Mobile genetic elements in the bacterial phylum Acidobacteria

Challacombe, Jean; Kuske, Cheryl

doi:10.4161/mge.21943

Mobile genetic elements in the bacterial phylum Acidobacteria

Journal Article · Sun Jul 01 00:00:00 EDT 2012 · Mobile Genetic Elements

DOI:https://doi.org/10.4161/mge.21943· OSTI ID:1629080

Challacombe, Jean ^[1]; Kuske, Cheryl ^[2]

Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); DOE/OSTI
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Analysis of the genome of “Candidatus Solibacter usitatus Ellin6076”, a member of the phylum Acidobacteria, revealed a large number of genes associated with mobile genetic elements. These genes encoded transposases, insertion sequence elements and phage integrases. When the amino acid sequences of the mobile element-associated genes were compared, many of them had high (90–100%) amino acid sequence identities, suggesting that these genes may have recently duplicated and dispersed throughout the genome. Although phage integrase encoding genes were prevalent in the “Can. S. usitatus Ellin6076” genome, no intact prophage regions were found. This suggests that the “Can. S. usitatus Ellin6076” large genome arose by horizontal gene transfer via ancient bacteriophage and/or plasmid-mediated transduction, followed by widespread small-scale gene duplications, resulting in an increased number of paralogs encoding traits that could provide selective metabolic, defensive and regulatory advantages in the soil environment. Here we examine the mobile element repertoire of “Can. S. usitatus Ellin6076” in comparison to other genomes from the Acidobacteria phylum, reviewing published studies and contributing some new analyses. We also discuss the presence and potential roles of mobile elements in members of this phylum that inhabit a variety of environments.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1629080

Journal Information:: Mobile Genetic Elements, Journal Name: Mobile Genetic Elements Journal Issue: 4 Vol. 2; ISSN 2159-256X

Publisher:: Taylor & FrancisCopyright Statement

Country of Publication:: United States

Language:: English

References (63)

