Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem
Abstract
Marine microbial communities experience daily fluctuations in light and temperature that can have important ramifications for carbon and nutrient cycling. Elucidation of such short time scale community-wide dynamics is hindered by system complexity. Hypersaline aquatic environments have lower species richness than marine environments and can be well-defined spatially, hence they provide a model system for diel cycle analysis. For this study, we conducted a 3-day time series experiment in a well-defined pool in hypersaline Lake Tyrrell, Australia. Microbial communities were tracked by combining cultivation-independent lipidomic, metagenomic and microscopy methods. The ratio of total bacterial to archaeal core lipids in the planktonic community increased by up to 58% during daylight hours and decreased by up to 32% overnight. However, total organism abundances remained relatively consistent over 3 days. Metagenomic analysis of the planktonic community composition, resolved at the genome level, showed dominance by Haloquadratum species and six uncultured members of the Halobacteriaceae. The post 0.8 μm filtrate contained six different nanohaloarchaeal types, three of which have not been identified previously, and cryo-transmission electron microscopy imaging confirmed the presence of small cells. Notably, these nano-sized archaea showed a strong diel cycle, with a pronounced increase in relative abundance over the night periods.more »
- Authors:
-
- Univ. of California, Berkeley, CA (United States)
- The Australian National Univ., Canberra, ACT (Australia)
- Univ. of Southern California, Los Angeles, CA (United States)
- Univ. of Colorado, Boulder, CO (United States); Univ. of California, Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Univ. of Melbourne, Carlton, Melbourne (Australia)
- Univ. of Colorado, Denver, CO (United States)
- Univ. of California, San Diego, La Jolla, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1579834
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 12; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Andrade, Karen, Logemann, Jörn, Heidelberg, Karla B., Emerson, Joanne B., Comolli, Luis R., Hug, Laura A., Probst, Alexander J., Keillar, Angus, Thomas, Brian C., Miller, Christopher S., Allen, Eric E., Moreau, John W., Brocks, Jochen J., and Banfield, Jillian F. Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem. United States: N. p., 2015.
Web. doi:10.1038/ismej.2015.66.
Andrade, Karen, Logemann, Jörn, Heidelberg, Karla B., Emerson, Joanne B., Comolli, Luis R., Hug, Laura A., Probst, Alexander J., Keillar, Angus, Thomas, Brian C., Miller, Christopher S., Allen, Eric E., Moreau, John W., Brocks, Jochen J., & Banfield, Jillian F. Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem. United States. https://doi.org/10.1038/ismej.2015.66
Andrade, Karen, Logemann, Jörn, Heidelberg, Karla B., Emerson, Joanne B., Comolli, Luis R., Hug, Laura A., Probst, Alexander J., Keillar, Angus, Thomas, Brian C., Miller, Christopher S., Allen, Eric E., Moreau, John W., Brocks, Jochen J., and Banfield, Jillian F. Tue .
"Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem". United States. https://doi.org/10.1038/ismej.2015.66. https://www.osti.gov/servlets/purl/1579834.
@article{osti_1579834,
title = {Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem},
author = {Andrade, Karen and Logemann, Jörn and Heidelberg, Karla B. and Emerson, Joanne B. and Comolli, Luis R. and Hug, Laura A. and Probst, Alexander J. and Keillar, Angus and Thomas, Brian C. and Miller, Christopher S. and Allen, Eric E. and Moreau, John W. and Brocks, Jochen J. and Banfield, Jillian F.},
abstractNote = {Marine microbial communities experience daily fluctuations in light and temperature that can have important ramifications for carbon and nutrient cycling. Elucidation of such short time scale community-wide dynamics is hindered by system complexity. Hypersaline aquatic environments have lower species richness than marine environments and can be well-defined spatially, hence they provide a model system for diel cycle analysis. For this study, we conducted a 3-day time series experiment in a well-defined pool in hypersaline Lake Tyrrell, Australia. Microbial communities were tracked by combining cultivation-independent lipidomic, metagenomic and microscopy methods. The ratio of total bacterial to archaeal core lipids in the planktonic community increased by up to 58% during daylight hours and decreased by up to 32% overnight. However, total organism abundances remained relatively consistent over 3 days. Metagenomic analysis of the planktonic community composition, resolved at the genome level, showed dominance by Haloquadratum species and six uncultured members of the Halobacteriaceae. The post 0.8 μm filtrate contained six different nanohaloarchaeal types, three of which have not been identified previously, and cryo-transmission electron microscopy imaging confirmed the presence of small cells. Notably, these nano-sized archaea showed a strong diel cycle, with a pronounced increase in relative abundance over the night periods. We detected no eukaryotic algae or other photosynthetic primary producers, suggesting that carbon resources may derive from patchily distributed microbial mats at the sediment-water interface or from surrounding land. Results show the operation of a strong community-level diel cycle, probably driven by interconnected temperature, light abundance, dissolved oxygen concentration and nutrient flux effects.},
doi = {10.1038/ismej.2015.66},
journal = {The ISME Journal},
number = 12,
volume = 9,
place = {United States},
year = {Tue Apr 28 00:00:00 EDT 2015},
month = {Tue Apr 28 00:00:00 EDT 2015}
}
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Works referenced in this record:
Geochemistry of modern seawater and brines from salt pans: Main components and bromine distribution
journal, January 1973
- Herrmann, Albert G�nter; Knake, Doris; Schneider, J�rgen
- Contributions to Mineralogy and Petrology, Vol. 40, Issue 1
Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria
journal, March 2007
- Lo, Ian; Denef, Vincent J.; VerBerkmoes, Nathan C.
