-0844-4	journal	February 2017
Mutagenesis of the hydrocarbon monooxygenase indicates a metal centre in subunit-C, and not subunit-B, is essential for copper-containing membrane monooxygenase activity Liew, E. F.; Tong, D.; Coleman, N. V. Microbiology, Vol. 160, Issue Pt_6 https://doi.org/10.1099/mic.0.078584-0	journal	March 2014
Transcription of All amoC Copies Is Associated with Recovery of Nitrosomonas europaea from Ammonia Starvation Berube, Paul M.; Samudrala, Ram; Stahl, David A. Journal of Bacteriology, Vol. 189, Issue 11 https://doi.org/10.1128/JB.01861-06	journal	June 2007
An efficient algorithm for large-scale detection of protein families Enright, A. J. Nucleic Acids Research, Vol. 30, Issue 7 https://doi.org/10.1093/nar/30.7.1575	journal	April 2002
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Role of multiple gene copies in particulate methane monooxygenase activity in the methane-oxidizing bacterium Methylococcus capsulatus Bath Stolyar, S.; Costello, A. M.; Peeples, T. L. Microbiology, Vol. 145, Issue 5 https://doi.org/10.1099/13500872-145-5-1235	journal	May 1999
CD-HIT Suite: a web server for clustering and comparing biological sequences Huang, Ying; Niu, Beifang; Gao, Ying Bioinformatics, Vol. 26, Issue 5 https://doi.org/10.1093/bioinformatics/btq003	journal	January 2010
Microbiology and potential applications of aerobic methane oxidation coupled to denitrification (AME-D) process: A review Zhu, Jing; Wang, Qian; Yuan, Mengdong Water Research, Vol. 90 https://doi.org/10.1016/j.watres.2015.12.020	journal	March 2016
Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations Bendall, Matthew L.; Stevens, Sarah LR; Chan, Leong-Keat The ISME Journal, Vol. 10, Issue 7 https://doi.org/10.1038/ismej.2015.241	journal	January 2016
The distinction of CPR bacteria from other bacteria based on protein family content Meheust, Raphael figshare https://doi.org/10.6084/m9.figshare.6296987	dataset	January 2019
The distinction of CPR bacteria from other bacteria based on protein family content Meheust, Raphael figshare https://doi.org/10.6084/m9.figshare.6296987.v3	dataset	January 2019

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