Acidobacterium capsulatum gen. nov., sp. nov.: An acidophilic chemoorganotrophic bacterium containing menaquinone from acidic mineral environment Kishimoto, Noriaki; Kosako, Yoshimasa; Tano, Tatsuo Current Microbiology, Vol. 22, Issue 1 https://doi.org/10.1007/bf02106205	journal	January 1991
Phage Integrases: Biology and Applications Groth, Amy C.; Calos, Michele P. Journal of Molecular Biology, Vol. 335, Issue 3 https://doi.org/10.1016/j.jmb.2003.09.082	journal	January 2004
Dynamics of insertion sequence elements during experimental evolution of bacteria Schneider, Dominique; Lenski, Richard E. Research in Microbiology, Vol. 155, Issue 5 https://doi.org/10.1016/j.resmic.2003.12.008	journal	June 2004
Detection of an IS21 insertion sequence in the mexR gene of Pseudomonas aeruginosa increasing Î²-lactam resistance Boutoille, David; Corvec, StÃ©phane; Caroff, Nathalie FEMS Microbiology Letters, Vol. 230, Issue 1 https://doi.org/10.1016/s0378-1097(03)00882-6	journal	January 2004
Causes of Insertion Sequences Abundance in Prokaryotic Genomes Touchon, Marie; Rocha, Eduardo P. C. Molecular Biology and Evolution, Vol. 24, Issue 4 https://doi.org/10.1093/molbev/msm014	journal	January 2007
ISfinder: the reference centre for bacterial insertion sequences Siguier, P. Nucleic Acids Research, Vol. 34, Issue 90001 https://doi.org/10.1093/nar/gkj014	journal	January 2006
The integrated microbial genomes (IMG) system Markowitz, V. M. Nucleic Acids Research, Vol. 34, Issue 90001 https://doi.org/10.1093/nar/gkj024	journal	January 2006
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB Pruesse, E.; Quast, C.; Knittel, K. Nucleic Acids Research, Vol. 35, Issue 21 https://doi.org/10.1093/nar/gkm864	journal	November 2007
Association of newly discovered IS elements with the dichloromethane utilization genes of methylotrophic bacteria Schmid-Appert, M.; Zoller, K.; Traber, H. Microbiology, Vol. 143, Issue 8 https://doi.org/10.1099/00221287-143-8-2557	journal	August 1997
Terriglobus saanensis sp. nov., an acidobacterium isolated from tundra soil Mannisto, M. K.; Rawat, S.; Starovoytov, V. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 61, Issue 8 https://doi.org/10.1099/ijs.0.026005-0	journal	December 2010
Granulicella arctica sp. nov., Granulicella mallensis sp. nov., Granulicella tundricola sp. nov. and Granulicella sapmiensis sp. nov., novel acidobacteria from tundra soil Mannisto, M. K.; Rawat, S.; Starovoytov, V. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue Pt 9 https://doi.org/10.1099/ijs.0.031864-0	journal	November 2011
Edaphobacter modestus gen. nov., sp. nov., and Edaphobacter aggregans sp. nov., acidobacteria isolated from alpine and forest soils Koch, I. H.; Gich, F.; Dunfield, P. F. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 5 https://doi.org/10.1099/ijs.0.65303-0	journal	May 2008
Isolation and characterization of IS 31831, a transposable element from Corynebacterium glutamicum Vertès, Alain A.; Inui, Masayuki; Kobayashi, Miki Molecular Microbiology, Vol. 11, Issue 4 https://doi.org/10.1111/j.1365-2958.1994.tb00351.x	journal	February 1994
Isolation of novel bacteria, including a candidate division, from geothermal soils in New Zealand Stott, Matthew B.; Crowe, Michelle A.; Mountain, Bruce W. Environmental Microbiology, Vol. 10, Issue 8 https://doi.org/10.1111/j.1462-2920.2008.01621.x	journal	August 2008
Phylogenetic analyses of ribosomal DNA-containing bacterioplankton genome fragments from a 4000 m vertical profile in the North Pacific Subtropical Gyre Pham, Vinh D.; Konstantinidis, Konstantinos T.; Palden, Tsultrim Environmental Microbiology, Vol. 10, Issue 9 https://doi.org/10.1111/j.1462-2920.2008.01657.x	journal	September 2008
Complete genome of Candidatus Chloracidobacterium thermophilum, a chlorophyll-based photoheterotroph belonging to the phylum Acidobacteria: Candidatus Chloracidobacterium thermophilum genome Garcia Costas, Amaya M.; Liu, Zhenfeng; Tomsho, Lynn P. Environmental Microbiology, Vol. 14, Issue 1 https://doi.org/10.1111/j.1462-2920.2011.02592.x	journal	September 2011
