Assembly-Driven Community Genomics of a Hypersaline Microbial Ecosystem
Abstract
Microbial populations inhabiting a natural hypersaline lake ecosystem in Lake Tyrrell, Victoria, Australia, have been characterized using deep metagenomic sampling, iterative de novo assembly, and multidimensional phylogenetic binning. Composite genomes representing habitat-specific microbial populations were reconstructed for eleven different archaea and one bacterium, comprising between 0.6 and 14.1% of the planktonic community. Eight of the eleven archaeal genomes were from microbial species without previously cultured representatives. These new genomes provide habitat-specific reference sequences enabling detailed, lineage-specific compartmentalization of predicted functional capabilities and cellular properties associated with both dominant and less abundant community members, including organisms previously known only by their 16S rRNA sequences. Together, these data provide a comprehensive, culture-independent genomic blueprint for ecosystem-wide analysis of protein functions, population structure, and lifestyles of co-existing, co-evolving microbial groups within the same natural habitat. The ‘‘assembly-driven’’ community genomic approach demonstrated in this study advances our ability to push beyond single gene investigations, and promotes genome-scale reconstructions as a tangible goal in the quest to define the metabolic, ecological, and evolutionary dynamics that underpin environmental microbial diversity.
- Authors:
-
- Univ. of California, San Diego, CA (United States). Scripps Inst. of Oceanography. Marine Biology Research Division
- Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Sciences; Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy, and Management
- Univ. of Southern California, Los Angeles, CA (United States). Dept. of Biological Sciences
- Univ. of California, San Diego, CA (United States). Scripps Inst. of Oceanography. Marine Biology Research Division; Univ. of California, San Diego, CA (United States). Division of Biological Sciences
- 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). Biological Systems Science Division
- OSTI Identifier:
- 1627601
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 8; Journal Issue: 4; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Science & Technology - Other Topics
Citation Formats
Podell, Sheila, Ugalde, Juan A., Narasingarao, Priya, Banfield, Jillian F., Heidelberg, Karla B., and Allen, Eric E. Assembly-Driven Community Genomics of a Hypersaline Microbial Ecosystem. United States: N. p., 2013.
Web. doi:10.1371/journal.pone.0061692.
Podell, Sheila, Ugalde, Juan A., Narasingarao, Priya, Banfield, Jillian F., Heidelberg, Karla B., & Allen, Eric E. Assembly-Driven Community Genomics of a Hypersaline Microbial Ecosystem. United States. https://doi.org/10.1371/journal.pone.0061692
Podell, Sheila, Ugalde, Juan A., Narasingarao, Priya, Banfield, Jillian F., Heidelberg, Karla B., and Allen, Eric E. Thu .
"Assembly-Driven Community Genomics of a Hypersaline Microbial Ecosystem". United States. https://doi.org/10.1371/journal.pone.0061692. https://www.osti.gov/servlets/purl/1627601.
@article{osti_1627601,
title = {Assembly-Driven Community Genomics of a Hypersaline Microbial Ecosystem},
author = {Podell, Sheila and Ugalde, Juan A. and Narasingarao, Priya and Banfield, Jillian F. and Heidelberg, Karla B. and Allen, Eric E.},
abstractNote = {Microbial populations inhabiting a natural hypersaline lake ecosystem in Lake Tyrrell, Victoria, Australia, have been characterized using deep metagenomic sampling, iterative de novo assembly, and multidimensional phylogenetic binning. Composite genomes representing habitat-specific microbial populations were reconstructed for eleven different archaea and one bacterium, comprising between 0.6 and 14.1% of the planktonic community. Eight of the eleven archaeal genomes were from microbial species without previously cultured representatives. These new genomes provide habitat-specific reference sequences enabling detailed, lineage-specific compartmentalization of predicted functional capabilities and cellular properties associated with both dominant and less abundant community members, including organisms previously known only by their 16S rRNA sequences. Together, these data provide a comprehensive, culture-independent genomic blueprint for ecosystem-wide analysis of protein functions, population structure, and lifestyles of co-existing, co-evolving microbial groups within the same natural habitat. The ‘‘assembly-driven’’ community genomic approach demonstrated in this study advances our ability to push beyond single gene investigations, and promotes genome-scale reconstructions as a tangible goal in the quest to define the metabolic, ecological, and evolutionary dynamics that underpin environmental microbial diversity.},
doi = {10.1371/journal.pone.0061692},
journal = {PLoS ONE},
number = 4,
volume = 8,
place = {United States},
year = {Thu Apr 18 00:00:00 EDT 2013},
month = {Thu Apr 18 00:00:00 EDT 2013}
}
Works referenced in this record:
Explaining microbial population genomics through phage predation
journal, November 2009
- Rodriguez-Valera, Francisco; Martin-Cuadrado, Ana-Belen; Rodriguez-Brito, Beltran
- Nature Reviews Microbiology, Vol. 7, Issue 11
New Abundant Microbial Groups in Aquatic Hypersaline Environments
journal, October 2011
- Ghai, Rohit; Pašić, Lejla; Fernández, Ana Beatriz
- Scientific Reports, Vol. 1, Issue 1
Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw
journal, November 2011
- Mackelprang, Rachel; Waldrop, Mark P.; DeAngelis, Kristen M.
