Hypersaline sapropels act as hotspots for microbial dark matter
Abstract
Present-day terrestrial analogue sites are crucial ground truth proxies for studying life in geochemical conditions close to those assumed to be present on early Earth or inferred to exist on other celestial bodies (e.g. Mars, Europa). Although hypersaline sapropels are border-of-life habitats with moderate occurrence, their microbiological and physicochemical characterization lags behind. Here, we study the diversity of life under low water activity by describing the prokaryotic communities from two disparate hypersaline sapropels (Transylvanian Basin, Romania) in relation to geochemical milieu and pore water chemistry, while inferring their role in carbon cycling by matching taxa to known taxon-specific biogeochemical functions. Furthermore, the polyphasic approach combined deep coverage SSU rRNA gene amplicon sequencing and bioinformatics with RT-qPCR and physicochemical investigations. We found that sapropels developed an analogous elemental milieu and harbored prokaryotes affiliated with fifty-nine phyla, among which the most abundant were Proteobacteria, Bacteroidetes and Chloroflexi. Containing thirty-two candidate divisions and possibly undocumented prokaryotic lineages, the hypersaline sapropels were found to accommodate one of the most diverse and novel ecosystems reported to date and may contribute to completing the phylogenetic branching of the tree of life.
- Authors:
-
[1];
[3];
[5]
- Babes-Bolyai Univ., Cluj-Napoca (Romania); Biology Center of the Academy of Sciences of the Czech Republic, Ceske Budejovice (Czech Republic)
- National Institute of Research and Development for Biological Sciences (NIRDBS), Cluj-Napoca (Romania)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Interstitial Genomics, LLC, Longmont, CO (United States)
- Medical Univ. of Graz, Graz (Austria)
- Babes-Bolyai Univ., Cluj-Napoca (Romania)
- Babes-Bolyai Univ., Cluj-Napoca (Romania); National Institute of Research and Development for Biological Sciences (NIRDBS), Cluj-Napoca (Romania)
- INCDO-INOE 2000, Cluj-Napoca (Romania)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1400156
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Scientific Reports
- Additional Journal Information:
- Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2045-2322
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES
Citation Formats
Andrei, Adrian -Stefan, Baricz, Andreea, Robeson, Michael Scott, Pausan, Manuela Raluca, Tamas, Tudor, Chiriac, Cecilia, Szekeres, Edina, Barbu-Tudoran, Lucian, Levei, Erika Andrea, Coman, Cristian, Podar, Mircea, and Banciu, Horia Leonard. Hypersaline sapropels act as hotspots for microbial dark matter. United States: N. p., 2017.
Web. doi:10.1038/s41598-017-06232-w.
Andrei, Adrian -Stefan, Baricz, Andreea, Robeson, Michael Scott, Pausan, Manuela Raluca, Tamas, Tudor, Chiriac, Cecilia, Szekeres, Edina, Barbu-Tudoran, Lucian, Levei, Erika Andrea, Coman, Cristian, Podar, Mircea, & Banciu, Horia Leonard. Hypersaline sapropels act as hotspots for microbial dark matter. United States. https://doi.org/10.1038/s41598-017-06232-w
Andrei, Adrian -Stefan, Baricz, Andreea, Robeson, Michael Scott, Pausan, Manuela Raluca, Tamas, Tudor, Chiriac, Cecilia, Szekeres, Edina, Barbu-Tudoran, Lucian, Levei, Erika Andrea, Coman, Cristian, Podar, Mircea, and Banciu, Horia Leonard. Fri .
"Hypersaline sapropels act as hotspots for microbial dark matter". United States. https://doi.org/10.1038/s41598-017-06232-w. https://www.osti.gov/servlets/purl/1400156.
@article{osti_1400156,
title = {Hypersaline sapropels act as hotspots for microbial dark matter},
author = {Andrei, Adrian -Stefan and Baricz, Andreea and Robeson, Michael Scott and Pausan, Manuela Raluca and Tamas, Tudor and Chiriac, Cecilia and Szekeres, Edina and Barbu-Tudoran, Lucian and Levei, Erika Andrea and Coman, Cristian and Podar, Mircea and Banciu, Horia Leonard},
abstractNote = {Present-day terrestrial analogue sites are crucial ground truth proxies for studying life in geochemical conditions close to those assumed to be present on early Earth or inferred to exist on other celestial bodies (e.g. Mars, Europa). Although hypersaline sapropels are border-of-life habitats with moderate occurrence, their microbiological and physicochemical characterization lags behind. Here, we study the diversity of life under low water activity by describing the prokaryotic communities from two disparate hypersaline sapropels (Transylvanian Basin, Romania) in relation to geochemical milieu and pore water chemistry, while inferring their role in carbon cycling by matching taxa to known taxon-specific biogeochemical functions. Furthermore, the polyphasic approach combined deep coverage SSU rRNA gene amplicon sequencing and bioinformatics with RT-qPCR and physicochemical investigations. We found that sapropels developed an analogous elemental milieu and harbored prokaryotes affiliated with fifty-nine phyla, among which the most abundant were Proteobacteria, Bacteroidetes and Chloroflexi. Containing thirty-two candidate divisions and possibly undocumented prokaryotic lineages, the hypersaline sapropels were found to accommodate one of the most diverse and novel ecosystems reported to date and may contribute to completing the phylogenetic branching of the tree of life.},
doi = {10.1038/s41598-017-06232-w},
journal = {Scientific Reports},
number = 1,
volume = 7,
place = {United States},
year = {Fri Jul 21 00:00:00 EDT 2017},
month = {Fri Jul 21 00:00:00 EDT 2017}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 10 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Geochemistry and Mineralogy of Western Australian Salt Lake Sediments: Implications for Meridiani Planum on Mars
journal, July 2016
- Ruecker, A.; Schröder, C.; Byrne, J.
- Astrobiology, Vol. 16, Issue 7
Culturable diversity of aerobic halophilic archaea (Fam. Halobacteriaceae) from hypersaline, meromictic Transylvanian lakes
journal, February 2015
- Baricz, Andreea; Cristea, Adorján; Muntean, Vasile
- Extremophiles, Vol. 19, Issue 2
Cutadapt removes adapter sequences from high-throughput sequencing reads
journal, May 2011
- Martin, Marcel
- EMBnet.journal, Vol. 17, Issue 1
Cutadapt removes adapter sequences from high-throughput sequencing reads
journal, May 2011
- Martin, Marcel
- EMBnet.journal, Vol. 17, Issue 1
Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA.
journal, January 1993
- Muyzer, G.; de Waal, E. C.; Uitterlinden, A. G.
- Applied and Environmental Microbiology, Vol. 59, Issue 3
Culturable diversity of aerobic halophilic archaea (Fam. Halobacteriaceae) from hypersaline, meromictic Transylvanian lakes
journal, February 2015
- Baricz, Andreea; Cristea, Adorján; Muntean, Vasile
- Extremophiles, Vol. 19, Issue 2
Extracellular DNA extraction is a fast, cheap and reliable alternative for multi-taxa surveys based on soil DNA
journal, May 2016
- Zinger, Lucie; Chave, Jérôme; Coissac, Eric
- Soil Biology and Biochemistry, Vol. 96
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea
journal, December 2011
- McDonald, Daniel; Price, Morgan N.; Goodrich, Julia
- The ISME Journal, Vol. 6, Issue 3
UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013
- Edgar, Robert C.
- Nature Methods, Vol. 10, Issue 10
Planetary habitability: lessons learned from terrestrial analogues
journal, January 2014
- Preston, Louisa J.; Dartnell, Lewis R.
- International Journal of Astrobiology, Vol. 13, Issue 1
Geochemistry and Mineralogy of Western Australian Salt Lake Sediments: Implications for Meridiani Planum on Mars
journal, July 2016
- Ruecker, A.; Schröder, C.; Byrne, J.
- Astrobiology, Vol. 16, Issue 7
Practical innovations for high-throughput amplicon sequencing
journal, September 2013
- Lundberg, Derek S.; Yourstone, Scott; Mieczkowski, Piotr
- Nature Methods, Vol. 10, Issue 10
A Deeply Branching Thermophilic Bacterium with an Ancient Acetyl-CoA Pathway Dominates a Subsurface Ecosystem
journal, January 2012
- Takami, Hideto; Noguchi, Hideki; Takaki, Yoshihiro
- PLoS ONE, Vol. 7, Issue 1
Microbial biosignatures in evaporite deposits: Evidence from Death Valley, California
journal, January 2004
- Douglas, Susanne
- Planetary and Space Science, Vol. 52, Issue 1-3
The protection and management of saline lakes of therapeutic value in Romania
journal, December 1993
- Bulgâreanu, V. A. C.
- International Journal of Salt Lake Research, Vol. 2, Issue 2
Enumeration of Archaea and Bacteria in seafloor basalt using real-time quantitative PCR and fluorescence microscopy: Enumeration of Archaea and Bacteria in seafloor basalt
journal, April 2008
- Einen, Jørn; Thorseth, Ingunn H.; Øvreås, Lise
- FEMS Microbiology Letters, Vol. 282, Issue 2
Physicochemical characterization, elemental speciation and hydrogeochemical modeling of river and peloid sediments used for therapeutic uses
journal, February 2015
- Suárez Muñoz, Margaret; Melián Rodríguez, Clara; Gelen Rudnikas, Alina
- Applied Clay Science, Vol. 104
Selective preservation of organic matter in marine environments; processes and impact on the sedimentary record
journal, January 2010
- Zonneveld, K. A. F.; Versteegh, G. J. M.; Kasten, S.
- Biogeosciences, Vol. 7, Issue 2
Genomic properties of Marine Group A bacteria indicate a role in the marine sulfur cycle
journal, September 2013
- Wright, Jody J.; Mewis, Keith; Hanson, Niels W.
- The ISME Journal, Vol. 8, Issue 2
Extracellular DNA extraction is a fast, cheap and reliable alternative for multi-taxa surveys based on soil DNA
journal, May 2016
- Zinger, Lucie; Chave, Jérôme; Coissac, Eric
- Soil Biology and Biochemistry, Vol. 96
Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes
journal, May 2015
- Andrei, Adrian-Ştefan; Robeson, Michael S.; Baricz, Andreea
- The ISME Journal, Vol. 9, Issue 12
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
UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013
- Edgar, Robert C.
- Nature Methods, Vol. 10, Issue 10
Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla
journal, October 2013
- Kantor, Rose S.; Wrighton, Kelly C.; Handley, Kim M.
- mBio, Vol. 4, Issue 5
Compact graphical representation of phylogenetic data and metadata with GraPhlAn
journal, January 2015
- Asnicar, Francesco; Weingart, George; Tickle, Timothy L.
- PeerJ, Vol. 3
Simultaneous Measurements of Organic Carbon Mineralization and Bacterial Production in Oxic and Anoxic Lake Sediments
journal, July 2003
- Bastviken, D.; Olsson, M.; Tranvik, L.
- Microbial Ecology, Vol. 46, Issue 1
Extraction, detection and persistence of extracellular DNA in forest litter microcosms
journal, October 2004
- England, L. S.; Vincent, M. L.; Trevors, J. T.
- Molecular and Cellular Probes, Vol. 18, Issue 5
Extraction, detection and persistence of extracellular DNA in forest litter microcosms
journal, October 2004
- England, L. S.; Vincent, M. L.; Trevors, J. T.
- Molecular and Cellular Probes, Vol. 18, Issue 5
Phylogenetic analysis of community assembly and structure over space and time
journal, November 2008
- Emerson, Brent C.; Gillespie, Rosemary G.
- Trends in Ecology & Evolution, Vol. 23, Issue 11
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data
journal, October 2012
- Kopylova, Evguenia; Noé, Laurent; Touzet, Hélène
- Bioinformatics, Vol. 28, Issue 24
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data
journal, October 2012
- Kopylova, Evguenia; Noé, Laurent; Touzet, Hélène
- Bioinformatics, Vol. 28, Issue 24
Phylogenetic analysis of community assembly and structure over space and time
journal, November 2008
- Emerson, Brent C.; Gillespie, Rosemary G.
- Trends in Ecology & Evolution, Vol. 23, Issue 11
Genomic properties of Marine Group A bacteria indicate a role in the marine sulfur cycle
journal, September 2013
- Wright, Jody J.; Mewis, Keith; Hanson, Niels W.
- The ISME Journal, Vol. 8, Issue 2
Diversity of cultivable halophilic archaea and bacteria from superficial hypersaline sediments of Tunisian solar salterns
journal, July 2014
- Boujelben, Ines; Martínez-García, Manuel; van Pelt, Jos
- Antonie van Leeuwenhoek, Vol. 106, Issue 4
Extremophile microbiomes in acidic and hypersaline river sediments of Western Australia: Extremophiles in acidic hypersaline river sediments
journal, December 2015
- Lu, Shipeng; Peiffer, Stefan; Lazar, Cassandre Sara
- Environmental Microbiology Reports, Vol. 8, Issue 1
Characterization of Bacterial Communities Associated with Organic Aggregates in a Large, Shallow, Eutrophic Freshwater Lake (Lake Taihu, China)
journal, January 2009
- Tang, Xiangming; Gao, Guang; Qin, Boqiang
- Microbial Ecology, Vol. 58, Issue 2
Selective preservation of organic matter in marine environments; processes and impact on the sedimentary record
journal, January 2010
- Zonneveld, K. A. F.; Versteegh, G. J. M.; Kasten, S.
- Biogeosciences, Vol. 7, Issue 2
Physicochemical characterization, elemental speciation and hydrogeochemical modeling of river and peloid sediments used for therapeutic uses
journal, February 2015
- Suárez Muñoz, Margaret; Melián Rodríguez, Clara; Gelen Rudnikas, Alina
- Applied Clay Science, Vol. 104
Microbiota-accessible carbohydrates suppress Clostridium difficile infection in a murine model
journal, April 2018
- Hryckowian, Andrew J.; Van Treuren, William; Smits, Samuel A.
- Nature Microbiology, Vol. 3, Issue 6
Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes
journal, May 2015
- Andrei, Adrian-Ştefan; Robeson, Michael S.; Baricz, Andreea
- The ISME Journal, Vol. 9, Issue 12
Peloids and pelotherapy: Historical evolution, classification and glossary
journal, May 2013
- Gomes, Celso; Carretero, Maria Isabel; Pozo, Manuel
- Applied Clay Science, Vol. 75-76
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
Microbial biosignatures in evaporite deposits: Evidence from Death Valley, California
journal, January 2004
- Douglas, Susanne
- Planetary and Space Science, Vol. 52, Issue 1-3
Temperature and salinity history of the Precambrian ocean: implications for the course of microbial evolution
journal, April 2005
- Knauth, L. Paul
- Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 219, Issue 1-2
Microbial dissolution of clay minerals as a source of iron and silica in marine sediments
journal, February 2009
- Vorhies, John S.; Gaines, Robert R.
- Nature Geoscience, Vol. 2, Issue 3
Temperature and salinity history of the Precambrian ocean: implications for the course of microbial evolution
journal, April 2005
- Knauth, L. Paul
- Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 219, Issue 1-2
Salt marsh sediment diversity: a test of the variability of the rare biosphere among environmental replicates
journal, June 2012
- Bowen, Jennifer L.; Morrison, Hilary G.; Hobbie, John E.
- The ISME Journal, Vol. 6, Issue 11
Microbial dissolution of clay minerals as a source of iron and silica in marine sediments
journal, February 2009
- Vorhies, John S.; Gaines, Robert R.
- Nature Geoscience, Vol. 2, Issue 3
Salt marsh sediment diversity: a test of the variability of the rare biosphere among environmental replicates
journal, June 2012
- Bowen, Jennifer L.; Morrison, Hilary G.; Hobbie, John E.
- The ISME Journal, Vol. 6, Issue 11
Layered subsurface in Utopia Basin of Mars revealed by Zhurong rover radar
journal, September 2022
- Li, Chao; Zheng, Yikang; Wang, Xin
- Nature, Vol. 610, Issue 7931
Compact graphical representation of phylogenetic data and metadata with GraPhlAn
journal, January 2015
- Asnicar, Francesco; Weingart, George; Tickle, Timothy L.
- PeerJ, Vol. 3
A putative greigite-type magnetosome gene cluster from the candidate phylum L atescibacteria: Magnetosome gene cluster from Latescibacteria
journal, December 2014
- Lin, Wei; Pan, Yongxin
- Environmental Microbiology Reports, Vol. 7, Issue 2
Members of the uncultured bacterial candidate division WWE1 are implicated in anaerobic digestion of cellulose
journal, February 2014
- Limam, Rim Driss; Chouari, Rakia; Mazéas, Laurent
- MicrobiologyOpen, Vol. 3, Issue 2
Single-cell analysis reveals a novel uncultivated magnetotactic bacterium within the candidate division OP3: Uncultivated MTB in candidate division OP3
journal, October 2011
- Kolinko, Sebastian; Jogler, Christian; Katzmann, Emanuel
- Environmental Microbiology, Vol. 14, Issue 7
Preservation, origin and genetic imprint of extracellular DNA in permanently anoxic deep-sea sediments: GENE SEQUENCES PRESERVED IN EXTRACELLULAR DNA
journal, December 2010
- Corinaldesi, C.; Barucca, M.; Luna, G. M.
- Molecular Ecology, Vol. 20, Issue 3
METAGENassist: a comprehensive web server for comparative metagenomics
journal, May 2012
- Arndt, D.; Xia, J.; Liu, Y.
- Nucleic Acids Research, Vol. 40, Issue W1
A Deeply Branching Thermophilic Bacterium with an Ancient Acetyl-CoA Pathway Dominates a Subsurface Ecosystem
journal, January 2012
- Takami, Hideto; Noguchi, Hideki; Takaki, Yoshihiro
- PLoS ONE, Vol. 7, Issue 1
Infant gut microbiota characteristics generally do not modify effects of lipid-based nutrient supplementation on growth or inflammation: secondary analysis of a randomized controlled trial in Malawi
journal, September 2020
- Hughes, Riley L.; Arnold, Charles D.; Young, Rebecca R.
- Scientific Reports, Vol. 10, Issue 1
Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments
journal, February 2010
- Hollister, Emily B.; Engledow, Amanda S.; Hammett, Amy Jo M.
- The ISME Journal, Vol. 4, Issue 6
Impact of training sets on classification of high-throughput bacterial 16s rRNA gene surveys
journal, June 2011
- Werner, Jeffrey J.; Koren, Omry; Hugenholtz, Philip
- The ISME Journal, Vol. 6, Issue 1
Transient liquid water and water activity at Gale crater on Mars
journal, April 2015
- Martín-Torres, F. Javier; Zorzano, María-Paz; Valentín-Serrano, Patricia
- Nature Geoscience, Vol. 8, Issue 5
Works referencing / citing this record:
Bioturbation of peanut worms Sipunculus nudus on the composition of prokaryotic communities in a tidal flat as revealed by 16S rRNA gene sequences
journal, February 2019
- Li, Junwei; Hu, Ruiping; Guo, Yongjian
- MicrobiologyOpen, Vol. 8, Issue 8
Ecology and physiology of halophilic microorganisms – Thematic issue based on papers presented at Halophiles 2019 – 12th International Conference on Halophilic Microorganisms, Cluj-Napoca, Romania, 24–28 June, 2019
journal, December 2019
- Banciu, Horia L.; Enache, Mădălin; Rodriguez, Rafael Montalvo
- FEMS Microbiology Letters, Vol. 366, Issue 23
Spatio‐temporal insights into microbiology of the freshwater‐to‐hypersaline, oxic‐hypoxic‐euxinic waters of Ursu Lake
journal, January 2020
- Baricz, Andreea; Chiriac, Cecilia Maria; Andrei, Adrian‐Ștefan
- Environmental Microbiology
Bioturbation of peanut worms Sipunculus nudus on the composition of prokaryotic communities in a tidal flat as revealed by 16S rRNA gene sequences
journal, February 2019
- Li, Junwei; Hu, Ruiping; Guo, Yongjian
- MicrobiologyOpen, Vol. 8, Issue 8