Giant virus diversity and host interactions through global metagenomics
Abstract
Our current knowledge about nucleocytoplasmic large DNA viruses (NCLDVs) is largely derived from viral isolates that are co-cultivated with protists and algae. Here we reconstructed 2,074 NCLDV genomes from sampling sites across the globe by building on the rapidly increasing amount of publicly available metagenome data. This led to an 11-fold increase in phylogenetic diversity and a parallel 10-fold expansion in functional diversity. Analysis of 58,023 major capsid proteins from large and giant viruses using metagenomic data revealed the global distribution patterns and cosmopolitan nature of these viruses. The discovered viral genomes encoded a wide range of proteins with putative roles in photosynthesis and diverse substrate transport processes, indicating that host reprogramming is probably a common strategy in the NCLDVs. Furthermore, inferences of horizontal gene transfer connected viral lineages to diverse eukaryotic hosts. We anticipate that the global diversity of NCLDVs that we describe here will establish giant viruses-which are associated with most major eukaryotic lineages-as important players in ecosystems across Earth's biomes.
- Authors:
-
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint Genome Institute
- Concordia University, Québec (Canada), Groupe de recherche interuniversitaire en limnologie, Dept. of Biology
- Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Ecology and Evolutionary Biology
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology; Univ. of Wisconsin, Madison, WI (United States). Dept. Civil and Environmental Engineering
- Georgia Inst. of Technology, Atlanta, GA (United States). School of Civil and Environmental Engineering
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1624270
- Alternate Identifier(s):
- OSTI ID: 1760213
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature (London)
- Additional Journal Information:
- Journal Name: Nature (London); Journal Volume: 578; Journal Issue: 7795; Journal ID: ISSN 0028-0836
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Biodiversity; environmental microbiology; evolution; viral evolution; virus-host interactions
Citation Formats
Schulz, Frederik, Roux, Simon, Paez-Espino, David, Jungbluth, Sean, Walsh, David A., Denef, Vincent J., McMahon, Katherine D., Konstantinidis, Konstantinos T., Eloe-Fadrosh, Emiley A., Kyrpides, Nikos C., and Woyke, Tanja. Giant virus diversity and host interactions through global metagenomics. United States: N. p., 2020.
Web. doi:10.1038/s41586-020-1957-x.
Schulz, Frederik, Roux, Simon, Paez-Espino, David, Jungbluth, Sean, Walsh, David A., Denef, Vincent J., McMahon, Katherine D., Konstantinidis, Konstantinos T., Eloe-Fadrosh, Emiley A., Kyrpides, Nikos C., & Woyke, Tanja. Giant virus diversity and host interactions through global metagenomics. United States. https://doi.org/10.1038/s41586-020-1957-x
Schulz, Frederik, Roux, Simon, Paez-Espino, David, Jungbluth, Sean, Walsh, David A., Denef, Vincent J., McMahon, Katherine D., Konstantinidis, Konstantinos T., Eloe-Fadrosh, Emiley A., Kyrpides, Nikos C., and Woyke, Tanja. Wed .
"Giant virus diversity and host interactions through global metagenomics". United States. https://doi.org/10.1038/s41586-020-1957-x. https://www.osti.gov/servlets/purl/1624270.
