The Mosaic Genome of Anaeromyxobacter dehalogenans Strain 2CP-C Suggests an Aerobic Common Ancestor to the Delta-Proteobacteria

Thomas, Sara H.; Wagner, Ryan D.; Arakaki, Adrian K.; Skolnick, Jeffrey; Kirby, John R.; Shimkets, Lawrence J.; Sanford, Robert A.; Löffler, Frank E.

doi:10.1371/journal.pone.0002103

Title: **The Mosaic Genome of Anaeromyxobacter dehalogenans Strain 2CP-C Suggests an Aerobic Common Ancestor to the Delta-Proteobacteria**

Journal Article · Wed May 07 00:00:00 EDT 2008 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0002103· OSTI ID:1627347

Thomas, Sara H. ^[1]; Wagner, Ryan D. ^[1]; Arakaki, Adrian K. ^[1]; Skolnick, Jeffrey ^[1]; Kirby, John R. ^[2]; Shimkets, Lawrence J. ^[3]; Sanford, Robert A. ^[4]; Löffler, Frank E. ^[1]

Georgia Institute of Technology, Atlanta, GA (United States)
University of Iowa, Iowa City, IA (United States)
University of Georgia, Athens, GA (United States)
University of Illinois at Urbana-Champaign, IL (United States)

Anaeromyxobacter dehalogenans strain 2CP-C is a versaphilic delta-Proteobacterium distributed throughout many diverse soil and sediment environments. 16S rRNA gene phylogenetic analysis groups A. dehalogenans together with the myxobacteria, which have distinguishing characteristics including strictly aerobic metabolism, sporulation, fruiting body formation, and surface motility. Analysis of the 5.01 Mb strain 2CP-C genome substantiated that this organism is a myxobacterium but shares genotypic traits with the anaerobic majority of the delta-Proteobacteria (i.e., the Desulfuromonadales). Reflective of its respiratory versatility, strain 2CP-C possesses 68 genes coding for putative c-type cytochromes, including one gene with 40 heme binding motifs. Consistent with its relatedness to the myxobacteria, surface motility was observed in strain 2CP-C and multiple types of motility genes are present, including 28 genes for gliding, adventurous (A-) motility and 17 genes for type IV pilus-based motility (i.e., social (S-) motility) that all have homologs in Myxococcus xanthus. Although A. dehalogenans shares many metabolic traits with the anaerobic majority of the delta-Proteobacteria, strain 2CP-C grows under microaerophilic conditions and possesses detoxification systems for reactive oxygen species. Accordingly, two gene clusters coding for NADH dehydrogenase subunits and two cytochrome oxidase gene clusters in strain 2CP-C are similar to those in M. xanthus. Remarkably, strain 2CP-C possesses a third NADH dehydrogenase gene cluster and a cytochrome cbb₃ oxidase gene cluster, apparently acquired through ancient horizontal gene transfer from a strictly anaerobic green sulfur bacterium. The mosaic nature of the A. dehalogenans strain 2CP-C genome suggests that the metabolically versatile, anaerobic members of the delta-Proteobacteria may have descended from aerobic ancestors with complex lifestyles.

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Research Organization:: Georgia Institute of Technology, Atlanta, GA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)

