Hot springs viruses at Yellowstone National Park have ancient origins and are adapted to thermophilic hosts

Benites, L. Felipe; Stephens, Timothy G.; Van Etten, Julia; James, Timeeka; Christian, William C.; Barry, Kerrie; Grigoriev, Igor V.; McDermott, Timothy R.; Bhattacharya, Debashish

doi:10.1038/s42003-024-05931-1

Title: Hot springs viruses at Yellowstone National Park have ancient origins and are adapted to thermophilic hosts

Journal Article · 09 April 2024 · Communications Biology

DOI: https://doi.org/10.1038/s42003-024-05931-1 · OSTI ID:2448327

Benites, L. Felipe ^[1]; Stephens, Timothy G. ^[1];

^[1]; James, Timeeka ^[1];

^[2];

^[3];

^[4]; McDermott, Timothy R. ^[2];

^[1]

The State University of New Jersey, New Brunswick, NJ (United States)
Montana State University, Bozeman, MT (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); University of California, Berkeley, CA (United States)

Geothermal springs house unicellular red algae in the class Cyanidiophyceae that dominate the microbial biomass at these sites. Little is known about host-virus interactions in these environments. We analyzed the virus community associated with red algal mats in three neighboring habitats (creek, endolithic, soil) at Lemonade Creek, Yellowstone National Park (YNP), USA. We find that despite proximity, each habitat houses a unique collection of viruses, with the giant viruses, Megaviricetes, dominant in all three. The early branching phylogenetic position of genes encoded on metagenome assembled virus genomes (vMAGs) suggests that the YNP lineages are of ancient origin and not due to multiple invasions from mesophilic habitats. The existence of genomic footprints of adaptation to thermophily in the vMAGs is consistent with this idea. The Cyanidiophyceae at geothermal sites originated ca. 1.5 Bya and are therefore relevant to understanding biotic interactions on the early Earth.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: NIFA-USDA; National Aeronautics and Space Administration (NASA); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2448327

Journal Information:: Communications Biology, Journal Name: Communications Biology Journal Issue: 1 Vol. 7; ISSN 2399-3642

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

References (100)