Comparative genomic and physiological analysis provides insights into the role of Acidobacteria in organic carbon utilization in Arctic tundra soils Rawat, Suman R.; Männistö, Minna K.; Bromberg, Yana FEMS Microbiology Ecology, Vol. 82, Issue 2 https://doi.org/10.1111/j.1574-6941.2012.01381.x	journal	April 2012
Three Genomes from the Phylum Acidobacteria Provide Insight into the Lifestyles of These Microorganisms in Soils Ward, N. L.; Challacombe, J. F.; Janssen, P. H. Applied and Environmental Microbiology, Vol. 75, Issue 7 https://doi.org/10.1128/aem.02294-08	journal	February 2009
Levels of Bacterial Community Diversity in Four Arid Soils Compared by Cultivation and 16S rRNA Gene Cloning Dunbar, John; Takala, Shannon; Barns, Susan M. Applied and Environmental Microbiology, Vol. 65, Issue 4 https://doi.org/10.1128/aem.65.4.1662-1669.1999	journal	April 1999
Wide Distribution and Diversity of Members of the Bacterial Kingdom Acidobacterium in the Environment Barns, Susan M.; Takala, Shannon L.; Kuske, Cheryl R. Applied and Environmental Microbiology, Vol. 65, Issue 4 https://doi.org/10.1128/aem.65.4.1731-1737.1999	journal	April 1999
Laboratory Cultivation of Widespread and Previously Uncultured Soil Bacteria Joseph, S. J.; Hugenholtz, P.; Sangwan, P. Applied and Environmental Microbiology, Vol. 69, Issue 12 https://doi.org/10.1128/aem.69.12.7210-7215.2003	journal	December 2003
Phage Community Dynamics in Hot Springs Breitbart, M.; Wegley, L.; Leeds, S. Applied and Environmental Microbiology, Vol. 70, Issue 3 https://doi.org/10.1128/aem.70.3.1633-1640.2004	journal	March 2004
Effects of Growth Medium, Inoculum Size, and Incubation Time on Culturability and Isolation of Soil Bacteria Davis, K. E. R.; Joseph, S. J.; Janssen, P. H. Applied and Environmental Microbiology, Vol. 71, Issue 2 https://doi.org/10.1128/aem.71.2.826-834.2005	journal	February 2005
Investigation of the Microbial Ecology of Intertidal Hot Springs by Using Diversity Analysis of 16S rRNA and Chitinase Genes Hobel, Cédric F. V.; Marteinsson, Viggó T.; Hreggvidsson, Gudmundur Ó. Applied and Environmental Microbiology, Vol. 71, Issue 5 https://doi.org/10.1128/aem.71.5.2771-2776.2005	journal	May 2005
Identifying the Dominant Soil Bacterial Taxa in Libraries of 16S rRNA and 16S rRNA Genes Janssen, P. H. Applied and Environmental Microbiology, Vol. 72, Issue 3 https://doi.org/10.1128/aem.72.3.1719-1728.2006	journal	March 2006
Identification and Characterization of IS 1411 , a New Insertion Sequence Which Causes Transcriptional Activation of the Phenol Degradation Genes in Pseudomonas putida Kallastu, Aili; Hõrak, Rita; Kivisaar, Maia Journal of Bacteriology, Vol. 180, Issue 20 https://doi.org/10.1128/jb.180.20.5306-5312.1998	journal	October 1998
Excision of IS492 Requires Flanking Target Sequences and Results in Circle Formation in Pseudoalteromonas atlantica Perkins-Balding, Donna; Duval-Valentin, Guy; Glasgow, Anna C. Journal of Bacteriology, Vol. 181, Issue 16 https://doi.org/10.1128/jb.181.16.4937-4948.1999	journal	August 1999
Structural and Functional Characterization of IS 679 and IS 66 -Family Elements Han, Chang-Gyun; Shiga, Yasuyuki; Tobe, Toru Journal of Bacteriology, Vol. 183, Issue 14 https://doi.org/10.1128/jb.183.14.4296-4304.2001	journal	July 2001
Phages and the Evolution of Bacterial Pathogens: from Genomic Rearrangements to Lysogenic Conversion Brussow, H.; Canchaya, C.; Hardt, W. -D. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 3 https://doi.org/10.1128/mmbr.68.3.560-602.2004	journal	September 2004
Mobile Antibiotic Resistance Encoding Elements Promote Their Own Diversity Garriss, Geneviève; Waldor, Matthew K.; Burrus, Vincent PLoS Genetics, Vol. 5, Issue 12 https://doi.org/10.1371/journal.pgen.1000775	journal	December 2009
IS911-mediated Transpositional Recombinationin Vitro Polard, Patrice; Ton-Hoang, Bao; Haren, Laurence Journal of Molecular Biology, Vol. 264, Issue 1 https://doi.org/10.1006/jmbi.1996.0624	journal	November 1996
