Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea

Journal Article · · BMC Genomics
 [1];  [2];  [3];  [2];  [4];  [4];  [5]
  1. Univ. of California, Berkeley, CA (United States). Dept of Environmental Science, Policy, and Management; DOE/OSTI
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division
  3. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  4. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  5. Univ. of California, Berkeley, CA (United States). Dept of Environmental Science, Policy, and Management
Background: Metal sulfide mineral dissolution during bioleaching and acid mine drainage (AMD) formation creates an environment that is inhospitable to most life. Despite dominance by a small number of bacteria, AMD microbial biofilm communities contain a notable variety of coexisting and closely related Euryarchaea, most of which have defied cultivation efforts. For this reason, we used metagenomics to analyze variation in gene content that may contribute to niche differentiation among co-occurring AMD archaea. Our analyses targeted members of the Thermoplasmatales and related archaea. These results greatly expand genomic information available for this archaeal order. Results: We reconstructed near-complete genomes for uncultivated, relatively low abundance organisms A-, E-, and Gplasma, members of Thermoplasmatales order, and for a novel organism, Iplasma. Genomic analyses of these organisms, as well as Ferroplasma type I and II, reveal that all are facultative aerobic heterotrophs with the ability to use many of the same carbon substrates, including methanol. Most of the genomes share genes for toxic metal resistance and surface-layer production. Only Aplasma and Eplasma have a full suite of flagellar genes whereas all but the Ferroplasma spp. have genes for pili production. Cryogenic-electron microscopy (cryo-EM) and tomography (cryo-ET) strengthen these metagenomics-based ultrastructural predictions. Notably, only Aplasma, Gplasma and the Ferroplasma spp. have predicted iron oxidation genes and Eplasma and Iplasma lack most genes for cobalamin, valine, (iso)leucine and histidine synthesis. Conclusion: The Thermoplasmatales AMD archaea share a large number of metabolic capabilities. All of the uncultivated organisms studied here (A-, E-, G-, and Iplasma) are metabolically very similar to characterized Ferroplasma spp., differentiating themselves mainly in their genetic capabilities for biosynthesis, motility, and possibly iron oxidation. These results indicate that subtle, but important genomic differences, coupled with unknown differences in gene expression, distinguish these organisms enough to allow for co-existence. Overall this study reveals shared features of organisms from the Thermoplasmatales lineage and provides new insights into the functioning of AMD communities.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC02-05CH11231; FG02-05ER64134
OSTI ID:
1626419
Journal Information:
BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 14; ISSN 1471-2164
Publisher:
SpringerCopyright Statement
Country of Publication:
United States
Language:
English

References (109)