Transproteomic evidence of a loop-deletion mechanism for enhancing protein thermostability Thompson, Michael J.; Eisenberg, David Journal of Molecular Biology, Vol. 290, Issue 2 https://doi.org/10.1006/jmbi.1999.2889	journal	July 1999
Double-stranded RNA as a Not-self Alarm Signal: to Evade, most Viruses Purine-load their RNAs, but some (HTLV-1, Epstein-Barr) Pyrimidine-load Cristillo, A. D.; Mortimer, J. R.; Barrette, I. H. Journal of Theoretical Biology, Vol. 208, Issue 4 https://doi.org/10.1006/jtbi.2000.2233	journal	February 2001
SeqinR 1.0-2: A Contributed Package to the R Project for Statistical Computing Devoted to Biological Sequences Retrieval and Analysis Charif, Delphine; Lobry, Jean R. Structural Approaches to Sequence Evolution https://doi.org/10.1007/978-3-540-35306-5_10	book	January 2007
Optimum growth temperature and the base composition of open reading frames in prokaryotes Lambros, R. J.; Mortimer, J. R.; Forsdyke, D. R. Extremophiles, Vol. 7, Issue 6 https://doi.org/10.1007/s00792-003-0353-4	journal	December 2003
Analysis of structural requirements for thermo-adaptation from orthologs in microbial genomes Gao, Junxiang; Wang, Wei Annals of Microbiology, Vol. 62, Issue 4 https://doi.org/10.1007/s13213-012-0420-0	journal	February 2012
The ancestor of the Bacteria domain was a hyperthermophile Di Giulio, Massimo Journal of Theoretical Biology, Vol. 224, Issue 3 https://doi.org/10.1016/S0022-5193(03)00164-4	journal	October 2003
Microbiology of ancient and modern hydrothermal systems Reysenbach, Anna-Louise; Cady, Sherry L. Trends in Microbiology, Vol. 9, Issue 2 https://doi.org/10.1016/S0966-842X(00)01921-1	journal	February 2001
Major New Microbial Groups Expand Diversity and Alter our Understanding of the Tree of Life Castelle, Cindy J.; Banfield, Jillian F. Cell, Vol. 172, Issue 6 https://doi.org/10.1016/j.cell.2018.02.016	journal	March 2018
Large-scale genome sequencing reveals the driving forces of viruses in microalgal evolution Nelson, David R.; Hazzouri, Khaled M.; Lauersen, Kyle J. Cell Host & Microbe, Vol. 29, Issue 2 https://doi.org/10.1016/j.chom.2020.12.005	journal	February 2021
Paleovirology—ghosts and gifts of viruses past Patel, Maulik R.; Emerman, Michael; Malik, Harmit S. Current Opinion in Virology, Vol. 1, Issue 4 https://doi.org/10.1016/j.coviro.2011.06.007	journal	October 2011
Adaptation through horizontal gene transfer in the cryptoendolithic red alga Galdieria phlegrea Qiu, Huan; Price, Dana C.; Weber, Andreas P. M. Current Biology, Vol. 23, Issue 19 https://doi.org/10.1016/j.cub.2013.08.046	journal	October 2013
LysM proteins in mammalian fungal pathogens Oguiza, José A. Fungal Biology Reviews, Vol. 40 https://doi.org/10.1016/j.fbr.2022.02.001	journal	June 2022
Synonymous codon usage and its potential link with optimal growth temperature in prokaryotes Lobry, J. R.; Necşulea, A. Gene, Vol. 385 https://doi.org/10.1016/j.gene.2006.05.033	journal	December 2006
Extremophilic red algae as models for understanding adaptation to hostile environments and the evolution of eukaryotic life on the early earth Van Etten, Julia; Cho, Chung Hyun; Yoon, Hwan Su Seminars in Cell & Developmental Biology, Vol. 134 https://doi.org/10.1016/j.semcdb.2022.03.007	journal	January 2023
Viral assemblage composition in Yellowstone acidic hot springs assessed by network analysis Bolduc, Benjamin; Wirth, Jennifer F.; Mazurie, Aurélien The ISME Journal, Vol. 9, Issue 10 https://doi.org/10.1038/ismej.2015.28	journal	June 2015
Palaeotemperature trend for Precambrian life inferred from resurrected proteins Gaucher, Eric A.; Govindarajan, Sridhar; Ganesh, Omjoy K. Nature, Vol. 451, Issue 7179 https://doi.org/10.1038/nature06510	journal	February 2008
Microbial habitability of the Hadean Earth during the late heavy bombardment Abramov, Oleg; Mojzsis, Stephen J. Nature, Vol. 459, Issue 7245 https://doi.org/10.1038/nature08015	journal	May 2009
Minimum Information about an Uncultivated Virus Genome (MIUViG) Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E. Nature Biotechnology, Vol. 37, Issue 1 https://doi.org/10.1038/nbt.4306	journal	December 2018
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
