Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics
Abstract
Virophages are small viruses that co-infect eukaryotic cells alongside giant viruses (Mimiviridae) and hijack their machinery to replicate. While two types of virophages have been isolated, their genomic diversity and ecology remain largely unknown. Here we use time series metagenomics to identify and study the dynamics of 25 uncultivated virophage populations, 17 of which represented by complete or near-complete genomes, in two North American freshwater lakes. Taxonomic analysis suggests that these freshwater virophages represent at least three new candidate genera. Ecologically, virophage populations are repeatedly detected over years and evolutionary stable, yet their distinct abundance profiles and gene content suggest that virophage genera occupy different ecological niches. Co-occurrence analyses reveal 11 virophages strongly associated with uncultivated Mimiviridae, and three associated with eukaryotes among the Dinophyceae, Rhizaria, Alveolata, and Cryptophyceae groups. Together, these findings significantly augment virophage databases, help refine virophage taxonomy, and establish baseline ecological hypotheses and tools to study virophages in nature.
- Authors:
-
- The Ohio State Univ., Columbus, OH (United States). Dept. of Microbiology
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology. Dept. of Civil and Environmental Engineering
- The Ohio State Univ., Columbus, OH (United States). Dept. of Microbiology. Dept. of Civil, Environmental and Geodetic Engineering
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Science Foundation (NSF); Gordon and Betty Moore Foundation (United States)
- OSTI Identifier:
- 1459396
- Grant/Contract Number:
- AC02-05CH11231; MCB-0702395; DEB-1344254; DEB-1440297; OCE-1536989; GBMF #3790
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 8; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; freshwater ecology; metagenomics; microbial ecology; phage biology
Citation Formats
Roux, Simon, Chan, Leong-Keat, Egan, Rob, Malmstrom, Rex R., McMahon, Katherine D., and Sullivan, Matthew B. Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics. United States: N. p., 2017.
Web. doi:10.1038/s41467-017-01086-2.
Roux, Simon, Chan, Leong-Keat, Egan, Rob, Malmstrom, Rex R., McMahon, Katherine D., & Sullivan, Matthew B. Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics. United States. doi:https://doi.org/10.1038/s41467-017-01086-2
Roux, Simon, Chan, Leong-Keat, Egan, Rob, Malmstrom, Rex R., McMahon, Katherine D., and Sullivan, Matthew B. Wed .
"Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics". United States. doi:https://doi.org/10.1038/s41467-017-01086-2. https://www.osti.gov/servlets/purl/1459396.
@article{osti_1459396,
title = {Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics},
author = {Roux, Simon and Chan, Leong-Keat and Egan, Rob and Malmstrom, Rex R. and McMahon, Katherine D. and Sullivan, Matthew B.},
abstractNote = {Virophages are small viruses that co-infect eukaryotic cells alongside giant viruses (Mimiviridae) and hijack their machinery to replicate. While two types of virophages have been isolated, their genomic diversity and ecology remain largely unknown. Here we use time series metagenomics to identify and study the dynamics of 25 uncultivated virophage populations, 17 of which represented by complete or near-complete genomes, in two North American freshwater lakes. Taxonomic analysis suggests that these freshwater virophages represent at least three new candidate genera. Ecologically, virophage populations are repeatedly detected over years and evolutionary stable, yet their distinct abundance profiles and gene content suggest that virophage genera occupy different ecological niches. Co-occurrence analyses reveal 11 virophages strongly associated with uncultivated Mimiviridae, and three associated with eukaryotes among the Dinophyceae, Rhizaria, Alveolata, and Cryptophyceae groups. Together, these findings significantly augment virophage databases, help refine virophage taxonomy, and establish baseline ecological hypotheses and tools to study virophages in nature.},
doi = {10.1038/s41467-017-01086-2},
journal = {Nature Communications},
number = ,
volume = 8,
place = {United States},
year = {2017},
month = {10}
}
Web of Science
Figures / Tables:

Works referenced in this record:
Population Genomics of Early Events in the Ecological Differentiation of Bacteria
journal, April 2012
- Shapiro, B. Jesse; Friedman, Jonathan; Cordero, Otto X.
- Science, Vol. 336, Issue 6077
Recombination and microdiversity in coastal marine cyanophages
journal, November 2009
- Marston, Marcia F.; Amrich, Christopher G.
