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Title: Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments

Journal Article · · Environmental Microbiology

Summary Members of the phylum Acidobacteria are abundant and ubiquitous across soils. We performed a large‐scale comparative genome analysis spanning subdivisions 1, 3, 4, 6, 8 and 23 ( n  = 24) with the goal to identify features to help explain their prevalence in soils and understand their ecophysiology. Our analysis revealed that bacteriophage integration events along with transposable and mobile elements influenced the structure and plasticity of these genomes. Low‐ and high‐affinity respiratory oxygen reductases were detected in multiple genomes, suggesting the capacity for growing across different oxygen gradients. Among many genomes, the capacity to use a diverse collection of carbohydrates, as well as inorganic and organic nitrogen sources (such as via extracellular peptidases), was detected – both advantageous traits in environments with fluctuating nutrient environments. We also identified multiple soil acidobacteria with the potential to scavenge atmospheric concentrations of H 2 , now encompassing mesophilic soil strains within the subdivision 1 and 3, in addition to a previously identified thermophilic strain in subdivision 4. This large‐scale acidobacteria genome analysis reveal traits that provide genomic, physiological and metabolic versatility, presumably allowing flexibility and versatility in the challenging and fluctuating soil environment.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1425534
Journal Information:
Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 3 Vol. 20; ISSN 1462-2912
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (129)

Numerical analysis of bacterial transport in saturated porous media journal January 2006
Viruses in Soil book January 2014
Holophaga foetida gen. nov., sp. nov., a new, homoacetogenic bacterium degrading methoxylated aromatic compounds journal July 1994
Acidobacterium capsulatum gen. nov., sp. nov.: An acidophilic chemoorganotrophic bacterium containing menaquinone from acidic mineral environment journal January 1991
Thermotomaculum hydrothermale gen. nov., sp. nov., a novel heterotrophic thermophile within the phylum Acidobacteria from a deep-sea hydrothermal vent chimney in the Southern Okinawa Trough journal January 2012
Centrifugal extraction and determination of free amino acids in soil solutions by TLC using tritiated 1-fluoro-2,4-dinitrobenzene journal January 1985
A novel scenario for the evolution of haem–copper oxygen reductases journal June 2001
Purification and characterization of the single-component nitric oxide reductase from Ralstonia eutropha H16 journal October 1999
PCR primers and functional probes for amplification and detection of bacterial genes for extracellular peptidases in single strains and in soil journal March 2001
Proteolytic activity in soil: A review journal August 2013
Looking for the minimum common denominator in haem–copper oxygen reductases: Towards a unified catalytic mechanism journal July 2008
Cytochrome bd oxidase and bacterial tolerance to oxidative and nitrosative stress journal July 2014
Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools journal June 2008
Factors influencing variability of proteolytic genes and activities in arable soils journal July 2008
Pathways of nitrogen utilization by soil microorganisms – A review journal December 2010
Blastocatella fastidiosa gen. nov., sp. nov., isolated from semiarid savanna soil – The first described species of Acidobacteria subdivision 4 journal March 2013
Silvibacterium bohemicum gen. nov. sp. nov., an acidobacterium isolated from coniferous soil in the Bohemian Forest National Park journal February 2016
Adapting to environmental changes using specialized paralogs journal April 2008
Denitrification in pathogenic bacteria: for better or worst? journal May 2005
A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses journal January 2009
Abundances and potential activities of nitrogen cycling microbial communities along a chronosequence of a glacier forefield journal December 2010
Genetic and life-history traits associated with the distribution of prophages in bacteria journal March 2016
Genome sequencing in microfabricated high-density picolitre reactors journal July 2005
Structures of protein–protein complexes involved in electron transfer journal March 2013
Uncovering Earth’s virome journal August 2016
Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses journal September 2016
Bacterial glycosidases for the production of universal red blood cells journal April 2007
Cryptic prophages help bacteria cope with adverse environments journal December 2010
GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes journal May 2010
Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data journal May 2013
Horizontal gene transfer: building the web of life journal July 2015
Mobile genetic elements: the agents of open source evolution journal September 2005
Shallow breathing: bacterial life at low O2 journal February 2013
HydDB: A web tool for hydrogenase classification and analysis journal September 2016
Binding and activation of nitrite and nitric oxide by copper nitrite reductase and corresponding model complexes journal January 2012
The cytochrome cbb 3 from Pseudomonas stutzeri displays nitric oxide reductase activity : NO reductase activity of cytochrome journal December 2001
Roles of NapF, NapG and NapH, subunits of the Escherichia coli periplasmic nitrate reductase, in ubiquinol oxidation: Roles of NapF, G and H in ubiquinol oxidation in E. coli journal April 2002
The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenic fungus Magnaporthe grisea: Glyoxylate cycle in Magnaporthe journal March 2003
Antagonism of PII signalling by the AmtB protein of Escherichia coli: AmtB antagonizes PII signalling journal May 2003
Prophages and bacterial genomics: what have we learned so far?: Prophage genomics journal June 2003
Genomic insights that advance the species definition for prokaryotes journal February 2005
Atomic resolution structures of resting-state, substrate- and product-complexed Cu-nitrite reductase provide insight into catalytic mechanism journal August 2005
High-quality draft assemblies of mammalian genomes from massively parallel sequence data journal December 2010
Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging journal August 2015
PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating journal June 2009
IMG ER: a system for microbial genome annotation expert review and curation journal June 2009
A low-polynomial algorithm for assembling clusters of orthologous groups from intergenomic symmetric best matches journal May 2010
genoPlotR: comparative gene and genome visualization in R journal July 2010
Easyfig: a genome comparison visualizer journal January 2011
SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes journal May 2012
Membrane sequestration of the signal transduction protein GlnK by the ammonium transporter AmtB journal February 2002
Reticulate Representation of Evolutionary and Functional Relationships between Phage Genomes journal February 2008
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence journal March 1997
ARB: a software environment for sequence data journal February 2004
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB journal November 2007
HMMER web server: interactive sequence similarity searching journal May 2011
dbCAN: a web resource for automated carbohydrate-active enzyme annotation journal May 2012
Pfam: the protein families database journal November 2013
eggNOG v4.0: nested orthology inference across 3686 organisms journal December 2013
Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation journal November 2015
Microbial species delineation using whole genome sequences journal July 2015
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees journal April 2016
PHASTER: a better, faster version of the PHAST phage search tool journal May 2016
Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer journal October 1999
Chloracidobacterium thermophilum gen. nov., sp. nov.: an anoxygenic microaerophilic chlorophotoheterotrophic acidobacterium journal February 2015
Bryobacter aggregatus gen. nov., sp. nov., a peat-inhabiting, aerobic chemo-organotroph from subdivision 3 of the Acidobacteria journal August 2009
Terriglobus saanensis sp. nov., an acidobacterium isolated from tundra soil journal December 2010
Telmatobacter bradus gen. nov., sp. nov., a cellulolytic facultative anaerobe from subdivision 1 of the Acidobacteria, and emended description of Acidobacterium capsulatum Kishimoto et al. 1991
  • Pankratov, T. A.; Kirsanova, L. A.; Kaparullina, E. N.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 62, Issue 2, p. 430-437 https://doi.org/10.1099/ijs.0.029629-0
journal April 2011
Granulicella arctica sp. nov., Granulicella mallensis sp. nov., Granulicella tundricola sp. nov. and Granulicella sapmiensis sp. nov., novel acidobacteria from tundra soil journal November 2011
Bryocella elongata gen. nov., sp. nov., a member of subdivision 1 of the Acidobacteria isolated from a methanotrophic enrichment culture, and emended description of Edaphobacter aggregans Koch et al. 2008 journal May 2011
Thermoanaerobaculum aquaticum gen. nov., sp. nov., the first cultivated member of Acidobacteria subdivision 23, isolated from a hot spring journal June 2013
Pyrinomonas methylaliphatogenes gen. nov., sp. nov., a novel group 4 thermophilic member of the phylum Acidobacteria from geothermal soils journal September 2013
Edaphobacter modestus gen. nov., sp. nov., and Edaphobacter aggregans sp. nov., acidobacteria isolated from alpine and forest soils journal May 2008
The first representative of the globally widespread subdivision 6 Acidobacteria, Vicinamibacter silvestris gen. nov., sp. nov., isolated from subtropical savannah soil journal August 2016
Membrane-bound oxygen reductases of the anaerobic sulfate-reducing Desulfovibrio vulgaris Hildenborough: roles in oxygen defence and electron link with periplasmic hydrogen oxidation journal October 2013
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs journal February 2008
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal May 2015
Base-Calling of Automated Sequencer Traces Using Phred.  I. Accuracy Assessment journal March 1998
Consed: A Graphical Tool for Sequence Finishing journal March 1998
The Biochemistry and Structural Biology of Plant Cell Wall Deconstruction journal April 2010
Acidobacterial community responses to agricultural management of soybean in Amazon forest soils journal October 2012
Acidobacteria dominate the active bacterial communities of Arctic tundra with widely divergent winter-time snow accumulation and soil temperatures journal November 2012
Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase journal March 2010
The oxidative and nitrosative stress defence network of Wolinella succinogenes: cytochrome c nitrite reductase mediates the stress response to nitrite, nitric oxide, hydroxylamine and hydrogen peroxide: Stress defence networks in W. succinogenes journal June 2011
Complete genome of Candidatus Chloracidobacterium thermophilum, a chlorophyll-based photoheterotroph belonging to the phylum Acidobacteria: Candidatus Chloracidobacterium thermophilum genome journal September 2011
Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers journal March 2012
Comparative genomic and physiological analysis provides insights into the role of Acidobacteria in organic carbon utilization in Arctic tundra soils journal April 2012
Acidophilic and thermophilic Bacillus strains from geothermally heated antarctic soil journal August 1989
Various players in the nitrogen cycle: Diversity and functions of the microorganisms involved in nitrification and denitrification journal February 2008
Sulfur Oxidation Genes in Diverse Deep-Sea Viruses journal May 2014
Genome Data Mining and Soil Survey for the Novel Group 5 [NiFe]-Hydrogenase To Explore the Diversity and Ecological Importance of Presumptive High-Affinity H 2 -Oxidizing Bacteria journal July 2011
Influence of Plant Polymers on the Distribution and Cultivation of Bacteria in the Phylum Acidobacteria journal November 2010
Acidobacteria Phylum Sequences in Uranium-Contaminated Subsurface Sediments Greatly Expand the Known Diversity within the Phylum journal March 2007
Isolation and Characterization of Soil Bacteria That Define Terriglobus gen. nov., in the Phylum Acidobacteria journal February 2007
Three Genomes from the Phylum Acidobacteria Provide Insight into the Lifestyles of These Microorganisms in Soils journal February 2009
Phylogenetic Distribution of Potential Cellulases in Bacteria journal December 2012
Terracidiphilus gabretensis gen. nov., sp. nov., an Abundant and Active Forest Soil Acidobacterium Important in Organic Matter Transformation journal November 2015
Atmospheric Hydrogen Scavenging: from Enzymes to Ecosystems journal December 2014
Identification of Cellulose-Responsive Bacterial and Fungal Communities in Geographically and Edaphically Different Soils by Using Stable Isotope Probing journal January 2012
Diverse uncultivated bacterial groups from soils of the arid southwestern United States that are present in many geographic regions. journal January 1997
Characterization of the norB Gene, Encoding Nitric Oxide Reductase, in the Nondenitrifying Cyanobacterium Synechocystis sp. Strain PCC6803 journal February 2002
Mechanisms for Accessing Insoluble Fe(III) Oxide during Dissimilatory Fe(III) Reduction by Geothrix fermentans journal May 2002
Empirical and Theoretical Bacterial Diversity in Four Arizona Soils journal June 2002
Nitric Oxide Reductase (norB) Genes from Pure Cultures and Environmental Samples journal June 2003
Seasonal Changes in an Alpine Soil Bacterial Community in the Colorado Rocky Mountains journal May 2004
Abundance and Diversity of Viruses in Six Delaware Soils journal June 2005
Regulation of Nitrite Stress Response in Desulfovibrio vulgaris Hildenborough, a Model Sulfate-Reducing Bacterium journal August 2015
Prokaryotic Nitrate Reduction: Molecular Properties and Functional Distinction among Bacterial Nitrate Reductases journal November 1999
OmcB, a c-Type Polyheme Cytochrome, Involved in Fe(III) Reduction in Geobacter sulfurreducens journal April 2003
Towards a Genome-Based Taxonomy for Prokaryotes journal September 2005
Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). journal January 1996
Insertion Sequences journal September 1998
Genome Sequence of Thermoanaerobaculum aquaticum MP-01T, the First Cultivated Member of Acidobacteria Subdivision 23, Isolated from a Hot Spring journal May 2014
Nitrate reductases: Structure, functions, and effect of stress factors journal October 2007
Acidobacteria in microbial communities of the bog and tundra lichens journal February 2012
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
Complete genome sequence of the thermophilic Acidobacteria, Pyrinomonas methylaliphatogenes type strain K22T journal November 2015
Environmental Adaptation: Genomic Analysis of the Piezotolerant and Psychrotolerant Deep-Sea Iron Reducing Bacterium Shewanella piezotolerans WP3 journal April 2008
Biological Consequences of Ancient Gene Acquisition and Duplication in the Large Genome of Candidatus Solibacter usitatus Ellin6076 journal September 2011
Global Patterns of Abundance, Diversity and Community Structure of the Aminicenantes (Candidate Phylum OP8) journal March 2014
Solexa Ltd journal June 2004
Direct Measurement of Oxygen Profiles and Denitrification Rates in Soil Aggregates1 journal January 1985
Amino Acid Absorption by Arctic Plants: Implications for Plant Nutrition and Nitrogen Cycling journal December 1994
Nutrient requirements and growth physiology of the photoheterotrophic Acidobacterium, Chloracidobacterium thermophilum journal March 2015
The Ecology of Acidobacteria: Moving beyond Genes and Genomes journal May 2016
Mobile genetic elements in the bacterial phylum Acidobacteria journal July 2012
Viral dark matter and virus–host interactions resolved from publicly available microbial genomes journal July 2015
VirSorter: mining viral signal from microbial genomic data journal January 2015