- Nature, Vol. 446, Issue 7135
A Role for Programmed Cell Death in the Microbial Loop
journal, May 2013
- Orellana, Mónica V.; Pang, Wyming L.; Durand, Pierre M.
- PLoS ONE, Vol. 8, Issue 5
New Abundant Microbial Groups in Aquatic Hypersaline Environments
journal, October 2011
- Ghai, Rohit; Pašić, Lejla; Fernández, Ana Beatriz
- Scientific Reports, Vol. 1, Issue 1
Circadian Rhythm of the Prokaryote Synechococcus sp. RF-1
journal, February 1990
- Huang, Tan-Chi; Tu, Jenn; Chow, Te-Jin
- Plant Physiology, Vol. 92, Issue 2
A Cyanobacterial Circadian Clockwork
journal, September 2008
- Johnson, Carl Hirschie; Mori, Tetsuya; Xu, Yao
- Current Biology, Vol. 18, Issue 17
InterProScan: protein domains identifier
journal, July 2005
- Quevillon, E.; Silventoinen, V.; Pillai, S.
- Nucleic Acids Research, Vol. 33, Issue Web Server
Genome-Wide Experimental Determination of Barriers to Horizontal Gene Transfer
journal, November 2007
- Sorek, R.; Zhu, Y.; Creevey, C. J.
- Science, Vol. 318, Issue 5855
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome
journal, January 2009
- Langmead, Ben; Trapnell, Cole; Pop, Mihai
- Genome Biology, Vol. 10, Issue 3
Molecular eco-systems biology: towards an understanding of community function
journal, June 2008
- Raes, Jeroen; Bork, Peer
- Nature Reviews Microbiology, Vol. 6, Issue 9
Independence of Circadian Timing from Cell Division in Cyanobacteria
journal, April 2001
- Mori, T.; Johnson, C. H.
- Journal of Bacteriology, Vol. 183, Issue 8
Seasonal fluctuations in ionic concentrations drive microbial succession in a hypersaline lake community
journal, December 2013
- Podell, Sheila; Emerson, Joanne B.; Jones, Claudia M.
- The ISME Journal, Vol. 8, Issue 5
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007
- Wang, Q.; Garrity, G. M.; Tiedje, J. M.
- Applied and Environmental Microbiology, Vol. 73, Issue 16
EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data
journal, May 2011
- Miller, Christopher S.; Baker, Brett J.; Thomas, Brian C.
- Genome Biology, Vol. 12, Issue 5
Pattern and synchrony of gene expression among sympatric marine microbial populations
journal, January 2013
- Ottesen, E. A.; Young, C. R.; Eppley, J. M.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 6
Community genomics in microbial ecology and evolution
journal, June 2005
- Allen, Eric E.; Banfield, Jillian F.
- Nature Reviews Microbiology, Vol. 3, Issue 6
Assembly-Driven Community Genomics of a Hypersaline Microbial Ecosystem
journal, April 2013
- Podell, Sheila; Ugalde, Juan A.; Narasingarao, Priya
- PLoS ONE, Vol. 8, Issue 4
Microbial life at high salt concentrations: phylogenetic and metabolic diversity
journal, January 2008
- Oren, Aharon
- Saline Systems, Vol. 4, Issue 1
Rapid method for the determination of fatty acid profiles from fats and oils using trimethylsulphonium hydroxide for transesterification
journal, January 1983
- Butte, W.
