Genomic variation and biogeography of Antarctic haloarchaea
Abstract
Background The genomes of halophilic archaea (haloarchaea) often comprise multiple replicons. Genomic variation in haloarchaea has been linked to viral infection pressure and, in the case of Antarctic communities, can be caused by intergenera gene exchange. To expand understanding of genome variation and biogeography of Antarctic haloarchaea, here we assessed genomic variation between two strains of Halorubrum lacusprofundi that were isolated from Antarctic hypersaline lakes from different regions (Vestfold Hills and Rauer Islands). To assess variation in haloarchaeal populations, including the presence of genomic islands, metagenomes from six hypersaline Antarctic lakes were characterised. Results The sequence of the largest replicon of each Hrr. lacusprofundi strain (primary replicon) was highly conserved, while each of the strains’ two smaller replicons (secondary replicons) were highly variable. Intergenera gene exchange was identified, including the sharing of a type I-B CRISPR system. Evaluation of infectivity of an Antarctic halovirus provided experimental evidence for the differential susceptibility of the strains, bolstering inferences that strain variation is important for modulating interactions with viruses. A relationship was found between genomic structuring and the location of variation within replicons and genomic islands, demonstrating that the way in which haloarchaea accommodate genomic variability relates to replicon structuring. Metagenome read andmore »
- Authors:
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); Australian Research Council
- OSTI Identifier:
- 1618939
- Alternate Identifier(s):
- OSTI ID: 1544022
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- Microbiome
- Additional Journal Information:
- Journal Name: Microbiome Journal Volume: 6 Journal Issue: 1; Journal ID: ISSN 2049-2618
- Publisher:
- Springer Science + Business Media
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Haloarchaea; Halobacteria; Antarctica; Genome variation; Metagenomics; Pan-genome; Genomic islands; Replicons; Virus infection; Biogeography
Citation Formats
Tschitschko, Bernhard, Erdmann, Susanne, DeMaere, Matthew Z., Roux, Simon, Panwar, Pratibha, Allen, Michelle A., Williams, Timothy J., Brazendale, Sarah, Hancock, Alyce M., Eloe-Fadrosh, Emiley A., and Cavicchioli, Ricardo. Genomic variation and biogeography of Antarctic haloarchaea. United Kingdom: N. p., 2018.
Web. doi:10.1186/s40168-018-0495-3.
Tschitschko, Bernhard, Erdmann, Susanne, DeMaere, Matthew Z., Roux, Simon, Panwar, Pratibha, Allen, Michelle A., Williams, Timothy J., Brazendale, Sarah, Hancock, Alyce M., Eloe-Fadrosh, Emiley A., & Cavicchioli, Ricardo. Genomic variation and biogeography of Antarctic haloarchaea. United Kingdom. https://doi.org/10.1186/s40168-018-0495-3
Tschitschko, Bernhard, Erdmann, Susanne, DeMaere, Matthew Z., Roux, Simon, Panwar, Pratibha, Allen, Michelle A., Williams, Timothy J., Brazendale, Sarah, Hancock, Alyce M., Eloe-Fadrosh, Emiley A., and Cavicchioli, Ricardo. Wed .
"Genomic variation and biogeography of Antarctic haloarchaea". United Kingdom. https://doi.org/10.1186/s40168-018-0495-3.