- Environmental Microbiology, Vol. 11, Issue 11
Invasive species triggers a massive loss of ecosystem services through a trophic cascade
journal, March 2016
- Walsh, Jake R.; Carpenter, Stephen R.; Vander Zanden, M. Jake
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 15
Protein homology detection by HMM-HMM comparison
journal, November 2004
- Soding, J.
- Bioinformatics, Vol. 21, Issue 7
Reticulate Representation of Evolutionary and Functional Relationships between Phage Genomes
journal, February 2008
- Lima-Mendez, G.; Van Helden, J.; Toussaint, A.
- Molecular Biology and Evolution, Vol. 25, Issue 4
Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer
journal, November 2016
- Gregory, Ann C.; Solonenko, Sergei A.; Ignacio-Espinoza, J. Cesar
- BMC Genomics, Vol. 17, Issue 1
An Ordination of the Upland Forest Communities of Southern Wisconsin
journal, February 1957
- Bray, J. Roger; Curtis, J. T.
- Ecological Monographs, Vol. 27, Issue 4
A General Framework for Weighted Gene Co-Expression Network Analysis
journal, January 2005
- Zhang, Bin; Horvath, Steve
- Statistical Applications in Genetics and Molecular Biology, Vol. 4, Issue 1
Related Giant Viruses in Distant Locations and Different Habitats: Acanthamoeba polyphaga moumouvirus Represents a Third Lineage of the Mimiviridae That Is Close to the Megavirus Lineage
journal, December 2012
- Yoosuf, Niyaz; Yutin, Natalya; Colson, Philippe
- Genome Biology and Evolution, Vol. 4, Issue 12
Temporal variation in freshwater viral and bacterial community composition
journal, June 2008
- Lymer, David; Logue, JÜRg Brendan; Brussaard, Corina P. D.
- Freshwater Biology, Vol. 53, Issue 6
WGCNA: an R package for weighted correlation network analysis
journal, December 2008
- Langfelder, Peter; Horvath, Steve
- BMC Bioinformatics, Vol. 9, Issue 1
Identification of ribosomal RNA genes in metagenomic fragments
journal, April 2009
- Huang, Ying; Gilna, Paul; Li, Weizhong
- Bioinformatics, Vol. 25, Issue 10
Correlation detection strategies in microbial data sets vary widely in sensitivity and precision
journal, February 2016
- Weiss, Sophie; Van Treuren, Will; Lozupone, Catherine
- The ISME Journal, Vol. 10, Issue 7
The virophage as a unique parasite of the giant mimivirus
journal, August 2008
- La Scola, Bernard; Desnues, Christelle; Pagnier, Isabelle
- Nature, Vol. 455, Issue 7209
Population Dynamics and Diversity of Viruses, Bacteria and Phytoplankton in a Shallow Eutrophic Lake
journal, October 2007
- Tijdens, Marjolijn; Hoogveld, Hans L.; Kamst-van Agterveld, Miranda P.
- Microbial Ecology, Vol. 56, Issue 1
Temporal Dynamics and Decay of Putatively Allochthonous and Autochthonous Viral Genotypes in Contrasting Freshwater Lakes
journal, July 2012
- Hewson, Ian; Barbosa, Jorge G.; Brown, Julia M.
- Applied and Environmental Microbiology, Vol. 78, Issue 18
A Guide to the Natural History of Freshwater Lake Bacteria
journal, March 2011
- Newton, R. J.; Jones, S. E.; Eiler, A.
- Microbiology and Molecular Biology Reviews, Vol. 75, Issue 1
Minimus: a fast, lightweight genome assembler
journal, January 2007
- Sommer, Daniel D.; Delcher, Arthur L.; Salzberg, Steven L.
- BMC Bioinformatics, Vol. 8, Issue 1
Genomic variation landscape of the human gut microbiome
journal, December 2012
- Schloissnig, Siegfried; Arumugam, Manimozhiyan; Sunagawa, Shinichi
- Nature, Vol. 493, Issue 7430
Easyfig: a genome comparison visualizer
journal, January 2011
- Sullivan, M. J.; Petty, N. K.; Beatson, S. A.
- Bioinformatics, Vol. 27, Issue 7
Viruses with More Than 1,000 Genes: Mamavirus, a New Acanthamoeba polyphagamimivirus Strain, and Reannotation of Mimivirus Genes
journal, January 2011
- Colson, Philippe; Yutin, Natalya; Shabalina, Svetlana A.