- Journal of Chromatography A, Vol. 261
Characterization of eukaryotic microbial diversity in hypersaline Lake Tyrrell, Australia
journal, January 2013
- Heidelberg, Karla B.; Nelson, William C.; Holm, Johanna B.
- Frontiers in Microbiology, Vol. 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
Hydrological processes in the Tyrrell Basin, southeastern Australia
journal, March 1992
- Macumber, Phillip G.
- Chemical Geology, Vol. 96, Issue 1-2
Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages
journal, July 2014
- Ottesen, E. A.; Young, C. R.; Gifford, S. M.
- Science, Vol. 345, Issue 6193
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
Active flagellates grazing on prokaryotes in high salinity waters of a solar saltern
journal, January 2003
- Park, Js; Kim, H.; Choi, Dh
- Aquatic Microbial Ecology, Vol. 33
A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont
journal, May 2002
- Huber, Harald; Hohn, Michael J.; Rachel, Reinhard
- Nature, Vol. 417, Issue 6884
A portable cryo-plunger for on-site intact cryogenic microscopy sample preparation in natural environments
journal, December 2011
- Comolli, Luis R.; Duarte, Robert; Baum, Dennis
- Microscopy Research and Technique, Vol. 75, Issue 6
Microbial community proteomics: elucidating the catalysts and metabolic mechanisms that drive the Earth's biogeochemical cycles
journal, June 2009
- Wilmes, Paul; Bond, Philip L.
- Current Opinion in Microbiology, Vol. 12, Issue 3
Diurnally Entrained Anticipatory Behavior in Archaea
journal, May 2009
- Whitehead, Kenia; Pan, Min; Masumura, Ken-ichi
- PLoS ONE, Vol. 4, Issue 5
Genetic and transcriptomic analysis of transcription factor genes in the model halophilic Archaeon: coordinate action of TbpD and TfbA
journal, September 2007
- Coker, James A.; DasSarma, Shiladitya
- BMC Genetics, Vol. 8, Issue 1
Xenorhodopsins, an enigmatic new class of microbial rhodopsins horizontally transferred between archaea and bacteria
journal, January 2011
- Ugalde, Juan A.; Podell, Sheila; Narasingarao, Priya
- Biology Direct, Vol. 6, Issue 1
Testing the Adaptive Value of Circadian Systems
book, January 2005
- Johnson, Carl Hirschie
- Methods in Enzymology
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012
- Peng, Y.; Leung, H. C. M.; Yiu, S. M.
- Bioinformatics, Vol. 28, Issue 11
Viral lysis and nanoflagellate grazing as factors controlling diel variations of Synechococcus spp. summer abundance in coastal waters of Taiwan
journal, May 2012
- Tsai, Ay; Gong, Gc; Sanders, Rw
- Aquatic Microbial Ecology, Vol. 66, Issue 2
Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon
journal, October 2008
- Comolli, Luis R.; Baker, Brett J.; Downing, Kenneth H.
- The ISME Journal, Vol. 3, Issue 2
Microbial communities in acid mine drainage
journal, May 2003
- Baker, Brett J.; Banfield, Jillian F.
- FEMS Microbiology Ecology, Vol. 44, Issue 2
Effects of temperature on ether lipid composition of Caldariella acidophila
journal, January 1980
- De Rosa, Mario; Esposito, Enrico; Gambacorta, Agata
- Phytochemistry, Vol. 19, Issue 5
Fast gapped-read alignment with Bowtie 2
journal, March 2012
- Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 9, Issue 4
Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling
journal, January 2013
- Hug, Laura A.; Castelle, Cindy J.; Wrighton, Kelly C.
- Microbiome, Vol. 1, Issue 1
Predictive Behavior Within Microbial Genetic Networks
journal, June 2008
- Tagkopoulos, I.; Liu, Y. -C.; Tavazoie, S.
- Science, Vol. 320, Issue 5881
Community Proteomics of a Natural Microbial Biofilm
journal, June 2005
- Ram, R. J.
- Science, Vol. 308, Issue 5730
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
Control of heterotrophic prokaryotic abundance and growth rate in hypersaline planktonic environments
journal, January 2004
- Gasol, Jm; Casamayor, Eo; Joint, I.