@article{osti_1624270,
title = {Giant virus diversity and host interactions through global metagenomics},
author = {Schulz, Frederik and Roux, Simon and Paez-Espino, David and Jungbluth, Sean and Walsh, David A. and Denef, Vincent J. and McMahon, Katherine D. and Konstantinidis, Konstantinos T. and Eloe-Fadrosh, Emiley A. and Kyrpides, Nikos C. and Woyke, Tanja},
abstractNote = {Our current knowledge about nucleocytoplasmic large DNA viruses (NCLDVs) is largely derived from viral isolates that are co-cultivated with protists and algae. Here we reconstructed 2,074 NCLDV genomes from sampling sites across the globe by building on the rapidly increasing amount of publicly available metagenome data. This led to an 11-fold increase in phylogenetic diversity and a parallel 10-fold expansion in functional diversity. Analysis of 58,023 major capsid proteins from large and giant viruses using metagenomic data revealed the global distribution patterns and cosmopolitan nature of these viruses. The discovered viral genomes encoded a wide range of proteins with putative roles in photosynthesis and diverse substrate transport processes, indicating that host reprogramming is probably a common strategy in the NCLDVs. Furthermore, inferences of horizontal gene transfer connected viral lineages to diverse eukaryotic hosts. We anticipate that the global diversity of NCLDVs that we describe here will establish giant viruses-which are associated with most major eukaryotic lineages-as important players in ecosystems across Earth's biomes.},
doi = {10.1038/s41586-020-1957-x},
journal = {Nature (London)},
number = 7795,
volume = 578,
place = {United States},
year = {Wed Jan 22 00:00:00 EST 2020},
month = {Wed Jan 22 00:00:00 EST 2020}
}
Web of Science
Works referenced in this record:
A Glimpse of Nucleo-Cytoplasmic Large DNA Virus Biodiversity through the Eukaryotic Genomics Window
journal, January 2017
- Gallot-Lavallée, Lucie; Blanc, Guillaume
- Viruses, Vol. 9, Issue 1
Study of Gene Trafficking between Acanthamoeba and Giant Viruses Suggests an Undiscovered Family of Amoeba-Infecting Viruses
journal, November 2016
- Maumus, Florian; Blanc, Guillaume
- Genome Biology and Evolution, Vol. 8, Issue 11
Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton
journal, August 2017
- Monier, Adam; Chambouvet, Aurélie; Milner, David S.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 36
UFBoot2: Improving the Ultrafast Bootstrap Approximation
journal, October 2017
- Hoang, Diep Thi; Chernomor, Olga; von Haeseler, Arndt
- Molecular Biology and Evolution, Vol. 35, Issue 2
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences
journal, May 2006
- Li, W.; Godzik, A.
- Bioinformatics, Vol. 22, Issue 13
Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea
journal, August 2017
- Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas
- Nature Biotechnology, Vol. 35, Issue 8
Eukaryotic large nucleo-cytoplasmic DNA viruses: Clusters of orthologous genes and reconstruction of viral genome evolution
journal, January 2009
- Yutin, Natalya; Wolf, Yuri I.; Raoult, Didier
- Virology Journal, Vol. 6, Issue 1
Eukaryotic Gene Prediction Using GeneMark.hmm-E and GeneMark-ES
journal, September 2011
- Borodovsky, Mark; Lomsadze, Alex
- Current Protocols in Bioinformatics, Vol. 35, Issue 1
Modifying HMMER3 to Run Efficiently on the Cori Supercomputer Using OpenMP Tasking
conference, May 2018
- Arndt, William
- 2018 IEEE International Parallel and Distributed Processing Symposium Workshops (IPDPSW)
Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere
journal, February 2018
- Abrahão, Jônatas; Silva, Lorena; Silva, Ludmila Santos
- Nature Communications, Vol. 9, Issue 1
Ultrastructure of Meelsvirus: A nuclear virus of arrow worms (phylum Chaetognatha) producing giant “tailed” virions
journal, September 2018
- Shinn, George L.; Bullard, Brianna L.
- PLOS ONE, Vol. 13, Issue 9
Microbial and Animal Rhodopsins: Structures, Functions, and Molecular Mechanisms
journal, September 2013
- Ernst, Oliver P.; Lodowski, David T.; Elstner, Marcus
- Chemical Reviews, Vol. 114, Issue 1
Route of NCLDV evolution: the genomic accordion
journal, October 2013
- Filée, Jonathan
- Current Opinion in Virology, Vol. 3, Issue 5
Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii
journal, June 2002
- Sineshchekov, O. A.; Jung, K. -H.; Spudich, J. L.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 13
Gene Exchange and the Origin of Giant Viruses
journal, January 2010
- Filée, Jonathan; Chandler, Michael
- Intervirology, Vol. 53, Issue 5
Giant viruses, giant chimeras: The multiple evolutionary histories of Mimivirus genes
journal, January 2008
- Moreira, David; Brochier-Armanet, Céline
- BMC Evolutionary Biology, Vol. 8, Issue 1
Carotenoid Cleavage Oxygenases from Microbes and Photosynthetic Organisms: Features and Functions
journal, October 2016
- Ahrazem, Oussama; Gómez-Gómez, Lourdes; Rodrigo, María
- International Journal of Molecular Sciences, Vol. 17, Issue 11
The Involvement of a Multicopper Oxidase in Iron Uptake by the Green Algae Chlamydomonas reinhardtii
journal, December 2002
- Herbik, Alexandra; Bölling, Christian; Buckhout, Thomas J.
- Plant Physiology, Vol. 130, Issue 4
Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010
- Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F.