- Genome Biology and Evolution, Vol. 3
FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011
- Magoc, T.; Salzberg, S. L.
- Bioinformatics, Vol. 27, Issue 21
Three Novel Virophage Genomes Discovered from Yellowstone Lake Metagenomes
journal, November 2014
- Zhou, Jinglie; Sun, Dawei; Childers, Alyson
- Journal of Virology, Vol. 89, Issue 2
Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China
journal, January 2016
- Ma, Bin; Wang, Haizhen; Dsouza, Melissa
- The ISME Journal, Vol. 10, Issue 8
UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004
- Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
- Journal of Computational Chemistry, Vol. 25, Issue 13
Mimivirus and its Virophage
journal, December 2009
- Claverie, Jean-Michel; Abergel, Chantal
- Annual Review of Genetics, Vol. 43, Issue 1
Large-scale search for genes on which positive selection may operate
journal, May 1996
- Endo, T.; Ikeo, K.; Gojobori, T.
- Molecular Biology and Evolution, Vol. 13, Issue 5
Microbial Co-occurrence Relationships in the Human Microbiome
journal, July 2012
- Faust, Karoline; Sathirapongsasuti, J. Fah; Izard, Jacques
- PLoS Computational Biology, Vol. 8, Issue 7
Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists
journal, November 2013
- Chow, Cheryl-Emiliane T.; Kim, Diane Y.; Sachdeva, Rohan
- The ISME Journal, Vol. 8, Issue 4
Conservation of major and minor jelly-roll capsid proteins in Polinton (Maverick) transposons suggests that they are bona fide viruses
journal, January 2014
- Krupovic, Mart; Bamford, Dennis H.; Koonin, Eugene V.
- Biology Direct, Vol. 9, Issue 1
Diversity of Virophages in Metagenomic Data Sets
journal, February 2013
- Zhou, J.; Zhang, W.; Yan, S.
- Journal of Virology, Vol. 87, Issue 8
InterProScan 5: genome-scale protein function classification
journal, January 2014
- Jones, P.; Binns, D.; Chang, H. -Y.
- Bioinformatics, Vol. 30, Issue 9
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
The virus of my virus is my friend: Ecological effects of virophage with alternative modes of coinfection
journal, August 2014
- Taylor, Bradford P.; Cortez, Michael H.; Weitz, Joshua S.
- Journal of Theoretical Biology, Vol. 354
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012
- Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
- Nucleic Acids Research, Vol. 41, Issue D1
Molecular ecological network analyses
journal, January 2012
- Deng, Ye; Jiang, Yi-Huei; Yang, Yunfeng
- BMC Bioinformatics, Vol. 13, Issue 1
Polintons: a hotbed of eukaryotic virus, transposon and plasmid evolution
journal, December 2014
- Krupovic, Mart; Koonin, Eugene V.
- Nature Reviews Microbiology, Vol. 13, Issue 2
Scale-Free Behavior in Protein Domain Networks
journal, September 2001
- Wuchty, Stefan
- Molecular Biology and Evolution, Vol. 18, Issue 9
Origin and Evolution of Eukaryotic Large Nucleo-Cytoplasmic DNA Viruses
journal, January 2010
- Koonin, Eugene V.; Yutin, Natalya
- Intervirology, Vol. 53, Issue 5
MEME SUITE: tools for motif discovery and searching
journal, May 2009
- Bailey, T. L.; Boden, M.; Buske, F. A.
- Nucleic Acids Research, Vol. 37, Issue Web Server
Zamilon, a Novel Virophage with Mimiviridae Host Specificity
journal, April 2014
- Gaia, Morgan; Benamar, Samia; Boughalmi, Mondher
- PLoS ONE, Vol. 9, Issue 4
Microcystin mcyA and mcyE Gene Abundances Are Not Appropriate Indicators of Microcystin Concentrations in Lakes
journal, May 2015
- Beversdorf, Lucas J.; Chaston, Sheena D.; Miller, Todd R.
- PLOS ONE, Vol. 10, Issue 5
MRBAYES: Bayesian inference of phylogenetic trees
journal, August 2001
- Huelsenbeck, J. P.; Ronquist, F.