Metagenomes from High-Temperature Chemotrophic Systems Reveal Geochemical Controls on Microbial Community Structure and Function journal March 2010
Proteomic and bioinformatic analysis of iron- and sulfur-oxidizingAcidithiobacillus ferrooxidans using immobilized pH gradients and mass spectrometry journal August 2006
Thermoplasmatales book January 2006
Genetic and Bioinformatic Insights into Iron and Sulfur Oxidation Mechanisms of Bioleaching Organisms book January 2007
Acetyl-CoA synthetase (ADP forming) in archaea, a novel enzyme involved in acetate formation and ATP synthesis journal January 1993
Plastocyanin: Structural and functional analysis journal February 1994
Acetyl-CoA synthetase (ADP forming) in archaea, a novel enzyme involved in acetate formation and ATP synthesis journal January 1993
Unusual ADP-forming acetyl-coenzyme A synthetases from the mesophilic halophilic euryarchaeon Haloarcula marismortui and from the hyperthermophilic crenarchaeon Pyrobaculum aerophilum journal August 2004
Acyl-CoA Dehydrogenases: Dynamic History of Protein Family Evolution journal July 2009
The rus Operon Genes Are Differentially Regulated When Acidithiobacillus ferrooxidans LR is Kept in Contact with Metal Sulfides journal July 2008
Insertional inactivation of the flaH gene in the archaeon Methanococcus voltae results in non-flagellated cells journal June 2001
Arsenic resistance in the archaeon "Ferroplasma acidarmanus": new insights into the structure and evolution of the ars genes journal January 2003
Towards determining details of anaerobic growth coupled to ferric iron reduction by the acidophilic archaeon ‘Ferroplasma acidarmanus’ Fer1 journal October 2006
Ferroplasma cupricumulans sp. nov., a novel moderately thermophilic, acidophilic archaeon isolated from an industrial-scale chalcocite bioleach heap journal May 2006
Production of methanethiol and volatile sulfur compounds by the archaeon “Ferroplasma acidarmanus” journal October 2007
Ferrous iron oxidation by sulfur-oxidizing Acidithiobacillus ferrooxidans and analysis of the process at the levels of transcription and protein synthesis journal January 2013
The respiratory chain of Thiobacillus ferrooxidans : The reduction of cytochromes by Fe 2+ and the preliminary characterization of rusticyanin a novel ‘blue’ copper protein journal December 1975
Metabolism of glucose via a modified Entner-Doudoroff pathway in the thermoacidophilic archaebacterium Thermoplasma acidophilum journal February 1986
Quinol:fumarate oxidoreductases and succinate:quinone oxidoreductases: phylogenetic relationships, metal centres and membrane attachment journal January 2002
Sulfocyanin and subunit II, two copper proteins with novel features, provide new insight into the archaeal SoxM oxidase supercomplex journal January 2001
Rusticyanin gene expression of Acidithiobacillus ferrooxidans ATCC 33020 in sulfur- and in ferrous iron media journal October 2003
Thermoplasma acidophilum and Thermoplasma volcanium sp. nov. from Solfatara Fields journal March 1988
The microbiology of acidic mine waters journal September 2003
Hexameric Ring Structure of the ATPase Domain of the Membrane-Integrated Metalloprotease FtsH from Thermus thermophilus HB8 journal October 2002
Novel energy metabolism in anaerobic hyperthermophilic archaea: a modified Embden-Meyerhof pathway journal May 2002
Glyceraldehyde dehydrogenases from the thermoacidophilic euryarchaeota Picrophilus torridus and Thermoplasma acidophilum, key enzymes of the non-phosphorylative Entner-Doudoroff pathway, constitute a novel enzyme family within the aldehyde dehydrogenase s journal January 2006
Regulation of acetate and acetyl-CoA converting enzymes during growth on acetate and/or glucose in the halophilic archaeon Haloarcula marismortui journal December 2004
Micron-scale Fe2+/Fe3+, intermediate sulfur species and O2 gradients across the biofilm–solution–sediment interface control biofilm organization journal June 2011
Insights into the iron and sulfur energetic metabolism of Acidithiobacillus ferrooxidans by microarray transcriptome profiling journal September 2006
Haloferax volcanii AglB and AglD are Involved in N-glycosylation of the S-layer Glycoprotein and Proper Assembly of the Surface Layer journal December 2007
The Structure of F-Pili journal January 2009
Unusual pathways and enzymes of central carbohydrate metabolism in Archaea journal December 2005
The Linked Conservation of Structure and Function in a Family of High Diversity journal June 2004
Thermoplasma acidophilum and Thermoplasma volcanium sp. nov. from Solfatara Fields journal March 1988
Insight into Molecular Stability and Physiological Properties of the Diheme Cytochrome CYC 41 from the Acidophilic Bacterium Acidithiobacillus ferrooxidans journal May 2005
Characterization of a New Dihemic c 4 -Type Cytochrome Isolated from Thiobacillus ferrooxidans journal June 2000
Quantitative Proteome and Transcriptome Analysis of the Archaeon Thermoplasma acidophilum Cultured under Aerobic and Anaerobic Conditions journal September 2010
New Structural Proteins of Halobacterium salinarum Gas Vesicle Revealed by Comparative Proteomics Analysis journal March 2011
The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum journal September 2000
Natural acidophilic biofilm communities reflect distinct organismal and functional organization journal October 2008
Correlating carbon monoxide oxidation with cox genes in the abundant Marine Roseobacter Clade journal November 2010
Community genomic analysis of an extremely acidophilic sulfur-oxidizing biofilm journal June 2011
De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities journal June 2011
Community structure and metabolism through reconstruction of microbial genomes from the environment journal February 2004
Formate-driven growth coupled with H2 production journal September 2010
Glucose metabolism in the extreme thermoacidophilic archaebacterium Sulfolobus solfataricus journal December 1984
Isolation and characterization of insertional mutations in flagellin genes in the archaeon Methanococcus voltae journal May 1996
The fla gene cluster is involved in the biogenesis of flagella in Halobacterium salinarum: fla gene cluster in H. salinarum journal August 2001
Mutants in flaI and flaJ of the archaeon Methanococcus voltae are deficient in flagellum assembly: Archaeal flagellum biogenesis in M. voltae journal October 2002
Genome sequence of Picrophilus torridus and its implications for life around pH 0 journal June 2004
Genome dynamics in a natural archaeal population journal January 2007
Biogeography of the Sulfolobus islandicus pan-genome journal May 2009
Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities journal February 2010