ModelFinder: fast model selection for accurate phylogenetic estimates Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F. Nature Methods, Vol. 14, Issue 6 https://doi.org/10.1038/nmeth.4285	journal	May 2017
The physiology and habitat of the last universal common ancestor Weiss, Madeline C.; Sousa, Filipa L.; Mrnjavac, Natalia Nature Microbiology, Vol. 1, Issue 9 https://doi.org/10.1038/nmicrobiol.2016.116	journal	July 2016
Phage or foe: an insight into the impact of viral predation on microbial communities Fernández, Lucía; Rodríguez, Ana; García, Pilar The ISME Journal, Vol. 12, Issue 5 https://doi.org/10.1038/s41396-018-0049-5	journal	January 2018
Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere Abrahão, Jônatas; Silva, Lorena; Silva, Ludmila Santos Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03168-1	journal	February 2018
Diversity and evolution of the emerging Pandoraviridae family Legendre, Matthieu; Fabre, Elisabeth; Poirot, Olivier Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04698-4	journal	June 2018
Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains Bacteria and Archaea Zhu, Qiyun; Mai, Uyen; Pfeiffer, Wayne Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13443-4	journal	December 2019
Dynamic genome evolution and complex virocell metabolism of globally-distributed giant viruses Moniruzzaman, Mohammad; Martinez-Gutierrez, Carolina A.; Weinheimer, Alaina R. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15507-2	journal	April 2020
Past and present giant viruses diversity explored through permafrost metagenomics Rigou, Sofia; Santini, Sébastien; Abergel, Chantal Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-33633-x	journal	October 2022
Genome-wide signatures of adaptation to extreme environments in red algae Cho, Chung Hyun; Park, Seung In; Huang, Tzu-Yen Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-022-35566-x	journal	January 2023
Identification of a deep-branching thermophilic clade sheds light on early bacterial evolution Leng, Hao; Wang, Yinzhao; Zhao, Weishu Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-39960-x	journal	July 2023
Phage puppet masters of the marine microbial realm Breitbart, Mya; Bonnain, Chelsea; Malki, Kema Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0166-y	journal	June 2018
Viruses interact with hosts that span distantly related microbial domains in dense hydrothermal mats Hwang, Yunha; Roux, Simon; Coclet, Clément Nature Microbiology, Vol. 8, Issue 5 https://doi.org/10.1038/s41564-023-01347-5	journal	April 2023
Mirusviruses link herpesviruses to giant viruses Gaïa, Morgan; Meng, Lingjie; Pelletier, Eric Nature, Vol. 616, Issue 7958 https://doi.org/10.1038/s41586-023-05962-4	journal	April 2023
CheckV assesses the quality and completeness of metagenome-assembled viral genomes Nayfach, Stephen; Camargo, Antonio Pedro; Schulz, Frederik Nature Biotechnology, Vol. 39, Issue 5 https://doi.org/10.1038/s41587-020-00774-7	journal	December 2020
Identification of mobile genetic elements with geNomad Camargo, Antonio Pedro; Roux, Simon; Schulz, Frederik Nature Biotechnology https://doi.org/10.1038/s41587-023-01953-y	journal	September 2023
Deciphering the rationale behind specific codon usage pattern in extremophiles Khan, Mohd Faheem; Patra, Sanjukta Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33476-x	journal	October 2018
Four novel algal virus genomes discovered from Yellowstone Lake metagenomes Zhang, Weijia; Zhou, Jinglie; Liu, Taigang Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep15131	journal	October 2015
Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga Qin, J.; Lehr, C. R.; Yuan, C. Proceedings of the National Academy of Sciences, Vol. 106, Issue 13 https://doi.org/10.1073/pnas.0900238106	journal	March 2009
Complete genome sequence of the Q-fever pathogen Coxiella burnetii Seshadri, R.; Paulsen, I. T.; Eisen, J. A. Proceedings of the National Academy of Sciences, Vol. 100, Issue 9 https://doi.org/10.1073/pnas.0931379100	journal	April 2003
Experimental evidence for the thermophilicity of ancestral life Akanuma, S.; Nakajima, Y.; Yokobori, S. -i. Proceedings of the National Academy of Sciences, Vol. 110, Issue 27 https://doi.org/10.1073/pnas.1308215110	journal	June 2013
Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium Kawashima, Tsuyoshi; Amano, Naoki; Koike, Hideaki Proceedings of the National Academy of Sciences, Vol. 97, Issue 26 https://doi.org/10.1073/pnas.97.26.14257	journal	December 2000
Viruses of Rhodophyta: lack of cultures and genomic resources pose a threat to the growing red algal aquaculture industry Benites, L. Felipe; Alves-Lima, Cícero Applied Phycology, Vol. 3, Issue 1 https://doi.org/10.1080/26388081.2022.2059701	journal	May 2022
The Hot Spring Hypothesis for an Origin of Life Damer, Bruce; Deamer, David Astrobiology, Vol. 20, Issue 4 https://doi.org/10.1089/ast.2019.2045	journal	April 2020
CnnPOGTP: a novel CNN-based predictor for identifying the optimal growth temperatures of prokaryotes using only genomick-mers distribution Wang, Shaojing; Li, Guoqiang; Liao, Zitong Bioinformatics, Vol. 38, Issue 11 https://doi.org/10.1093/bioinformatics/btac289	journal	April 2022
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
phangorn: phylogenetic analysis in R Schliep, Klaus Peter Bioinformatics, Vol. 27, Issue 4 https://doi.org/10.1093/bioinformatics/btq706	journal	December 2010
CD-HIT: accelerated for clustering the next-generation sequencing data Fu, Limin; Niu, Beifang; Zhu, Zhengwei Bioinformatics, Vol. 28, Issue 23 https://doi.org/10.1093/bioinformatics/bts565	journal	October 2012
ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R Paradis, Emmanuel; Schliep, Klaus Bioinformatics, Vol. 35, Issue 3 https://doi.org/10.1093/bioinformatics/bty633	journal	July 2018
Growth Temperature and Genome Size in Bacteria Are Negatively Correlated, Suggesting Genomic Streamlining During Thermal Adaptation Sabath, Niv; Ferrada, Evandro; Barve, Aditya Genome Biology and Evolution, Vol. 5, Issue 5 https://doi.org/10.1093/gbe/evt050	journal	April 2013
Twelve years of SAMtools and BCFtools Danecek, Petr; Bonfield, James K.; Liddle, Jennifer GigaScience, Vol. 10, Issue 2 https://doi.org/10.1093/gigascience/giab008	journal	January 2021
eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale Cantalapiedra, Carlos P.; Hernández-Plaza, Ana; Letunic, Ivica Molecular Biology and Evolution, Vol. 38, Issue 12 https://doi.org/10.1093/molbev/msab293	journal	October 2021
A Molecular Timeline for the Origin of Photosynthetic Eukaryotes Yoon, Hwan Su; Hackett, Jeremiah D.; Ciniglia, Claudia Molecular Biology and Evolution, Vol. 21, Issue 5 https://doi.org/10.1093/molbev/msh075	journal	May 2004
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Ultrafast Approximation for Phylogenetic Bootstrap Minh, B. Q.; Nguyen, M. A. T.; von Haeseler, A. Molecular Biology and Evolution, Vol. 30, Issue 5 https://doi.org/10.1093/molbev/mst024	journal	February 2013
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
IMG/VR v4: an expanded database of uncultivated virus genomes within a framework of extensive functional, taxonomic, and ecological metadata Camargo, Antonio Pedro; Nayfach, Stephen; Chen, I-Min A. Nucleic Acids Research, Vol. 51, Issue D1 https://doi.org/10.1093/nar/gkac1037	journal	November 2022
eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses Huerta-Cepas, Jaime; Szklarczyk, Damian; Heller, Davide Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1085	journal	November 2018
Structure of a filamentous virus uncovers familial ties within the archaeal virosphere Wang, Fengbin; Baquero, Diana P.; Su, Zhangli Virus Evolution, Vol. 6, Issue 1 https://doi.org/10.1093/ve/veaa023	journal	January 2020
The Hadean-Archaean Environment Sleep, N. H. Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 6 https://doi.org/10.1101/cshperspect.a002527	journal	May 2010
Thermophilic Bacteria Strictly Obey Szybalski's Transcription Direction Rule and Politely Purine-Load RNAs with Both Adenine and Guanine Lao, Perry J.; Forsdyke, Donald R. Genome Research, Vol. 10, Issue 2 https://doi.org/10.1101/gr.10.2.228	journal	February 2000
metaSPAdes: a new versatile metagenomic assembler Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton Genome Research, Vol. 27, Issue 5 https://doi.org/10.1101/gr.213959.116	journal	March 2017
ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data Yu, Guangchuang; Smith, David K.; Zhu, Huachen Methods in Ecology and Evolution, Vol. 8, Issue 1 https://doi.org/10.1111/2041-210X.12628	journal	September 2016
phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package Revell, Liam J. Methods in Ecology and Evolution, Vol. 3, Issue 2 https://doi.org/10.1111/j.2041-210X.2011.00169.x	journal	December 2011
Toward Automatic Reconstruction of a Highly Resolved Tree of Life Ciccarelli, F. D. Science, Vol. 311, Issue 5765 https://doi.org/10.1126/science.1123061	journal	March 2006
A Virus in a Fungus in a Plant: Three-Way Symbiosis Required for Thermal Tolerance Marquez, L. M.; Redman, R. S.; Rodriguez, R. J. Science, Vol. 315, Issue 5811 https://doi.org/10.1126/science.1136237	journal	January 2007
Massive Horizontal Gene Transfer in Bdelloid Rotifers Gladyshev, E. A.; Meselson, M.; Arkhipova, I. R. Science, Vol. 320, Issue 5880 https://doi.org/10.1126/science.1156407	journal	May 2008
Gene Transfer from Bacteria and Archaea Facilitated Evolution of an Extremophilic Eukaryote Schonknecht, G.; Chen, W. -H.; Ternes, C. M. Science, Vol. 339, Issue 6124 https://doi.org/10.1126/science.1231707	journal	March 2013
Evolutionary drivers of thermoadaptation in enzyme catalysis Nguyen, Vy; Wilson, Christopher; Hoemberger, Marc Science, Vol. 355, Issue 6322 https://doi.org/10.1126/science.aah3717	journal	December 2016
A rooted phylogeny resolves early bacterial evolution Coleman, Gareth A.; Davín, Adrián A.; Mahendrarajah, Tara A. Science, Vol. 372, Issue 6542 https://doi.org/10.1126/science.abe0511	journal	May 2021
Assembly of Viral Metagenomes from Yellowstone Hot Springs Schoenfeld, T.; Patterson, M.; Richardson, P. M. Applied and Environmental Microbiology, Vol. 74, Issue 13 https://doi.org/10.1128/AEM.02598-07	journal	April 2008
Phage Community Dynamics in Hot Springs Breitbart, M.; Wegley, L.; Leeds, S. Applied and Environmental Microbiology, Vol. 70, Issue 3 https://doi.org/10.1128/AEM.70.3.1633-1640.2004	journal	March 2004
Pacmanvirus, a New Giant Icosahedral Virus at the Crossroads between Asfarviridae and Faustoviruses Andreani, Julien; Khalil, Jacques Yaacoub Bou; Sevvana, Madhumati Journal of Virology, Vol. 91, Issue 14 https://doi.org/10.1128/JVI.00212-17	journal	April 2017
An Uncultivated Virus Infecting a Nanoarchaeal Parasite in the Hot Springs of Yellowstone National Park Munson-McGee, Jacob H.; Rooney, Colleen; Young, Mark J. Journal of Virology, Vol. 94, Issue 3 https://doi.org/10.1128/JVI.01213-19	journal	January 2020
The Replisome Pausing Factor Timeless Is Required for Episomal Maintenance of Latent Epstein-Barr Virus Dheekollu, Jayaraju; Lieberman, Paul M. Journal of Virology, Vol. 85, Issue 12 https://doi.org/10.1128/JVI.02425-10	journal	June 2011
Codon Usage Frequency of RNA Virus Genomes from High-Temperature Acidic-Environment Metagenomes Stedman, Kenneth M.; Kosmicki, Nicholas R.; Diemer, Geoffrey S. Journal of Virology, Vol. 87, Issue 3 https://doi.org/10.1128/JVI.02610-12	journal	February 2013
Three Novel Virophage Genomes Discovered from Yellowstone Lake Metagenomes Zhou, Jinglie; Sun, Dawei; Childers, Alyson Journal of Virology, Vol. 89, Issue 2 https://doi.org/10.1128/JVI.03039-14	journal	November 2014
Identification of Novel Positive-Strand RNA Viruses by Metagenomic Analysis of Archaea-Dominated Yellowstone Hot Springs Bolduc, B.; Shaughnessy, D. P.; Wolf, Y. I. Journal of Virology, Vol. 86, Issue 10 https://doi.org/10.1128/JVI.07196-11	journal	February 2012
Medusavirus, a Novel Large DNA Virus Discovered from Hot Spring Water Yoshikawa, Genki; Blanc-Mathieu, Romain; Song, Chihong Journal of Virology, Vol. 93, Issue 8 https://doi.org/10.1128/jvi.02130-18	journal	February 2019
Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism Bäckström, Disa; Yutin, Natalya; Jørgensen, Steffen L. mBio, Vol. 10, Issue 2 https://doi.org/10.1128/mBio.02497-18	journal	March 2019
Insights into thermoadaptation and the evolution of mesophily from the bacterial phylum Thermotogae Pollo, Stephen M. J.; Zhaxybayeva, Olga; Nesbø, Camilla L. Canadian Journal of Microbiology, Vol. 61, Issue 9 https://doi.org/10.1139/cjm-2015-0073	journal	September 2015
Mycovirus Diversity and Evolution Revealed/Inferred from Recent Studies Kondo, Hideki; Botella, Leticia; Suzuki, Nobuhiro Annual Review of Phytopathology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev-phyto-021621-122122	journal	August 2022