- Bioinformatics, Vol. 17, Issue 8
The Neutral Theory of Molecular Evolution in the Genomic Era
journal, September 2010
- Nei, Masatoshi; Suzuki, Yoshiyuki; Nozawa, Masafumi
- Annual Review of Genomics and Human Genetics, Vol. 11, Issue 1
A novel group of diverse Polinton-like viruses discovered by metagenome analysis
journal, November 2015
- Yutin, Natalya; Shevchenko, Sofiya; Kapitonov, Vladimir
- BMC Biology, Vol. 13, Issue 1
Fast gapped-read alignment with Bowtie 2
journal, March 2012
- Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 9, Issue 4
Host genome integration and giant virus-induced reactivation of the virophage mavirus
journal, December 2016
- Fischer, Matthias G.; Hackl, Thomas
- Nature, Vol. 540, Issue 7632
Structure of Sputnik, a virophage, at 3.5-A resolution
journal, October 2012
- Zhang, X.; Sun, S.; Xiang, Y.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 45
Network biology: understanding the cell's functional organization
journal, February 2004
- Barabási, Albert-László; Oltvai, Zoltán N.
- Nature Reviews Genetics, Vol. 5, Issue 2
Diversity and dynamics of algal Megaviridae members during a harmful brown tide caused by the pelagophyte, Aureococcus anophagefferens
journal, March 2016
- Moniruzzaman, Mohammad; Gann, Eric R.; LeCleir, Gary R.
- FEMS Microbiology Ecology, Vol. 92, Issue 5
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
Dynamic Viral Populations in Hypersaline Systems as Revealed by Metagenomic Assembly
journal, July 2012
- Emerson, Joanne B.; Thomas, Brian C.; Andrade, Karen
- Applied and Environmental Microbiology, Vol. 78, Issue 17
mRNA deep sequencing reveals 75 new genes and a complex transcriptional landscape in Mimivirus
journal, April 2010
- Legendre, M.; Audic, S.; Poirot, O.
- Genome Research, Vol. 20, Issue 5
Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes
journal, June 2013
- Santini, S.; Jeudy, S.; Bartoli, J.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 26
Efficient statistical significance approximation for local similarity analysis of high-throughput time series data
journal, November 2012
- Xia, Li C.; Ai, Dongmei; Cram, Jacob
- Bioinformatics, Vol. 29, Issue 2
An efficient algorithm for large-scale detection of protein families
journal, April 2002
- Enright, A. J.
- Nucleic Acids Research, Vol. 30, Issue 7
A classification system for virophages and satellite viruses
journal, October 2015
- Krupovic, Mart; Kuhn, Jens H.; Fischer, Matthias G.
- Archives of Virology, Vol. 161, Issue 1
Genomic insights that advance the species definition for prokaryotes
journal, February 2005
- Konstantinidis, K. T.; Tiedje, J. M.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 7
A new family of hybrid virophages from an animal gut metagenome
journal, April 2015
- Yutin, Natalya; Kapitonov, Vladimir V.; Koonin, Eugene V.
- Biology Direct, Vol. 10, Issue 1
EMBOSS: The European Molecular Biology Open Software Suite
journal, June 2000
- Rice, Peter; Longden, Ian; Bleasby, Alan
- Trends in Genetics, Vol. 16, Issue 6
Plankton networks driving carbon export in the oligotrophic ocean
journal, February 2016
- Guidi, Lionel; Chaffron, Samuel; Bittner, Lucie
- Nature, Vol. 532, Issue 7600
A Virophage at the Origin of Large DNA Transposons
journal, March 2011
- Fischer, M. G.; Suttle, C. A.
- Science, Vol. 332, Issue 6026
The Sequence Alignment/Map format and SAMtools
journal, June 2009
- Li, H.; Handsaker, B.; Wysoker, A.
- Bioinformatics, Vol. 25, Issue 16
Productivity and salinity structuring of the microplankton revealed by comparative freshwater metagenomics: Comparative freshwater metagenomics
journal, November 2013
- Eiler, Alexander; Zaremba-Niedzwiedzka, Katarzyna; Martínez-García, Manuel
- Environmental Microbiology, Vol. 16, Issue 9
Broad Spectrum of Mimiviridae Virophage Allows Its Isolation Using a Mimivirus Reporter
journal, April 2013
- Gaia, Morgan; Pagnier, Isabelle; Campocasso, Angélique
- PLoS ONE, Vol. 8, Issue 4
Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations
journal, January 2016
- Bendall, Matthew L.; Stevens, Sarah LR; Chan, Leong-Keat
- The ISME Journal, Vol. 10, Issue 7
Virophage control of antarctic algal host-virus dynamics
journal, March 2011
- Yau, S.; Lauro, F. M.; DeMaere, M. Z.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 15
The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes
preprint, March 2016
- Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T.