- Nature, Vol. 480, Issue 7377
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
journal, July 2006
- DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.
- Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072
A Catalog of Reference Genomes from the Human Microbiome
journal, May 2010
- Nelson, K. E.; Weinstock, G. M.; Highlander, S. K.
- Science, Vol. 328, Issue 5981
PhymmBL expanded: confidence scores, custom databases, parallelization and more
journal, April 2011
- Brady, Arthur; Salzberg, Steven
- Nature Methods, Vol. 8, Issue 5
Halobaculum gomorrense gen. nov., sp. nov., a Novel Extremely Halophilic Archaeon from the Dead Sea
journal, October 1995
- Oren, A.; Gurevich, P.; Gemmell, R. T.
- International Journal of Systematic Bacteriology, Vol. 45, Issue 4
Diversity of Haloquadratum and other haloarchaea in three, geographically distant, Australian saltern crystallizer ponds
journal, December 2009
- Oh, Dickson; Porter, Kate; Russ, Brendan
- Extremophiles, Vol. 14, Issue 2
Toward Automatic Reconstruction of a Highly Resolved Tree of Life
journal, March 2006
- Ciccarelli, F. D.
- Science, Vol. 311, Issue 5765
A Whole-Genome Assembly of Drosophila
journal, March 2000
- Myers, E. W.
- Science, Vol. 287, Issue 5461
Community genomics in microbial ecology and evolution
journal, June 2005
- Allen, Eric E.; Banfield, Jillian F.
- Nature Reviews Microbiology, Vol. 3, Issue 6
Living with salt: metabolic and phylogenetic diversity of archaea inhabiting saline ecosystems
journal, March 2012
- Andrei, Adrian-Ştefan; Banciu, Horia Leonard; Oren, Aharon
- FEMS Microbiology Letters, Vol. 330, Issue 1
A Sanger/pyrosequencing hybrid approach for the generation of high-quality draft assemblies of marine microbial genomes
journal, July 2006
- Goldberg, S. M. D.; Johnson, J.; Busam, D.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 30
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
Microbial life at high salt concentrations: phylogenetic and metabolic diversity
journal, January 2008
- Oren, Aharon
- Saline Systems, Vol. 4, Issue 1
Isolation and cultivation of Walsby's square archaeon
journal, December 2004
- Bolhuis, Henk; Poele, Evelien M. te; Rodriguez-Valera, Francisco
- Environmental Microbiology, Vol. 6, Issue 12
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006
- Stamatakis, Alexandros
- Bioinformatics, Vol. 22, Issue 21
Hawkeye: an interactive visual analytics tool for genome assemblies
journal, January 2007
- Schatz, Michael C.; Phillippy, Adam M.; Shneiderman, Ben
- Genome Biology, Vol. 8, Issue 3
Reconstructing Viral Genomes from the Environment Using Fosmid Clones: The Case of Haloviruses
journal, March 2012
- Garcia-Heredia, Inmaculada; Martin-Cuadrado, Ana-Belen; Mojica, Francisco J. M.
- PLoS ONE, Vol. 7, Issue 3
phyloXML: XML for evolutionary biology and comparative genomics
journal, October 2009
- Han, Mira V.; Zmasek, Christian M.
- BMC Bioinformatics, Vol. 10, Issue 1
Ecological traits of planktonic viruses and prokaryotes along a full-salinity gradient: Virioplankton along a full-salinity gradient
journal, February 2011
- Bettarel, Yvan; Bouvier, Thierry; Bouvier, Corinne
- FEMS Microbiology Ecology, Vol. 76, Issue 2
Human polymicrobial infections
journal, January 2005
- Brogden, K.; Guthmiller, J.; Taylor, C.
- The Lancet, Vol. 365, Issue 9455
Nanoarchaeal 16S rRNA gene sequences are widely dispersed in hyperthermophilic and mesophilic halophilic environments
journal, June 2008
- Casanueva, Ana; Galada, Ncebakazi; Baker, Gillian C.