- BMC Bioinformatics, Vol. 11, Issue 1
A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators
journal, September 2019
- Needham, David M.; Yoshizawa, Susumu; Hosaka, Toshiaki
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 41
Role of Ferric Reductases in Iron Acquisition and Virulence in the Fungal Pathogen Cryptococcus neoformans
journal, December 2013
- Saikia, Sanjay; Oliveira, Debora; Hu, Guanggan
- Infection and Immunity, Vol. 82, Issue 2
Minimum Information about an Uncultivated Virus Genome (MIUViG)
journal, December 2018
- Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E.
- Nature Biotechnology, Vol. 37, Issue 1
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015
- Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
- Genome Research, Vol. 25, Issue 7
Fast and sensitive protein alignment using DIAMOND
journal, November 2014
- Buchfink, Benjamin; Xie, Chao; Huson, Daniel H.
- Nature Methods, Vol. 12, Issue 1
Metabolic reprogramming by viruses in the sunlit and dark ocean
journal, January 2013
- Hurwitz, Bonnie L.; Hallam, Steven J.; Sullivan, Matthew B.
- Genome Biology, Vol. 14, Issue 11
Mimivirus and Mimiviridae: Giant viruses with an increasing number of potential hosts, including corals and sponges
journal, July 2009
- Claverie, Jean-Michel; Grzela, Renata; Lartigue, Audrey
- Journal of Invertebrate Pathology, Vol. 101, Issue 3
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014
- Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
- Molecular Biology and Evolution, Vol. 32, Issue 1
Giant viruses come of age
journal, June 2016
- Fischer, Matthias G.
- Current Opinion in Microbiology, Vol. 31
Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism
journal, March 2019
- Bäckström, Disa; Yutin, Natalya; Jørgensen, Steffen L.
- mBio, Vol. 10, Issue 2
PorthoMCL: Parallel orthology prediction using MCL for the realm of massive genome availability
journal, January 2017
- Tabari, Ehsan; Su, Zhengchang
- Big Data Analytics, Vol. 2, Issue 1
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016
- Letunic, Ivica; Bork, Peer
- Nucleic Acids Research, Vol. 44, Issue W1
Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families
journal, November 2017
- Kalvari, Ioanna; Argasinska, Joanna; Quinones-Olvera, Natalia
- Nucleic Acids Research, Vol. 46, Issue D1
290 metagenome-assembled genomes from the Mediterranean Sea: a resource for marine microbiology
journal, January 2017
- Tully, Benjamin J.; Sachdeva, Rohan; Graham, Elaina D.
- PeerJ, Vol. 5
Giant viruses with an expanded complement of translation system components
journal, April 2017
- Schulz, Frederik; Yutin, Natalya; Ivanova, Natalia N.
- Science, Vol. 356, Issue 6333
The Pfam protein families database: towards a more sustainable future
journal, December 2015
- Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
- Nucleic Acids Research, Vol. 44, Issue D1
ModelFinder: fast model selection for accurate phylogenetic estimates
journal, May 2017
- Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F.
- Nature Methods, Vol. 14, Issue 6
The rapidly expanding universe of giant viruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus
journal, September 2015
- Abergel, Chantal; Legendre, Matthieu; Claverie, Jean-Michel
- FEMS Microbiology Reviews, Vol. 39, Issue 6
Molecular systematics of sturgeon nucleocytoplasmic large DNA viruses
journal, November 2018
- Clouthier, Sharon; Anderson, Eric; Kurath, Gael
- Molecular Phylogenetics and Evolution, Vol. 128
Deciphering viral presences: two novel partial giant viruses detected in marine metagenome and in a mine drainage metagenome
journal, April 2018
- Andreani, Julien; Verneau, Jonathan; Raoult, Didier
- Virology Journal, Vol. 15, Issue 1
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
Taxonomic distribution of large DNA viruses in the sea
journal, January 2008
- Monier, Adam; Claverie, Jean-Michel; Ogata, Hiroyuki
- Genome Biology, Vol. 9, Issue 7
IMG/VR v.2.0: an integrated data management and analysis system for cultivated and environmental viral genomes
journal, November 2018
- Paez-Espino, David; Roux, Simon; Chen, I-Min A.