Enigmatic, ultrasmall, uncultivated Archaea journal April 2010
Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins journal February 2011
Life on carbon monoxide: X-ray structure of Rhodospirillum rubrum Ni-Fe-S carbon monoxide dehydrogenase journal October 2001
Redox Components of Cytochrome bc-type Enzymes in Acidophilic Prokaryotes journal June 1999
Interaction-induced Redox Switch in the Electron Transfer Complex Rusticyanin-Cytochrome c 4 journal October 1999
Soluble CuA Domain of Cyanobacterial Cytochrome c Oxidase journal March 2004
A New Iron-oxidizing/O 2 -reducing Supercomplex Spanning Both Inner and Outer Membranes, Isolated from the Extreme Acidophile Acidithiobacillus ferrooxidans journal July 2008
Recent developments in the MAFFT multiple sequence alignment program journal March 2008
A simple and fast secondary structure prediction method using hidden neural networks journal September 2004
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models journal August 2006
Glycan structure of a heptose-containing S-layer glycoprotein of Bacillus thermoaerophilus journal January 1995
Structural heterogeneity in the core oligosaccharide of the S-layer glycoprotein from Aneurinibacillus thermoaerophilus DSM 10155 journal August 1999
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix journal April 2009
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform journal July 2002
Picrophilus oshimae and Picrophilus torridus fam. nov., gen. nov., sp. nov., Two Species of Hyperacidophilic, Thermophilic, Heterotrophic, Aerobic Archaea journal July 1996
Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea. journal May 2000
Novel pathways for biosynthesis of nucleotide-activated glycero-manno-heptose precursors of bacterial glycoproteins and cell surface polysaccharides journal July 2002
Thermogymnomonas acidicola gen. nov., sp. nov., a novel thermoacidophilic, cell wall-less archaeon in the order Thermoplasmatales, isolated from a solfataric soil in Hakone, Japan journal November 2007
Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin journal July 2004
Molecular insight into extreme copper resistance in the extremophilic archaeon ‘Ferroplasma acidarmanus’ Fer1 journal August 2005
Analysis of differential protein expression during growth states of Ferroplasma strains and insights into electron transport for iron oxidation journal December 2005
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs journal February 2008
Consed: A Graphical Tool for Sequence Finishing journal March 1998
Isolation and characterization of Ferroplasma thermophilum sp. nov., a novel extremely acidophilic, moderately thermophilic archaeon and its role in bioleaching of chalcopyrite journal August 2008
Electron microscopy encounters with unusual thermophiles helps direct genomic analysis of Aciduliprofundum boonei journal June 2008
Archaeal diversity in a terrestrial acidic spring field revealed by a novel PCR primer targeting archaeal 16S rRNA genes: Novel Archaea in a thermoacidic spring journal April 2011
Molecular mechanisms of copper resistance and accumulation in bacteria journal August 1994
Geographic Barriers Isolate Endemic Populations of Hyperthermophilic Archaea journal August 2003
A Thermophilic, Acidophilic Mycoplasma Isolated from a Coal Refuse Pile journal December 1970
An Archaeal Iron-Oxidizing Extreme Acidophile Important in Acid Mine Drainage journal March 2000
Identification of a Novel Class of Membrane-Bound [NiFe]-Hydrogenases in Thermococcus onnurineus NA1 by In Silico Analysis journal July 2010
Heterotrophic Archaea Contribute to Carbon Cycling in Low-pH, Suboxic Biofilm Communities journal September 2012
Microbial Communities in Contaminated Sediments, Associated with Bioremediation of Uranium to Submicromolar Levels journal May 2008
Community Genomic and Proteomic Analyses of Chemoautotrophic Iron-Oxidizing "Leptospirillum rubarum" (Group II) and "Leptospirillum ferrodiazotrophum" (Group III) Bacteria in Acid Mine Drainage Biofilms journal May 2009
Characterization of an Operon Encoding Two c-Type Cytochromes, an aa3-Type Cytochrome Oxidase, and Rusticyanin in Thiobacillus ferrooxidansATCC 33020 journal November 1999
Mechanism of Pyrite Dissolution in the Presence of Thiobacillus ferrooxidans journal July 1999
Molecular and Culture-Based Analyses of Aerobic Carbon Monoxide Oxidizer Diversity  journal December 2003
Characterization of Ferroplasma Isolates and Ferroplasma acidarmanus sp. nov., Extreme Acidophiles from Acid Mine Drainage and Industrial Bioleaching Environments journal April 2004
Differential Protein Expression during Growth of Acidithiobacillus ferrooxidans on Ferrous Iron, Sulfur Compounds, or Metal Sulfides journal August 2004
The Nonphosphorylative Entner-Doudoroff Pathway in the Thermoacidophilic Euryarchaeon Picrophilus torridus Involves a Novel 2-Keto-3-Deoxygluconate- Specific Aldolase journal December 2009
Genome Analyses of Icelandic Strains of Sulfolobus islandicus, Model Organisms for Genetic and Virus-Host Interaction Studies journal January 2011
Reconstruction of the Central Carbohydrate Metabolism of Thermoproteus tenax by Use of Genomic and Biochemical Data journal April 2004
Towards a Genome-Based Taxonomy for Prokaryotes journal September 2005
Mapping the Tree of Life: Progress and Prospects journal November 2009
Organic solutes in hyperthermophilic archaea journal March 1997
Sequence analysis and expression of the Salmonella typhimurium asr operon encoding production of hydrogen sulfide from sulfite. journal February 1991
The superfamily of heme-copper respiratory oxidases. journal September 1994
Isolation and characterization of flagella and flagellin proteins from the Thermoacidophilic archaea Thermoplasma volcanium and Sulfolobus shibatae. journal February 1996
Involvement of alkylhydroxybenzenes in the Escherichia coli response to the lethal effect of UV irradiation journal April 2012
Gas Vesicles journal June 1975
Functionally specified protein signatures distinctive for each of the different blue copper proteins journal January 2004
A Semi-Quantitative, Synteny-Based Method to Improve Functional Predictions for Hypothetical and Poorly Annotated Bacterial and Archaeal Genes journal October 2011
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments journal March 2010
The Archaeal Respiratory Supercomplex SoxM from S.acidocaldarius Combines Features of Quinole and Cytochrome c Oxidases journal January 2002
Genetic Exchange Across a Species Boundary in the Archaeal Genus Ferroplasma journal July 2007
Identification of proteins present in the archaeon Thermoplasma volcanium cultured in aerobic or anaerobic conditions journal January 2005