Acidobacterium capsulatum gen. nov., sp. nov.: An acidophilic chemoorganotrophic bacterium containing menaquinone from acidic mineral environment Kishimoto, Noriaki; Kosako, Yoshimasa; Tano, Tatsuo Current Microbiology, Vol. 22, Issue 1 https://doi.org/10.1007/BF02106205	journal	January 1991
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Detection of an IS21 insertion sequence in the mexR gene of Pseudomonas aeruginosa increasing Î²-lactam resistance Boutoille, David; Corvec, StÃ©phane; Caroff, Nathalie FEMS Microbiology Letters, Vol. 230, Issue 1 https://doi.org/10.1016/S0378-1097(03)00882-6	journal	January 2004
Order and disorder in bacterial genomes Rocha, Eduardo PC Current Opinion in Microbiology, Vol. 7, Issue 5 https://doi.org/10.1016/j.mib.2004.08.006	journal	October 2004
Phages across the biosphere: contrasts of viruses in soil and aquatic environments Srinivasiah, Sharath; Bhavsar, Jaysheel; Thapar, Kanika Research in Microbiology, Vol. 159, Issue 5 https://doi.org/10.1016/j.resmic.2008.04.010	journal	June 2008
Insertion sequence IS256 in canine pyoderma isolates of Staphylococcus pseudintermedius associated with antibiotic resistance Casagrande Proietti, P.; Bietta, A.; Coletti, M. Veterinary Microbiology, Vol. 157, Issue 3-4 https://doi.org/10.1016/j.vetmic.2011.12.028	journal	June 2012
Biodiversity and biogeography of phages in modern stromatolites and thrombolites Desnues, Christelle; Rodriguez-Brito, Beltran; Rayhawk, Steve Nature, Vol. 452, Issue 7185 https://doi.org/10.1038/nature06735	journal	March 2008
Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys: Cultivation of soil bacteria Sait, Michelle; Hugenholtz, Philip; Janssen, Peter H. Environmental Microbiology, Vol. 4, Issue 11 https://doi.org/10.1046/j.1462-2920.2002.00352.x	journal	November 2002
Acanthopleuribacter pedis gen. nov., sp. nov., a marine bacterium isolated from a chiton, and description of Acanthopleuribacteraceae fam. nov., Acanthopleuribacterales ord. nov., Holophagaceae fam. nov., Holophagales ord. nov. and Holophagae classis nov. in the phylum 'Acidobacteria' Fukunaga, Y.; Kurahashi, M.; Yanagi, K. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 11 https://doi.org/10.1099/ijs.0.65589-0	journal	November 2008
Structural and functional analysis of the mini-circle, a transposable element of Streptomyces coelicolor A3(2) Henderson, D. J.; Lydiate, D. J.; Hopwood, D. A. Molecular Microbiology, Vol. 3, Issue 10 https://doi.org/10.1111/j.1365-2958.1989.tb00112.x	journal	October 1989
Comparative analysis of genome fragments of Acidobacteria from deep Mediterranean plankton: Acidobacteria in deep sea plankton Quaiser, Achim; López-García, Purificación; Zivanovic, Yvan Environmental Microbiology, Vol. 10, Issue 10 https://doi.org/10.1111/j.1462-2920.2008.01691.x	journal	July 2008
Candidatus Chloracidobacterium thermophilum: An Aerobic Phototrophic Acidobacterium Bryant, D. A.; Costas, A. M. G.; Maresca, J. A. Science, Vol. 317, Issue 5837 https://doi.org/10.1126/science.1143236	journal	July 2007
Acidobacteria Phylum Sequences in Uranium-Contaminated Subsurface Sediments Greatly Expand the Known Diversity within the Phylum Barns, S. M.; Cain, E. C.; Sommerville, L. Applied and Environmental Microbiology, Vol. 73, Issue 9 https://doi.org/10.1128/AEM.02012-06	journal	March 2007
Isolation and Characterization of Soil Bacteria That Define Terriglobus gen. nov., in the Phylum Acidobacteria Eichorst, S. A.; Breznak, J. A.; Schmidt, T. M. Applied and Environmental Microbiology, Vol. 73, Issue 8 https://doi.org/10.1128/AEM.02140-06	journal	February 2007
Three Genomes from the Phylum Acidobacteria Provide Insight into the Lifestyles of These Microorganisms in Soils Ward, N. L.; Challacombe, J. F.; Janssen, P. H. Applied and Environmental Microbiology, Vol. 75, Issue 7 https://doi.org/10.1128/AEM.02294-08	journal	February 2009
Levels of Bacterial Community Diversity in Four Arid Soils Compared by Cultivation and 16S rRNA Gene Cloning Dunbar, John; Takala, Shannon; Barns, Susan M. Applied and Environmental Microbiology, Vol. 65, Issue 4 https://doi.org/10.1128/AEM.65.4.1662-1669.1999	journal	April 1999