- Extremophiles, Vol. 12, Issue 5
Flotation characteristics of cyanobacteriumAnabaena flos-aquae for gas vesicle production
journal, December 1998
- Kashyap, Sunil; Sundararajan, Anand; Ju, Lu-Kwang
- Biotechnology and Bioengineering, Vol. 60, Issue 5
Untangling Genomes from Metagenomes: Revealing an Uncultured Class of Marine Euryarchaeota
journal, February 2012
- Iverson, V.; Morris, R. M.; Frazar, C. D.
- Science, Vol. 335, Issue 6068
Search for a 'Tree of Life' in the thicket of the phylogenetic forest
journal, January 2009
- Puigbò, Pere; Wolf, Yuri I.; Koonin, Eugene V.
- Journal of Biology, Vol. 8, Issue 6
Novel and Unexpected Prokaryotic Diversity in Water and Sediments of the Alkaline, Hypersaline Lakes of the Wadi An Natrun, Egypt
journal, April 2007
- Mesbah, Noha M.; Abou-El-Ela, Soad H.; Wiegel, Juergen
- Microbial Ecology, Vol. 54, Issue 4
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009
- Schloss, P. D.; Westcott, S. L.; Ryabin, T.
- Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
A simple, fast, and accurate method of phylogenomic inference
journal, January 2008
- Wu, Martin; Eisen, Jonathan A.
- Genome Biology, Vol. 9, Issue 10
Community structure and metabolism through reconstruction of microbial genomes from the environment
journal, February 2004
- Tyson, Gene W.; Chapman, Jarrod; Hugenholtz, Philip
- Nature, Vol. 428, Issue 6978
Thermophilic anaerobic oxidation of methane by marine microbial consortia
journal, June 2011
- Holler, Thomas; Widdel, Friedrich; Knittel, Katrin
- The ISME Journal, Vol. 5, Issue 12
De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities
journal, June 2011
- Narasingarao, Priya; Podell, Sheila; Ugalde, Juan A.
- The ISME Journal, Vol. 6, Issue 1
Haloquadratum walsbyi : Limited Diversity in a Global Pond
journal, June 2011
- Dyall-Smith, Mike L.; Pfeiffer, Friedhelm; Klee, Kathrin
- PLoS ONE, Vol. 6, Issue 6
The genome of the square archaeon Haloquadratum walsbyi : life at the limits of water activity
journal, July 2006
- Bolhuis, Henk; Palm, Peter; Wende, Andy
- BMC Genomics, Vol. 7, Issue 1
Environmental Shotgun Sequencing: Its Potential and Challenges for Studying the Hidden World of Microbes
journal, March 2007
- Eisen, Jonathan A.; Levin, Simon
- PLoS Biology, Vol. 5, Issue 3, p. e82
Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities
journal, September 2006
- Martín, Héctor García; Ivanova, Natalia; Kunin, Victor
- Nature Biotechnology, Vol. 24, Issue 10
The metavirome of a hypersaline environment: The metavirome of a hypersaline environment
journal, November 2010
- Santos, Fernando; Yarza, Pablo; Parro, Víctor
- Environmental Microbiology, Vol. 12, Issue 11
Genomic plasticity in prokaryotes: the case of the square haloarchaeon
journal, May 2007
- Cuadros-Orellana, Sara; Martin-Cuadrado, Ana-Belen; Legault, Boris
- The ISME Journal, Vol. 1, Issue 3
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
pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree
journal, October 2010
- Matsen, Frederick A.; Kodner, Robin B.; Armbrust, E. Virginia
- BMC Bioinformatics, Vol. 11, Issue 1
An efficient algorithm for large-scale detection of protein families
journal, April 2002
- Enright, A. J.
- Nucleic Acids Research, Vol. 30, Issue 7
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
IMG ER: a system for microbial genome annotation expert review and curation
journal, June 2009
- Markowitz, Victor M.; Mavromatis, Konstantinos; Ivanova, Natalia N.
- Bioinformatics, Vol. 25, Issue 17
Halonotius pteroides gen. nov., sp. nov., an extremely halophilic archaeon recovered from a saltern crystallizer
journal, May 2010
- Burns, David G.; Janssen, Peter H.; Itoh, Takashi
- International Journal of Systematic and Evolutionary Microbiology, Vol. 60, Issue 5
Bacterial diversity in the oral cavity of 10 healthy individuals
journal, March 2010
- Bik, Elisabeth M.; Long, Clara Davis; Armitage, Gary C.
- The ISME Journal, Vol. 4, Issue 8