- PeerJ Preprints 4:e1900v1
Topological Properties of Co-Occurrence Networks in Published Gene Expression Signatures
journal, January 2008
- Muller, Heiko; Acquati, Francesco
- Bioinformatics and Biology Insights, Vol. 2
Works referencing / citing this record:
Defective viral genomes are key drivers of the virus–host interaction
journal, June 2019
- Vignuzzi, Marco; López, Carolina B.
- Nature Microbiology, Vol. 4, Issue 7
Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks
journal, May 2019
- Bin Jang, Ho; Bolduc, Benjamin; Zablocki, Olivier
- Nature Biotechnology, Vol. 37, Issue 6
Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales
journal, June 2018
- Borton, Mikayla A.; Hoyt, David W.; Roux, Simon
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 28
Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics
journal, October 2019
- Kavagutti, Vinicius S.; Andrei, Adrian-Ştefan; Mehrshad, Maliheh
- Microbiome, Vol. 7, Issue 1
Defective viral genomes are key drivers of the virus–host interaction
journal, June 2019
- Vignuzzi, Marco; López, Carolina B.
- Nature Microbiology, Vol. 4, Issue 7
Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks
journal, May 2019
- Bin Jang, Ho; Bolduc, Benjamin; Zablocki, Olivier
- Nature Biotechnology, Vol. 37, Issue 6
Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales
journal, June 2018
- Borton, Mikayla A.; Hoyt, David W.; Roux, Simon
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 28
Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics
journal, October 2019
- Kavagutti, Vinicius S.; Andrei, Adrian-Ştefan; Mehrshad, Maliheh
- Microbiome, Vol. 7, Issue 1
Metagenomics detection and characterisation of viruses in faecal samples from Australian wild birds
journal, June 2018
- Vibin, Jessy; Chamings, Anthony; Collier, Fiona
- Scientific Reports, Vol. 8, Issue 1
Capsid protein structure, self-assembly, and processing reveal morphogenesis of the marine virophage mavirus
journal, June 2018
- Born, Diana; Reuter, Lukas; Mersdorf, Ulrike
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 28
Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake
journal, September 2019
- Okazaki, Yusuke; Nishimura, Yosuke; Yoshida, Takashi
- Environmental Microbiology, Vol. 21, Issue 12
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
Charting the diversity of uncultured viruses of Archaea and Bacteria
journal, December 2019
- Coutinho, F. H.; Edwards, R. A.; Rodríguez-Valera, F.
- BMC Biology, Vol. 17, Issue 1
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
Diversity, evolution, and classification of virophages uncovered through global metagenomics
journal, December 2019
- Paez-Espino, David; Zhou, Jinglie; Roux, Simon
- Microbiome, Vol. 7, Issue 1
Viva lavidaviruses! Five features of virophages that parasitize giant DNA viruses
journal, March 2019
- Duponchel, Sarah; Fischer, Matthias G.
- PLOS Pathogens, Vol. 15, Issue 3
Archaeal Viruses from High-Temperature Environments
journal, February 2018
- Munson-McGee, Jacob; Snyder, Jamie; Young, Mark
- Genes, Vol. 9, Issue 3
Viruses of Eukaryotic Algae: Diversity, Methods for Detection, and Future Directions
journal, September 2018
- Coy, Samantha; Gann, Eric; Pound, Helena
- Viruses, Vol. 10, Issue 9
Virophages of Giant Viruses: An Update at Eleven
journal, August 2019
- Mougari, Said; Sahmi-Bounsiar, Dehia; Levasseur, Anthony
- Viruses, Vol. 11, Issue 8
Freshwater carbon and nutrient cycles revealed through reconstructed population genomes
journal, January 2018
- Linz, Alexandra M.; He, Shaomei; Stevens, Sarah L. R.
- PeerJ, Vol. 6
Figures / Tables found in this record: