Culture independent genomic comparisons reveal environmental adaptations for Altiarchaeales
Abstract
The recently proposed candidatus order Altiarchaeales remains an uncultured archaeal lineage composed of genetically diverse, globally widespread organisms frequently observed in anoxic subsurface environments. In spite of 15 years of studies on the psychrophilic biofilm-producing Candidatus Altiarchaeum hamiconexum and its close relatives, very little is known about the phylogenetic and functional diversity of the widespread free-living marine members of this taxon. From methanogenic sediments in the White Oak River Estuary, NC, USA, we sequenced a single cell amplified genome (SAG), WOR_SM1_SCG, and used it to identify and refine two high-quality genomes from metagenomes, WOR_SM1_79 and WOR_SM1_86-2, from the same site. These three genomic reconstructions form a monophyletic group, which also includes three previously published genomes from metagenomes from terrestrial springs and a SAG from Sakinaw Lake in a group previously designated as pMC2A384. A synapomorphic mutation in the Altiarchaeales tRNA synthetase β subunit, pheT, caused the protein to be encoded as two subunits at non-adjacent loci. Consistent with the terrestrial spring clades, our estuarine genomes contained a near-complete autotrophic metabolism, H2 or CO as potential electron donors, a reductive acetyl-CoA pathway for carbon fixation, and methylotroph-like NADP(H)-dependent dehydrogenase. Phylogenies based on 16S rRNA genes and concatenated conserved proteins identified twomore »
- Authors:
-
- Univ. of Tennessee, Knoxville, TN (United States)
- Univ. of Texas at Austin, Port Aransas, TX (United States)
- Univ. of California at Berkeley, Berkeley, CA (United States)
- Univ. of Tennessee, Knoxville, TN (United States); 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 Laboratory Directed Research and Development (LDRD) Program
- OSTI Identifier:
- 1326536
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 7; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; single cell genomics; uncultured archaea; comparative genomics; marine sediment; autotrophy; metagenomics; ecophysiology
Citation Formats
Bird, Jordan T., Baker, Brett J., Probst, Alexander J., Podar, Mircea, and Lloyd, Karen G. Culture independent genomic comparisons reveal environmental adaptations for Altiarchaeales. United States: N. p., 2016.
Web. doi:10.3389/fmicb.2016.01221.
Bird, Jordan T., Baker, Brett J., Probst, Alexander J., Podar, Mircea, & Lloyd, Karen G. Culture independent genomic comparisons reveal environmental adaptations for Altiarchaeales. United States. https://doi.org/10.3389/fmicb.2016.01221
Bird, Jordan T., Baker, Brett J., Probst, Alexander J., Podar, Mircea, and Lloyd, Karen G. Fri .
"Culture independent genomic comparisons reveal environmental adaptations for Altiarchaeales". United States. https://doi.org/10.3389/fmicb.2016.01221. https://www.osti.gov/servlets/purl/1326536.
@article{osti_1326536,
title = {Culture independent genomic comparisons reveal environmental adaptations for Altiarchaeales},
author = {Bird, Jordan T. and Baker, Brett J. and Probst, Alexander J. and Podar, Mircea and Lloyd, Karen G.},
abstractNote = {The recently proposed candidatus order Altiarchaeales remains an uncultured archaeal lineage composed of genetically diverse, globally widespread organisms frequently observed in anoxic subsurface environments. In spite of 15 years of studies on the psychrophilic biofilm-producing Candidatus Altiarchaeum hamiconexum and its close relatives, very little is known about the phylogenetic and functional diversity of the widespread free-living marine members of this taxon. From methanogenic sediments in the White Oak River Estuary, NC, USA, we sequenced a single cell amplified genome (SAG), WOR_SM1_SCG, and used it to identify and refine two high-quality genomes from metagenomes, WOR_SM1_79 and WOR_SM1_86-2, from the same site. These three genomic reconstructions form a monophyletic group, which also includes three previously published genomes from metagenomes from terrestrial springs and a SAG from Sakinaw Lake in a group previously designated as pMC2A384. A synapomorphic mutation in the Altiarchaeales tRNA synthetase β subunit, pheT, caused the protein to be encoded as two subunits at non-adjacent loci. Consistent with the terrestrial spring clades, our estuarine genomes contained a near-complete autotrophic metabolism, H2 or CO as potential electron donors, a reductive acetyl-CoA pathway for carbon fixation, and methylotroph-like NADP(H)-dependent dehydrogenase. Phylogenies based on 16S rRNA genes and concatenated conserved proteins identified two distinct sub-clades of Altiarchaeales, Alti-1 populated by organisms from actively flowing springs, and Alti-2 which was more widespread, diverse, and not associated with visible mats. The core Alti-1 genome suggested Alti-1 is adapted for the stream environment with lipopolysaccharide production capacity and extracellular hami structures. The core Alti-2 genome suggested members of this clade are free-living with distinct mechanisms for energy maintenance, motility, osmoregulation, and sulfur redox reactions. These data suggested that the hamus structures found in Candidatus Altiarchaeum hamiconexum are not present outside of stream-adapted Altiarchaeales. Homologs to a Na+ transporter and membrane bound coenzyme As a result, a disulfide reductase that were unique to the brackish sediment Alti-2 genomes, could indicate adaptations to the estuarine, sulfur-rich environment.},
doi = {10.3389/fmicb.2016.01221},
journal = {Frontiers in Microbiology},
number = ,
volume = 7,
place = {United States},
year = {Fri Aug 05 00:00:00 EDT 2016},
month = {Fri Aug 05 00:00:00 EDT 2016}
}
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Works referenced in this record:
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria
journal, April 2015
- Baker, Brett J.; Lazar, Cassandre Sara; Teske, Andreas P.
- Microbiome, Vol. 3, Issue 1
Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea
journal, February 2016
- Baker, Brett J.; Saw, Jimmy H.; Lind, Anders E.
- Nature Microbiology, Vol. 1, Issue 3
The characterization of functions involved in the establishment and maturation of Klebsiella pneumoniae in vitro biofilm reveals dual roles for surface exopolysaccharides
journal, March 2008
- Balestrino, Damien; Ghigo, Jean-Marc; Charbonnel, Nicolas
- Environmental Microbiology, Vol. 10, Issue 3
Involvement of Lipoprotein NlpI in the Virulence of Adherent Invasive Escherichia coli Strain LF82 Isolated from a Patient with Crohn's Disease
journal, April 2004
- Barnich, N.; Bringer, M. -A.; Claret, L.
- Infection and Immunity, Vol. 72, Issue 5
Single Cell Genomics of Uncultured, Health-Associated Tannerella BU063 (Oral Taxon 286) and Comparison to the Closely Related Pathogen Tannerella forsythia
journal, February 2014
- Beall, Clifford J.; Campbell, Alisha G.; Dayeh, Daniel M.
- PLoS ONE, Vol. 9, Issue 2
ITEP: An integrated toolkit for exploration of microbial pan-genomes
journal, January 2014
- Benedict, Matthew N.; Henriksen, James R.; Metcalf, William W.
- BMC Genomics, Vol. 15, Issue 1
Sulfolobus: A new genus of sulfur-oxidizing bacteria living at low pH and high temperature
journal, January 1972
- Brock, Thomas D.; Brock, Katherine M.; Belly, Robert T.
- Archiv fur Mikrobiologie, Vol. 84, Issue 1, p. 54-68
Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling
journal, March 2015
- Castelle, Cindy J.; Wrighton, Kelly C.; Thomas, Brian C.
- Current Biology, Vol. 25, Issue 6
Galactose Metabolism Plays a Crucial Role in Biofilm Formation by Bacillus subtilis
journal, August 2012
- Chai, Yunrong; Beauregard, Pascale B.; Vlamakis, Hera
- mBio, Vol. 3, Issue 4
Community-wide analysis of microbial genome sequence signatures
journal, January 2009
- Dick, Gregory J.; Andersson, Anders F.; Baker, Brett J.
- Genome Biology, Vol. 10, Issue 8
Accelerated Profile HMM Searches
journal, October 2011
- Eddy, Sean R.
- PLoS Computational Biology, Vol. 7, Issue 10
Anvi’o: an advanced analysis and visualization platform for ‘omics data
journal, January 2015
- Eren, A. Murat; Esen, Özcan C.; Quince, Christopher
- PeerJ, Vol. 3
Structure and Substrate Specificity of the Pyrococcal Coenzyme A Disulfide Reductases/Polysulfide Reductases (CoADR/Psr): Implications for S 0 -Based Respiration and a Sulfur-Dependent Antioxidant System in Pyrococcus
journal, April 2013
- Herwald, Sanna; Liu, Albert Y.; Zhu, Brian E.
- Biochemistry, Vol. 52, Issue 16
ETE: a python Environment for Tree Exploration
journal, January 2010
- Huerta-Cepas, Jaime; Dopazo, Joaquín; Gabaldón, Toni
- BMC Bioinformatics, Vol. 11, Issue 1
eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences
journal, November 2015
- Huerta-Cepas, Jaime; Szklarczyk, Damian; Forslund, Kristoffer
- Nucleic Acids Research, Vol. 44, Issue D1
A new view of the tree of life
journal, April 2016
- Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik
- Nature Microbiology, Vol. 1, Issue 5
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
Variations in sedimentary carbon remineralization rates in the White Oak River estuary, North Carolina
journal, March 1990
- Kelley, Cheryl A.; Martens, Christopher S.; Chanton, Jefrey P.
- Limnology and Oceanography, Vol. 35, Issue 2
Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments
journal, May 2012
- Kubo, Kyoko; Lloyd, Karen G.; F. Biddle, Jennifer
- The ISME Journal, Vol. 6, Issue 10
Relative rates of gene fusion and fission in multi-domain proteins
journal, January 2005
- Kummerfeld, Sarah K.; Teichmann, Sarah A.
- Trends in Genetics, Vol. 21, Issue 1
Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments: Genomic content of uncultured benthic Bathyarchaeota
journal, January 2016
- Lazar, Cassandre Sara; Baker, Brett J.; Seitz, Kiley
- Environmental Microbiology, Vol. 18, Issue 4
Environmental evidence for net methane production and oxidation in putative ANaerobic MEthanotrophic (ANME) archaea: Methanogenesis and methanotrophy in ANME-1 archaea
journal, August 2011
- Lloyd, Karen G.; Alperin, Marc J.; Teske, Andreas
- Environmental Microbiology, Vol. 13, Issue 9
Predominant archaea in marine sediments degrade detrital proteins
journal, March 2013
- Lloyd, Karen G.; Schreiber, Lars; Petersen, Dorthe G.
- Nature, Vol. 496, Issue 7444
Split Leucine-Specific Domain of Leucyl-tRNA Synthetase from the Hyperthermophilic Bacterium Aquifex aeolicus †
journal, December 2006
- Ma, Jing-Jing; Zhao, Ming-Wei; Wang, En-Duo
- Biochemistry, Vol. 45, Issue 49
IMG/M 4 version of the integrated metagenome comparative analysis system
journal, October 2013
- Markowitz, Victor M.; Chen, I-Min A.; Chu, Ken
- Nucleic Acids Research, Vol. 42, Issue D1, p. D568-D573
Interstitial water chemistry of anoxic Long Island Sound sediments. 1. Dissolved gases1: Dissolved gases in sediments
journal, January 1977
- Martens, Christopher S.; Berner, Robert A.
- Limnology and Oceanography, Vol. 22, Issue 1
Early diagenesis in transitional sedimentary environments of the White Oak River Estuary, North Carolina 1: Transitional environments
journal, May 1978
- Martens, Christopher S.; Goldhaber, Martin B.
- Limnology and Oceanography, Vol. 23, Issue 3
Microbial Reefs in the Black Sea Fueled by Anaerobic Oxidation of Methane
journal, August 2002
- Michaelis, W.
- Science, Vol. 297, Issue 5583
The unique structure of archaeal ‘hami’, highly complex cell appendages with nano-grappling hooks: Unique structure of archaeal ‘hami’
journal, March 2005
- Moissl, Christine; Rachel, Reinhard; Briegel, Ariane
- Molecular Microbiology, Vol. 56, Issue 2
Natural Communities of Novel Archaea and Bacteria with a String-of-Pearls-Like Morphology: Molecular Analysis of the Bacterial Partners
journal, February 2002
- Moissl, C.; Rudolph, C.; Huber, R.
- Applied and Environmental Microbiology, Vol. 68, Issue 2
In situ growth of the novel SM1 euryarchaeon from a string-of-pearls-like microbial community in its cold biotope, its physical separation and insights into its structure and physiology
journal, September 2003
- Moissl, Christine; Rudolph, Christian; Rachel, Reinhard
- Archives of Microbiology, Vol. 180, Issue 3
Evaluation of methods for the prediction of membrane spanning regions
journal, July 2001
- Moller, S.; Croning, M. D. R.; Apweiler, R.
- Bioinformatics, Vol. 17, Issue 7
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015
- Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
- Genome Research, Vol. 25, Issue 7
Gene fusion/fission is a major contributor to evolution of multi-domain bacterial proteins
journal, April 2006
- Pasek, S.; Risler, J. -L.; Brezellec, P.
- Bioinformatics, Vol. 22, Issue 12
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
S-layers at second glance? Altiarchaeal grappling hooks (hami) resemble archaeal S-layer proteins in structure and sequence
journal, June 2015
- Perras, Alexandra K.; Daum, Bertram; Ziegler, Christine
- Frontiers in Microbiology, Vol. 6
Grappling archaea: ultrastructural analyses of an uncultivated, cold-loving archaeon, and its biofilm
journal, August 2014
- Perras, Alexandra K.; Wanner, Gerhard; Klingl, Andreas
- Frontiers in Microbiology, Vol. 5
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
“Altiarchaeales”: Uncultivated Archaea from the Subsurface
journal, May 2015
- Probst, Alexander; Moissl-Eichinger, Christine
- Life, Vol. 5, Issue 2
Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO 2 concentrations : Genomic resolution of a high-CO
journal, July 2016
- Probst, Alexander J.; Castelle, Cindy J.; Singh, Andrea
- Environmental Microbiology, Vol. 19, Issue 2
Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface
journal, November 2014
- Probst, Alexander J.; Weinmaier, Thomas; Raymann, Kasie
- Nature Communications, Vol. 5, Issue 1
In Vitro Assembly of the Outer Core of the Lipopolysaccharide from Escherichia coli K-12 and Salmonella typhimurium
journal, February 2014
- Qian, Jinghua; Garrett, Teresa A.; Raetz, Christian R. H.
- Biochemistry, Vol. 53, Issue 8
Cyclic Lipopeptide Production by Plant-Associated Pseudomonas spp.: Diversity, Activity, Biosynthesis, and Regulation
journal, July 2006
- Raaijmakers, Jos M.; de Bruijn, Irene; de Kock, Maarten J. D.
- Molecular Plant-Microbe Interactions, Vol. 19, Issue 7
Global Phylogenomic Analysis Disentangles the Complex Evolutionary History of DNA Replication in Archaea
journal, January 2014
- Raymann, Kasie; Forterre, Patrick; Brochier-Armanet, Céline
- Genome Biology and Evolution, Vol. 6, Issue 1
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
Ecology and microbial structures of archaeal/bacterial strings-of-pearls communities and archaeal relatives thriving in cold sulfidic springs
journal, October 2004
- Rudolph, Christian; Moissl, Christine; Henneberger, Ruth
- FEMS Microbiology Ecology, Vol. 50, Issue 1
Natural Communities of Novel Archaea and Bacteria Growing in Cold Sulfurous Springs with a String-of-Pearls-Like Morphology
journal, May 2001
- Rudolph, C.; Wanner, G.; Huber, R.