Wide Distribution and Diversity of Members of the Bacterial Kingdom Acidobacterium in the Environment Barns, Susan M.; Takala, Shannon L.; Kuske, Cheryl R. Applied and Environmental Microbiology, Vol. 65, Issue 4 https://doi.org/10.1128/AEM.65.4.1731-1737.1999	journal	April 1999
Phylogenetic Analysis of Bacterial Communities in Mesophilic and Thermophilic Bioreactors Treating Pharmaceutical Wastewater LaPara, Timothy M.; Nakatsu, Cindy H.; Pantea, Lisa Applied and Environmental Microbiology, Vol. 66, Issue 9 https://doi.org/10.1128/AEM.66.9.3951-3959.2000	journal	September 2000
Laboratory Cultivation of Widespread and Previously Uncultured Soil Bacteria Joseph, S. J.; Hugenholtz, P.; Sangwan, P. Applied and Environmental Microbiology, Vol. 69, Issue 12 https://doi.org/10.1128/AEM.69.12.7210-7215.2003	journal	December 2003
Phage Community Dynamics in Hot Springs Breitbart, M.; Wegley, L.; Leeds, S. Applied and Environmental Microbiology, Vol. 70, Issue 3 https://doi.org/10.1128/AEM.70.3.1633-1640.2004	journal	March 2004
Effects of Growth Medium, Inoculum Size, and Incubation Time on Culturability and Isolation of Soil Bacteria Davis, K. E. R.; Joseph, S. J.; Janssen, P. H. Applied and Environmental Microbiology, Vol. 71, Issue 2 https://doi.org/10.1128/AEM.71.2.826-834.2005	journal	February 2005
Investigation of the Microbial Ecology of Intertidal Hot Springs by Using Diversity Analysis of 16S rRNA and Chitinase Genes Hobel, Cédric F. V.; Marteinsson, Viggó T.; Hreggvidsson, Gudmundur Ó. Applied and Environmental Microbiology, Vol. 71, Issue 5 https://doi.org/10.1128/AEM.71.5.2771-2776.2005	journal	May 2005
Identifying the Dominant Soil Bacterial Taxa in Libraries of 16S rRNA and 16S rRNA Genes Janssen, P. H. Applied and Environmental Microbiology, Vol. 72, Issue 3 https://doi.org/10.1128/AEM.72.3.1719-1728.2006	journal	March 2006
Identification and Characterization of IS 1411 , a New Insertion Sequence Which Causes Transcriptional Activation of the Phenol Degradation Genes in Pseudomonas putida Kallastu, Aili; Hõrak, Rita; Kivisaar, Maia Journal of Bacteriology, Vol. 180, Issue 20 https://doi.org/10.1128/JB.180.20.5306-5312.1998	journal	October 1998
Excision of IS492 Requires Flanking Target Sequences and Results in Circle Formation in Pseudoalteromonas atlantica Perkins-Balding, Donna; Duval-Valentin, Guy; Glasgow, Anna C. Journal of Bacteriology, Vol. 181, Issue 16 https://doi.org/10.1128/JB.181.16.4937-4948.1999	journal	August 1999
Structural and Functional Characterization of IS 679 and IS 66 -Family Elements Han, Chang-Gyun; Shiga, Yasuyuki; Tobe, Toru Journal of Bacteriology, Vol. 183, Issue 14 https://doi.org/10.1128/JB.183.14.4296-4304.2001	journal	July 2001
Insertion Sequences Mahillon, Jacques; Chandler, Michael Microbiology and Molecular Biology Reviews, Vol. 62, Issue 3 https://doi.org/10.1128/MMBR.62.3.725-774.1998	journal	September 1998
Phages and the Evolution of Bacterial Pathogens: from Genomic Rearrangements to Lysogenic Conversion Brussow, H.; Canchaya, C.; Hardt, W. -D. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 3 https://doi.org/10.1128/MMBR.68.3.560-602.2004	journal	September 2004
The Diverse and Dynamic Structure of Bacterial Genomes Casjens, Sherwood Annual Review of Genetics, Vol. 32, Issue 1 https://doi.org/10.1146/annurev.genet.32.1.339	journal	December 1998
Insertion sequence content reflects genome plasticity in strains of the root nodule actinobacterium Frankia Bickhart, Derek M.; Gogarten, Johann P.; Lapierre, Pascal BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-468	journal	January 2009
Biological Consequences of Ancient Gene Acquisition and Duplication in the Large Genome of Candidatus Solibacter usitatus Ellin6076 Challacombe, Jean F.; Eichorst, Stephanie A.; Hauser, Loren PLoS ONE, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pone.0024882	journal	September 2011
Acidophilic heterotrophic bacteria isolated from acidic mine drainage, sewage, and soils. Kishimoto, Noriaki; Tano, Tatsuo The Journal of General and Applied Microbiology, Vol. 33, Issue 1 https://doi.org/10.2323/jgam.33.11	journal	January 1987