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
Consistent mutational paths predict eukaryotic thermostability van Noort, Vera; Bradatsch, Bettina; Arumugam, Manimozhiyan BMC Evolutionary Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2148-13-7	journal	January 2013
Discrimination of thermophilic and mesophilic proteins Taylor, Todd J.; Vaisman, Iosif I. BMC Structural Biology, Vol. 10, Issue Suppl 1 https://doi.org/10.1186/1472-6807-10-S1-S5	journal	January 2010
Eukaryotic large nucleo-cytoplasmic DNA viruses: Clusters of orthologous genes and reconstruction of viral genome evolution Yutin, Natalya; Wolf, Yuri I.; Raoult, Didier Virology Journal, Vol. 6, Issue 1 https://doi.org/10.1186/1743-422X-6-223	journal	January 2009
Microscale spatial distributions of microbes and viruses in intertidal photosynthetic microbial mats Carreira, Cátia; Piel, Tim; Staal, Marc SpringerPlus, Vol. 4, Issue 1 https://doi.org/10.1186/s40064-015-0977-8	journal	May 2015
VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses Guo, Jiarong; Bolduc, Ben; Zayed, Ahmed A. Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-020-00990-y	journal	February 2021
Multiple evolutionary origins of giant viruses Koonin, Eugene V.; Yutin, Natalya F1000Research, Vol. 7 https://doi.org/10.12688/f1000research.16248.1	journal	January 2018
A phylogenomic framework for charting the diversity and evolution of giant viruses Aylward, Frank O.; Moniruzzaman, Mohammad; Ha, Anh D. PLOS Biology, Vol. 19, Issue 10 https://doi.org/10.1371/journal.pbio.3001430	journal	October 2021
Protein and DNA Sequence Determinants of Thermophilic Adaptation Zeldovich, Konstantin B.; Berezovsky, Igor N.; Shakhnovich, Eugene I. PLoS Computational Biology, Vol. 3, Issue 1 https://doi.org/10.1371/journal.pcbi.0030005	journal	January 2007
Biochemical Diversification through Foreign Gene Expression in Bdelloid Rotifers Boschetti, Chiara; Carr, Adrian; Crisp, Alastair PLoS Genetics, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pgen.1003035	journal	November 2012
Metagenomes from High-Temperature Chemotrophic Systems Reveal Geochemical Controls on Microbial Community Structure and Function Inskeep, William P.; Rusch, Douglas B.; Jay, Zackary J. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009773	journal	March 2010
Taxonomic Novelty and Distinctive Genomic Features of Hot Spring Cyanobacteria Alcorta, Jaime; Alarcón-Schumacher, Tomás; Salgado, Oscar Frontiers in Genetics, Vol. 11 https://doi.org/10.3389/fgene.2020.568223	journal	November 2020
Faustoviruses: Comparative Genomics of New Megavirales Family Members Benamar, Samia; Reteno, Dorine G. I.; Bandaly, Victor Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00003	journal	February 2016
A Review on Viral Metagenomics in Extreme Environments Dávila-Ramos, Sonia; Castelán-Sánchez, Hugo G.; Martínez-Ávila, Liliana Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02403	journal	October 2019
Updated Virophage Taxonomy and Distinction from Polinton-like Viruses Roux, Simon; Fischer, Matthias G.; Hackl, Thomas Biomolecules, Vol. 13, Issue 2 https://doi.org/10.3390/biom13020204	journal	January 2023
Dataset from the paper "Viruses from geothermal springs have ancient origins reflecting long-term interactions with extremophilic red algal mats" Benites, L. Felipe Zenodo https://doi.org/10.5281/zenodo.10086280	dataset	January 2023
Identification of a deep-branching thermophilic clade sheds light on early bacterial evolution Leng, Hao; Wang, Yinzhao; Zhao, Weishu figshare https://doi.org/10.6084/m9.figshare.22586701	dataset	January 2023
The genomes of polyextremophilic cyanidiales contain 1% horizontally transferred genes with diverse adaptive functions Rossoni, Alessandro W.; Price, Dana C.; Seger, Mark eLife, Vol. 8 https://doi.org/10.7554/eLife.45017	journal	May 2019
Benchmarking viromics: an in silico evaluation of metagenome-enabled estimates of viral community composition and diversity Roux, Simon; Emerson, Joanne B.; Eloe-Fadrosh, Emiley A. PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3817	journal	January 2017
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies Kang, Dongwan D.; Li, Feng; Kirton, Edward PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7359	journal	January 2019