- Aquatic Microbial Ecology, Vol. 34
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004
- Edgar, Robert C.
- BMC Bioinformatics, Vol. 5, Issue 1, p. 113
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
New Approaches Indicate Constant Viral Diversity despite Shifts in Assemblage Structure in an Australian Hypersaline Lake
journal, August 2013
- Emerson, Joanne B.; Thomas, Brian C.; Andrade, Karen
- Applied and Environmental Microbiology, Vol. 79, Issue 21
SYSTEMS BIOLOGY: The Scale of Prediction
journal, June 2008
- Baliga, N. S.
- Science, Vol. 320, Issue 5881
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
Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013
- Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
- Nature, Vol. 499, Issue 7459
The microbial food web along salinity gradients
journal, April 2000
- Pedrós-Alió, C.
- FEMS Microbiology Ecology, Vol. 32, Issue 2
Virus-Host and CRISPR Dynamics in Archaea-Dominated Hypersaline Lake Tyrrell, Victoria, Australia
journal, January 2013
- Emerson, Joanne B.; Andrade, Karen; Thomas, Brian C.
- Archaea, Vol. 2013
Viral and microbial community dynamics in four aquatic environments
journal, February 2010
- Rodriguez-Brito, Beltran; Li, LinLin; Wegley, Linda
- The ISME Journal, Vol. 4, Issue 6
Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park
journal, April 2013
- Podar, Mircea; Makarova, Kira S.; Graham, David E.
- Biology Direct, Vol. 8, Issue 1
The distribution of manganese in the Pacific Ocean
journal, February 1980
- Klinkhammer, Gary P.; Bender, Michael L.
- Earth and Planetary Science Letters, Vol. 46, Issue 3
Use of nuclepore filters for counting bacteria by fluorescence microscopy.
journal, January 1977
- Hobbie, J. E.; Daley, R. J.; Jasper, S.
- Applied and Environmental Microbiology, Vol. 33, Issue 5
Works referencing / citing this record:
Temperature-dependent expression of different guanine-plus-cytosine content 16S rRNA genes in Haloarcula strains of the class Halobacteria
journal, August 2018
- Sato, Yu; Kimura, Hiroyuki
- Antonie van Leeuwenhoek, Vol. 112, Issue 2
Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations
journal, September 2018
- Castelle, Cindy J.; Brown, Christopher T.; Anantharaman, Karthik
- Nature Reviews Microbiology, Vol. 16, Issue 10
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
Functional interactions of archaea, bacteria and viruses in a hypersaline endolithic community: Halite metagenome
journal, March 2016
- Crits-Christoph, Alexander; Gelsinger, Diego R.; Ma, Bing
- Environmental Microbiology, Vol. 18, Issue 6
Predominance of deterministic microbial community dynamics in salterns exposed to different light intensities
journal, October 2019
- Viver, Tomeu; Orellana, Luis H.; Díaz, Sara
- Environmental Microbiology, Vol. 21, Issue 11
Extremely halophilic archaeal communities are resilient to short‐term entombment in halite
journal, January 2020
- Huby, Tom J. C.; Clark, Dave R.; McKew, Boyd A.
- Environmental Microbiology
Paleoecology of Neoproterozoic hypersaline environments: Biomarker evidence for haloarchaea, methanogens, and cyanobacteria
journal, July 2017
- Schinteie, R.; Brocks, J. J.
- Geobiology, Vol. 15, Issue 5
Applying Genome-Resolved Metagenomics to Deconvolute the Halophilic Microbiome
journal, March 2019
- Uritskiy, Gherman; DiRuggiero, Jocelyne
- Genes, Vol. 10, Issue 3
Metagenomic Insights into the Uncultured Diversity and Physiology of Microbes in Four Hypersaline Soda Lake Brines
journal, February 2016
- Vavourakis, Charlotte D.; Ghai, Rohit; Rodriguez-Valera, Francisco
- Frontiers in Microbiology, Vol. 7
Expression and Function of Different Guanine-Plus-Cytosine Content 16S rRNA Genes in Haloarcula hispanica at Different Temperatures
journal, March 2017
- Sato, Yu; Fujiwara, Taketomo; Kimura, Hiroyuki
- Frontiers in Microbiology, Vol. 08
Applying Genome-Resolved Metagenomics to Deconvolute the Halophilic Microbiome
journal, March 2019
- Uritskiy, Gherman; DiRuggiero, Jocelyne
- Genes, Vol. 10, Issue 3