@article{osti_1618939,
title = {Genomic variation and biogeography of Antarctic haloarchaea},
author = {Tschitschko, Bernhard and Erdmann, Susanne and DeMaere, Matthew Z. and Roux, Simon and Panwar, Pratibha and Allen, Michelle A. and Williams, Timothy J. and Brazendale, Sarah and Hancock, Alyce M. and Eloe-Fadrosh, Emiley A. and Cavicchioli, Ricardo},
abstractNote = {Background The genomes of halophilic archaea (haloarchaea) often comprise multiple replicons. Genomic variation in haloarchaea has been linked to viral infection pressure and, in the case of Antarctic communities, can be caused by intergenera gene exchange. To expand understanding of genome variation and biogeography of Antarctic haloarchaea, here we assessed genomic variation between two strains of Halorubrum lacusprofundi that were isolated from Antarctic hypersaline lakes from different regions (Vestfold Hills and Rauer Islands). To assess variation in haloarchaeal populations, including the presence of genomic islands, metagenomes from six hypersaline Antarctic lakes were characterised. Results The sequence of the largest replicon of each Hrr. lacusprofundi strain (primary replicon) was highly conserved, while each of the strains’ two smaller replicons (secondary replicons) were highly variable. Intergenera gene exchange was identified, including the sharing of a type I-B CRISPR system. Evaluation of infectivity of an Antarctic halovirus provided experimental evidence for the differential susceptibility of the strains, bolstering inferences that strain variation is important for modulating interactions with viruses. A relationship was found between genomic structuring and the location of variation within replicons and genomic islands, demonstrating that the way in which haloarchaea accommodate genomic variability relates to replicon structuring. Metagenome read and contig mapping and clustering and scaling analyses demonstrated biogeographical patterning of variation consistent with environment and distance effects. The metagenome data also demonstrated that specific haloarchaeal species dominated the hypersaline systems indicating they are endemic to Antarctica. Conclusion The study describes how genomic variation manifests in Antarctic-lake haloarchaeal communities and provides the basis for future assessments of Antarctic regional and global biogeography of haloarchaea.},
doi = {10.1186/s40168-018-0495-3},
journal = {Microbiome},
number = 1,
volume = 6,
place = {United Kingdom},
year = {Wed Jun 20 00:00:00 EDT 2018},
month = {Wed Jun 20 00:00:00 EDT 2018}
}
https://doi.org/10.1186/s40168-018-0495-3
Web of Science
Figures / Tables:
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
CONTIGuator: a bacterial genomes finishing tool for structural insights on draft genomes
journal, January 2011
- Galardini, Marco; Biondi, Emanuele G.; Bazzicalupo, Marco
- Source Code for Biology and Medicine, Vol. 6, Issue 1
Versatile and open software for comparing large genomes
journal, January 2004
- Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L.
- Genome Biology, Vol. 5, Issue 2, R12
The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4)
journal, October 2015
- Huntemann, Marcel; Ivanova, Natalia N.; Mavromatis, Konstantinos
- Standards in Genomic Sciences, Vol. 10, Issue 1
CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats
journal, May 2007
- Grissa, I.; Vergnaud, G.; Pourcel, C.
- Nucleic Acids Research, Vol. 35, Issue Web Server
Halobacterium lacusprofundi sp. nov., a Halophilic Bacterium Isolated from Deep Lake, Antarctica
journal, November 1988
- Franzmann, P. D.; Stackebrandt, E.; Sanderson, K.
- Systematic and Applied Microbiology, Vol. 11, Issue 1
Genomic Islands and the Ecology and Evolution of Prochlorococcus
journal, March 2006
- Coleman, M. L.
- Science, Vol. 311, Issue 5768
High level of intergenera gene exchange shapes the evolution of haloarchaea in an isolated Antarctic lake
journal, September 2013
- DeMaere, M. Z.; Williams, T. J.; Allen, M. A.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 42
Comparative Analysis of the Mosaic Genomes of Tailed Archaeal Viruses and Proviruses Suggests Common Themes for Virion Architecture and Assembly with Tailed Viruses of Bacteria
journal, March 2010
- Krupovič, Mart; Forterre, Patrick; Bamford, Dennis H.
- Journal of Molecular Biology, Vol. 397, Issue 1
Antarctic archaea–virus interactions: metaproteome-led analysis of invasion, evasion and adaptation
journal, June 2015
- Tschitschko, Bernhard; Williams, Timothy J.; Allen, Michelle A.
- The ISME Journal, Vol. 9, Issue 9
Prochlorococcus: the structure and function of collective diversity
journal, December 2014
- Biller, Steven J.; Berube, Paul M.; Lindell, Debbie
- Nature Reviews Microbiology, Vol. 13, Issue 1
From genomes to function: haloarchaea as model organisms
journal, March 2006
- Soppa, J.
- Microbiology, Vol. 152, Issue 3
Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: Implications for the microbial "pan-genome"
journal, September 2005
- Tettelin, H.; Masignani, V.; Cieslewicz, M. J.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 39
The meromictic lakes and stratified marine basins of the Vestfold Hills, East Antarctica
journal, June 1999
- Gibson, John A. E.