Cited By (4)

Bipartite Network Analysis of Gene Sharings in the Microbial World Corel, Eduardo; Méheust, Raphaël; Watson, Andrew K. Molecular Biology and Evolution, Vol. 35, Issue 4 https://doi.org/10.1093/molbev/msy001	journal	January 2018
Ruminal metagenomic analyses of goat data reveals potential functional microbiota by supplementation with essential oil-cobalt complexes Lei, Zhaomin; Zhang, Ke; Li, Chao BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1400-3	journal	February 2019
Characterization of bacterial communities associated with the pinewood nematode insect vector Monochamus alternatus Hope and the host tree Pinus massoniana Guo, Yajie; Lin, Qiannan; Chen, Lyuyi BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-6718-6	journal	May 2020
Characterization of bacterial communities associated with the pinewood nematode insect vector Monochamus alternatus Hope and the host tree Pinus massoniana Guo, Yajie; Lin, Qiannan; Chen, Ivyi BMC Genomics https://doi.org/10.21203/rs.2.14055/v3	posted_content	May 2020

Similar Records

Biological Consequences of Ancient Gene Acquisition and Duplication in the Large Genome of Candidatus Solibacter usitatus Ellin6076

Journal Article · Fri Dec 31 23:00:00 EST 2010 · PLoS ONE · OSTI ID:1024790

Biological consequences of ancient gene acquisition and duplication in the large genome soil bacterium, ""solibacter usitatus"" strain Ellin6076

Journal Article · Wed Dec 31 23:00:00 EST 2008 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:972053

Identification of Mobile Elements and Pseudogenes in the Shewanella oneidensis MR-1 Genome

Journal Article · Thu May 01 00:00:00 EDT 2008 · Applied and Environmental Microbiology, 74(10):3257-3265 · OSTI ID:937378

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
acidobacteria
environment
genome
horizontal gene transfer
insertion sequence
phage integrase
transposase

Mobile genetic elements in the bacterial phylum Acidobacteria

Citation Formats

References (63)

Cited By (4)

Similar Records

Related Subjects