Cited By (22)

Elevated temperature alters proteomic responses of individual organisms within a biofilm community journal July 2014
Comparative metagenomic and metatranscriptomic analyses of microbial communities in acid mine drainage journal December 2014
New CRISPR–Cas systems from uncultivated microbes journal December 2016
Dispersing misconceptions and identifying opportunities for the use of 'omics' in soil microbial ecology journal June 2015
Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere journal November 2019
‘ARMAN’ archaea depend on association with euryarchaeal host in culture and in situ journal July 2017
Characterisation of a stable laboratory co-culture of acidophilic nanoorganisms journal June 2017
Diversity, Co-occurrence and Implications of Fungal Communities in Wastewater Treatment Plants journal October 2019
Diversity of Prokaryotic Communities Indigenous to Acid Mine Drainage and Related Rocks from Baiyin Open-Pit Copper Mine Stope, China journal March 2018
Metagenomic analysis reveals adaptations to a cold-adapted lifestyle in a low-temperature acid mine drainage stream journal January 2015
The novel extremely acidophilic, cell-wall-deficient archaeon Cuniculiplasma divulgatum gen. nov., sp. nov. represents a new family, Cuniculiplasmataceae fam. nov., of the order Thermoplasmatales journal January 2016
Microbial residents of the Atlantis Massif’s shallow serpentinite subsurface journal January 2019
15 N- and 2 H proteomic stable isotope probing links nitrogen flow to archaeal heterotrophic activity : Tracking nitrogen flow with proteomic-SIP journal May 2014
Multi-omics Reveals the Lifestyle of the Acidophilic, Mineral-Oxidizing Model Species Leptospirillum ferriphilum T journal November 2017
Diversity and Niche of Archaea in Bioremediation journal September 2018
Archaea dominate the microbial community in an ecosystem with low-to-moderate temperature and extreme acidity journal January 2019
Microbial diversity and metabolic networks in acid mine drainage habitats journal May 2015
S-layers at second glance? Altiarchaeal grappling hooks (hami) resemble archaeal S-layer proteins in structure and sequence journal June 2015
Fungi Contribute Critical but Spatially Varying Roles in Nitrogen and Carbon Cycling in Acid Mine Drainage journal March 2016
Arsenic-Microbe-Mineral Interactions in Mining-Affected Environments journal October 2013
Characterisation of a stable laboratory co-culture of acidophilic nanoorganisms text January 2017
Diversity of Prokaryotic Communities Indigenous to Acid Mine Drainage and Related Rocks from Baiyin Open-Pit Copper Mine Stope, China text January 2018

Similar Records

Metabolic versatility of small archaea Micrarchaeota and Parvarchaeota
Journal Article · Thu Dec 07 23:00:00 EST 2017 · The ISME Journal · OSTI ID:1434028

A new group in the Leptospirillum clade: cultivation-independent community genomics, proteomics and transcriptomics of the new species Leptospirillum group IV UBA BS.
Journal Article · Mon Dec 31 23:00:00 EST 2012 · Applied and Environmental Microbiology · OSTI ID:1122704

Heterotrophic Archaea Contribute to Carbon Cycling in Low-pH, Suboxic Biofilm Communities
Journal Article · Sat Dec 31 23:00:00 EST 2011 · Applied and Environmental Microbiology · OSTI ID:1122705