- Antarctic Science, Vol. 11, Issue 2
POLYPHASIC STUDY OF ANTARCTIC CYANOBACTERIAL STRAINS 1
journal, November 2006
- Taton, Arnaud; Grubisic, Stana; Ertz, Damien
- Journal of Phycology, Vol. 42, Issue 6
Microbial species delineation using whole genome sequences
journal, July 2015
- Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia
- Nucleic Acids Research, Vol. 43, Issue 14
Fast and accurate long-read alignment with Burrows–Wheeler transform
journal, January 2010
- Li, Heng; Durbin, Richard
- Bioinformatics, Vol. 26, Issue 5
MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices
journal, June 2016
- Li, Dinghua; Luo, Ruibang; Liu, Chi-Man
- Methods, Vol. 102
Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems
journal, January 2011
- Makarova, Kira S.; Aravind, L.; Wolf, Yuri I.
- Biology Direct, Vol. 6, Issue 1
Diversity in prokaryotic glycosylation: an archaeal-derived N-linked glycan contains legionaminic acid: Diversity in haloarchaeal N-glycosylation
journal, April 2012
- Kandiba, Lina; Aitio, Olli; Helin, Jari
- Molecular Microbiology, Vol. 84, Issue 3
InterProScan 5: genome-scale protein function classification
journal, January 2014
- Jones, P.; Binns, D.; Chang, H. -Y.
- Bioinformatics, Vol. 30, Issue 9
Adaptive seeds tame genomic sequence comparison
journal, January 2011
- Kielbasa, S. M.; Wan, R.; Sato, K.
- Genome Research, Vol. 21, Issue 3
A plasmid from an Antarctic haloarchaeon uses specialized membrane vesicles to disseminate and infect plasmid-free cells
journal, August 2017
- Erdmann, Susanne; Tschitschko, Bernhard; Zhong, Ling
- Nature Microbiology, Vol. 2, Issue 10
Microbial ecology of Antarctic aquatic systems
journal, October 2015
- Cavicchioli, Ricardo
- Nature Reviews Microbiology, Vol. 13, Issue 11
Microbial ecology of an Antarctic hypersaline lake: genomic assessment of ecophysiology among dominant haloarchaea
journal, February 2014
- Williams, Timothy J.; Allen, Michelle A.; DeMaere, Matthew Z.
- The ISME Journal, Vol. 8, Issue 8
Ecophysiological Distinctions of Haloarchaea from a Hypersaline Antarctic Lake as Determined by Metaproteomics
journal, March 2016
- Tschitschko, Bernhard; Williams, Timothy J.; Allen, Michelle A.
- Applied and Environmental Microbiology, Vol. 82, Issue 11
N-Glycosylation Is Important for Proper Haloferax volcanii S-Layer Stability and Function
journal, December 2016
- Tamir, Adi; Eichler, Jerry
- Applied and Environmental Microbiology, Vol. 83, Issue 6
A low-polynomial algorithm for assembling clusters of orthologous groups from intergenomic symmetric best matches
journal, May 2010
- Kristensen, David M.; Kannan, Lavanya; Coleman, Michael K.
- Bioinformatics, Vol. 26, Issue 12
S-Layer Glycoproteins and Flagellins: Reporters of Archaeal Posttranslational Modifications
journal, January 2010
- Jarrell, Ken F.; Jones, Gareth M.; Kandiba, Lina
- Archaea, Vol. 2010
Analysis Tool Web Services from the EMBL-EBI
journal, May 2013
- McWilliam, Hamish; Li, Weizhong; Uludag, Mahmut
- Nucleic Acids Research, Vol. 41, Issue W1
De Novo Sequences of Haloquadratum walsbyi from Lake Tyrrell, Australia, Reveal a Variable Genomic Landscape
journal, January 2015
- Tully, Benjamin J.; Emerson, Joanne B.; Andrade, Karen
- Archaea, Vol. 2015
The Repetitive DNA Elements Called CRISPRs and Their Associated Genes: Evidence of Horizontal Transfer Among Prokaryotes
journal, April 2006
- Godde, James S.; Bickerton, Amanda
- Journal of Molecular Evolution, Vol. 62, Issue 6
Fast gapped-read alignment with Bowtie 2
journal, March 2012
- Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 9, Issue 4
BLAST+: architecture and applications
journal, January 2009
- Camacho, Christiam; Coulouris, George; Avagyan, Vahram
- BMC Bioinformatics, Vol. 10, 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
Antarctic biogeography revisited: updating the Antarctic Conservation Biogeographic Regions
journal, June 2016
- Terauds, Aleks; Lee, Jasmine R.