- Nucleic Acids Research, Vol. 47, Issue D1
Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper
journal, April 2017
- Huerta-Cepas, Jaime; Forslund, Kristoffer; Coelho, Luis Pedro
- Molecular Biology and Evolution, Vol. 34, Issue 8
Iron Utilization in Marine Cyanobacteria and Eukaryotic Algae
journal, January 2012
- Morrissey, Joe; Bowler, Chris
- Frontiers in Microbiology, Vol. 3
Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes
journal, April 2013
- Hingamp, Pascal; Grimsley, Nigel; Acinas, Silvia G.
- The ISME Journal, Vol. 7, Issue 9
The Revised Classification of Eukaryotes
journal, September 2012
- Adl, Sina M.; Simpson, Alastair G. B.; Lane, Christopher E.
- Journal of Eukaryotic Microbiology, Vol. 59, Issue 5
Bacterial, archaeal and viral-like rhodopsins from the Red Sea: Red Sea microbial rhodopsins
journal, February 2013
- Philosof, Alon; Béjà, Oded
- Environmental Microbiology Reports, Vol. 5, Issue 3
A simple method to control over-alignment in the MAFFT multiple sequence alignment program
journal, February 2016
- Katoh, Kazutaka; Standley, Daron M.
- Bioinformatics, Vol. 32, Issue 13
A giant virus infecting green algae encodes key fermentation genes
journal, May 2018
- Schvarcz, Christopher R.; Steward, Grieg F.
- Virology, Vol. 518
IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes
journal, October 2018
- Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna
- Nucleic Acids Research, Vol. 47, Issue D1
Faustovirus, an Asfarvirus-Related New Lineage of Giant Viruses Infecting Amoebae
journal, April 2015
- Reteno, Dorine Gaëlle; Benamar, Samia; Khalil, Jacques Bou
- Journal of Virology, Vol. 89, Issue 13
Giant Viruses of Amoebas: An Update
journal, March 2016
- Aherfi, Sarah; Colson, Philippe; La Scola, Bernard
- Frontiers in Microbiology, Vol. 7
Infernal 1.1: 100-fold faster RNA homology searches
journal, September 2013
- Nawrocki, E. P.; Eddy, S. R.
- Bioinformatics, Vol. 29, Issue 22
Variation in the Genetic Repertoire of Viruses Infecting Micromonas pusilla Reflects Horizontal Gene Transfer and Links to Their Environmental Distribution
journal, May 2017
- Finke, Jan; Winget, Danielle; Chan, Amy
- Viruses, Vol. 9, Issue 5
Genomic exploration of individual giant ocean viruses
journal, May 2017
- Wilson, William H.; Gilg, Ilana C.; Moniruzzaman, Mohammad
- The ISME Journal, Vol. 11, Issue 8
IMG/M: integrated genome and metagenome comparative data analysis system
journal, October 2016
- Chen, I-Min A.; Markowitz, Victor M.; Chu, Ken
- Nucleic Acids Research, Vol. 45, Issue D1
High-throughput isolation of giant viruses of the Mimiviridae and Marseilleviridae families in the Tunisian environment
journal, January 2013
- Boughalmi, Mondher; Saadi, Hanene; Pagnier, Isabelle
- Environmental Microbiology, Vol. 15, Issue 7
A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea
journal, December 2009
- Wu, Dongying; Hugenholtz, Philip; Mavromatis, Konstantinos
- Nature, Vol. 462, Issue 7276
Polinton-like viruses are abundant in aquatic ecosystems
journal, January 2021
- Bellas, Christopher M.; Sommaruga, Ruben
- Microbiome, Vol. 9, Issue 1
Minimum information about an uncultivated virus genome (MIUVIG)
text, January 2019
- Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E.
- ETH Zurich
Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper
text, January 2017
- Huerta-Cepas, Jaime; Forslund, Kristoffer; Coelho, Luis Pedro
- Oxford University Press
Works referencing / citing this record:
Advantages and Limits of Metagenomic Assembly and Binning of a Giant Virus
journal, June 2020
- Schulz, Frederik; Andreani, Julien; Francis, Rania
- mSystems, Vol. 5, Issue 3
Comparative Analysis of the Circular and Highly Asymmetrical Marseilleviridae Genomes
journal, November 2020
- Blanca, Léo; Christo-Foroux, Eugène; Rigou, Sofia
- Viruses, Vol. 12, Issue 11
Distributed Many-to-Many Protein Sequence Alignment using Sparse Matrices
preprint, January 2020
- Selvitopi, Oguz; Ekanayake, Saliya; Guidi, Giulia
- arXiv