- Applied and Environmental Microbiology, Vol. 67, Issue 5
Prokka: rapid prokaryotic genome annotation
journal, March 2014
- Seemann, T.
- Bioinformatics, Vol. 30, Issue 14
Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction
journal, January 2016
- Seitz, Kiley W.; Lazar, Cassandre S.; Hinrichs, Kai-Uwe
- The ISME Journal, Vol. 10, Issue 7
Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization
journal, August 2012
- Sharon, I.; Morowitz, M. J.; Thomas, B. C.
- Genome Research, Vol. 23, Issue 1
Genome evolution
journal, January 2000
- Snel, Berend; Bork, Peer; Huynen, Martijn
- Trends in Genetics, Vol. 16, Issue 1
FusionDB: a database for in-depth analysis of prokaryotic gene fusion events
journal, January 2004
- Suhre, K.
- Nucleic Acids Research, Vol. 32, Issue 90001
Sulfolobus tokodaii sp. nov. (f. Sulfolobus sp. strain 7), a new member of the genus Sulfolobus isolated from Beppu Hot Springs, Japan
journal, February 2002
- Suzuki, Toshiharu; Iwasaki, Toshio; Uzawa, Taketoshi
- Extremophiles, Vol. 6, Issue 1
Genomic and Metabolic Diversity of Marine Group I Thaumarchaeota in the Mesopelagic of Two Subtropical Gyres
journal, April 2014
- Swan, Brandon K.; Chaffin, Mark D.; Martinez-Garcia, Manuel
- PLoS ONE, Vol. 9, Issue 4
Rapid Detection and Quantification of Members of the Archaeal Community by Quantitative PCR Using Fluorogenic Probes
journal, November 2000
- Takai, K.; Horikoshi, K.
- Applied and Environmental Microbiology, Vol. 66, Issue 11
Microbial Diversity of Hydrothermal Sediments in the Guaymas Basin: Evidence for Anaerobic Methanotrophic Communities
journal, April 2002
- Teske, A.; Hinrichs, K. -U.; Edgcomb, V.
- Applied and Environmental Microbiology, Vol. 68, Issue 4
The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism
journal, October 2003
- Waters, E.; Hohn, M. J.; Ahel, I.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 22
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012
- Wrighton, K. C.; Thomas, B. C.; Sharon, I.
- Science, Vol. 337, Issue 6102
Isolation of Genes Involved in Biofilm Formation of a Klebsiella pneumoniae Strain Causing Pyogenic Liver Abscess
journal, August 2011
- Wu, Meng-Chuan; Lin, Tzu-Lung; Hsieh, Pei-Fang
- PLoS ONE, Vol. 6, Issue 8
Analysis of community structures in anaerobic processes using a quantitative real-time PCR method
journal, July 2005
- Yu, Y.; Lee, C.; Hwang, S.
- Water Science and Technology, Vol. 52, Issue 1-2
Sequencing genomes from single cells by polymerase cloning
journal, May 2006
- Zhang, Kun; Martiny, Adam C.; Reppas, Nikos B.
- Nature Biotechnology, Vol. 24, Issue 6, p. 680-686
The Sulfolobus-?Caldariella? group: Taxonomy on the basis of the structure of DNA-dependent RNA polymerases
journal, April 1980
- Zillig, Wolfram; Stetter, Karl O.; Wunderl, Simon
- Archives of Microbiology, Vol. 125, Issue 3
Commensal Pseudomonas protect Arabidopsis thaliana from a coexisting pathogen via multiple lineage-dependent mechanisms
journal, December 2021
- Shalev, Or; Ashkenazy, Haim; Neumann, Manuela
- The ISME Journal, Vol. 16, Issue 5
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Metal-ion-induced expression of gene fragments from subseafloor micro-organisms in the Kumano forearc basin, Nankai Trough
journal, September 2018
- Wakamatsu, T.; Morono, Y.; Futagami, T.
- Journal of Applied Microbiology, Vol. 125, Issue 5