- Diversity and Distributions, Vol. 22, Issue 8
Structuring effects of climate-related environmental factors on Antarctic microbial mat communities
journal, March 2010
- Verleyen, E.; Sabbe, K.; Hodgson, Da
- Aquatic Microbial Ecology, Vol. 59
Biogeographical distribution and ecological ranges of benthic cyanobacteria in East Antarctic lakes: Distribution and ecological ranges of Antarctic cyanobacteria
journal, August 2006
- Taton, Arnaud; Grubisic, Stana; Balthasart, Pierre
- FEMS Microbiology Ecology, Vol. 57, Issue 2
Metaproteogenomic analysis of a dominant green sulfur bacterium from Ace Lake, Antarctica
journal, March 2010
- Ng, Charmaine; DeMaere, Matthew Z.; Williams, Timothy J.
- The ISME Journal, Vol. 4, Issue 8
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
Fast optimal leaf ordering for hierarchical clustering
journal, June 2001
- Bar-Joseph, Z.; Gifford, D. K.; Jaakkola, T. S.
- Bioinformatics, Vol. 17, Issue Suppl 1
MEGAN-LR: new algorithms allow accurate binning and easy interactive exploration of metagenomic long reads and contigs
journal, January 2018
- Huson, Daniel H.; Albrecht, Benjamin; Bağcı, Caner
- Biology Direct, Vol. 13, Issue 1
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
On the use of high-throughput sequencing for the study of cyanobacterial diversity in Antarctic aquatic mats
journal, April 2016
- Pessi, Igor Stelmach; Maalouf, Pedro De Carvalho; Laughinghouse, Haywood Dail
- Journal of Phycology, Vol. 52, Issue 3
ACT: the Artemis comparison tool
journal, June 2005
- Carver, T. J.; Rutherford, K. M.; Berriman, M.
- Bioinformatics, Vol. 21, Issue 16
Genomic island variability facilitates Prochlorococcus–virus coexistence
journal, June 2011
- Avrani, Sarit; Wurtzel, Omri; Sharon, Itai
- Nature, Vol. 474, Issue 7353
N-Glycosylation of Haloferax volcanii Flagellins Requires Known Agl Proteins and Is Essential for Biosynthesis of Stable Flagella
journal, June 2012
- Tripepi, Manuela; You, Jason; Temel, Sevcan
- Journal of Bacteriology, Vol. 194, Issue 18
Reordering contigs of draft genomes using the Mauve Aligner
journal, June 2009
- Rissman, Anna I.; Mau, Bob; Biehl, Bryan S.
- Bioinformatics, Vol. 25, Issue 16
Fast algorithms for large-scale genome alignment and comparison
journal, June 2002
- Delcher, A. L.
- Nucleic Acids Research, Vol. 30, Issue 11
Haloferax volcanii N-Glycosylation: Delineating the Pathway of dTDP-rhamnose Biosynthesis
journal, May 2014
- Kaminski, Lina; Eichler, Jerry
- PLoS ONE, Vol. 9, Issue 5
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
Fine-scale evolution: genomic, phenotypic and ecological differentiation in two coexisting Salinibacter ruber strains
journal, February 2010
- Peña, Arantxa; Teeling, Hanno; Huerta-Cepas, Jaime
- The ISME Journal, Vol. 4, Issue 7
The Sequence Alignment/Map format and SAMtools
journal, June 2009
- Li, H.; Handsaker, B.; Wysoker, A.
- Bioinformatics, Vol. 25, Issue 16
Assembling Genomes and Mini-metagenomes from Highly Chimeric Reads
book, January 2013
- Nurk, Sergey; Bankevich, Anton; Antipov, Dmitry
- Lecture Notes in Computer Science
Developing a genetic manipulation system for the Antarctic archaeon, Halorubrum lacusprofundi: investigating acetamidase gene function
journal, October 2016
- Liao, Y.; Williams, T. J.; Walsh, J. C.
- Scientific Reports, Vol. 6, Issue 1
Works referencing / citing this record:
Unexpected host dependency of Antarctic Nanohaloarchaeota
journal, June 2019
- Hamm, Joshua N.; Erdmann, Susanne; Eloe-Fadrosh, Emiley A.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 29
Novel haloarchaeal viruses from Lake Retba infecting Haloferax and Halorubrum species
journal, April 2019
- Mizuno, Carolina M.; Prajapati, Bina; Lucas‐Staat, Soizick
- Environmental Microbiology, Vol. 21, Issue 6
Applying Genome-Resolved Metagenomics to Deconvolute the Halophilic Microbiome
journal, March 2019
- Uritskiy, Gherman; DiRuggiero, Jocelyne
- Genes, Vol. 10, Issue 3