Grant/Contract Number:: AC02-05CH11231; DGE 0114400; 0338261

OSTI ID:: 1627347

Journal Information:: PLoS ONE, Vol. 3, Issue 5; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Effects of Water-Saving Irrigation on Emissions of Greenhouse Gases and Prokaryotic Communities in Rice Paddy Soil Ahn, Jae-Hyung; Choi, Min-Young; Kim, Byung-Yong Microbial Ecology, Vol. 68, Issue 2 https://doi.org/10.1007/s00248-014-0371-z	journal	March 2014
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An integrative overview of genomic, transcriptomic and proteomic analyses in organohalide respiration research Türkowsky, Dominique; Jehmlich, Nico; Diekert, Gabriele FEMS Microbiology Ecology, Vol. 94, Issue 3 https://doi.org/10.1093/femsec/fiy013	journal	January 2018
The little bacteria that can - diversity, genomics and ecophysiology of ‘Dehalococcoides’ spp. in contaminated environments: Ecophysiology of ‘Dehalococcoides’ spp. Taş, Neslihan; Van Eekert, Miriam H. A.; De Vos, Willem M. Microbial Biotechnology, Vol. 3, Issue 4 https://doi.org/10.1111/j.1751-7915.2009.00147.x	journal	September 2009
Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases Hug, Laura A.; Maphosa, Farai; Leys, David Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1616 https://doi.org/10.1098/rstb.2012.0322	journal	April 2013
Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic complexes Adam, Panagiotis S.; Borrel, Guillaume; Gribaldo, Simonetta Proceedings of the National Academy of Sciences, Vol. 115, Issue 6 https://doi.org/10.1073/pnas.1716667115	journal	January 2018
The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer Shi, Liang; Richardson, David J.; Wang, Zheming Environmental Microbiology Reports, Vol. 1, Issue 4 https://doi.org/10.1111/j.1758-2229.2009.00035.x	journal	August 2009
Genome-wide analysis of myxobacterial two-component systems: genome relatedness and evolutionary changes Whitworth, David E. BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-2018-y	journal	October 2015
In silico characterization of a novel putative aerotaxis chemosensory system in the myxobacterium, Corallococcus coralloides Sharma, Gaurav; Parales, Rebecca; Singer, Mitchell BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-5151-6	journal	October 2018
Genomic determinants of organohalide-respiration in Geobacter lovleyi, an unusual member of the Geobacteraceae Wagner, Darlene D.; Hug, Laura A.; Hatt, Janet K. BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-200	journal	January 2012
Suppressor mutations reveal an NtrC-like response regulator, NmpR, for modulation of Type-IV Pili-dependent motility in Myxococcus xanthus Bretl, Daniel J.; Ladd, Kayla M.; Atkinson, Samantha N. PLOS Genetics, Vol. 14, Issue 10 https://doi.org/10.1371/journal.pgen.1007714	journal	October 2018
BAX inhibitor-1 enhances cancer metastasis by altering glucose metabolism and activating the sodium-hydrogen exchanger: the alteration of mitochondrial function Lee, G-H; Yan, C.; Shin, S-J Oncogene, Vol. 29, Issue 14 https://doi.org/10.1038/onc.2009.491	journal	February 2010
Culture-independent study of bacterial communities in tropical river sediment Thoetkiattikul, Honglada; Mhuantong, Wuttichai; Pinyakong, Onruthai Taylor & Francis https://doi.org/10.6084/m9.figshare.3860226.v1	text	January 2016
A selective force favoring increased G+C content in bacterial genes Raghavan, R.; Kelkar, Y. D.; Ochman, H. Proceedings of the National Academy of Sciences, Vol. 109, Issue 36 https://doi.org/10.1073/pnas.1205683109	journal	August 2012
Comparative c-type cytochrome expression analysis in Shewanella oneidensis strain MR-1 and Anaeromyxobacter dehalogenans strain 2CP-C grown with soluble and insoluble oxidized metal electron acceptors Nissen, Silke; Liu, Xiaoxin; Chourey, Karuna Biochemical Society Transactions, Vol. 40, Issue 6 https://doi.org/10.1042/bst20120182	journal	November 2012
Unravelling the Complete Genome of Archangium gephyra DSM 2261T and Evolutionary Insights into Myxobacterial Chitinases Sharma, Gaurav; Subramanian, Srikrishna Genome Biology and Evolution, Vol. 9, Issue 5 https://doi.org/10.1093/gbe/evx066	journal	May 2017
The Evolution of Bacterial Genome Architecture Bobay, Louis-Marie; Ochman, Howard Frontiers in Genetics, Vol. 8 https://doi.org/10.3389/fgene.2017.00072	journal	May 2017
Comparison of Antibiotic Resistance Mechanisms in Antibiotic-Producing and Pathogenic Bacteria Ogawara, Hiroshi Molecules, Vol. 24, Issue 19 https://doi.org/10.3390/molecules24193430	journal	September 2019
The regulatory action of the myxobacterial CarD/CarG complex: a bacterial enhanceosome? Elías-Arnanz, Montserrat; Padmanabhan, S.; Murillo, Francisco J. FEMS Microbiology Reviews, Vol. 34, Issue 5 https://doi.org/10.1111/j.1574-6976.2010.00235.x	journal	September 2010
Culture-independent study of bacterial communities in tropical river sediment Thoetkiattikul, Honglada; Mhuantong, Wuttichai; Pinyakong, Onruthai Bioscience, Biotechnology, and Biochemistry, Vol. 81, Issue 1 https://doi.org/10.1080/09168451.2016.1234927	journal	January 2017
The Multiple Evolutionary Histories of Dioxygen Reductases: Implications for the Origin and Evolution of Aerobic Respiration Brochier-Armanet, C.; Talla, E.; Gribaldo, S. Molecular Biology and Evolution, Vol. 26, Issue 2 https://doi.org/10.1093/molbev/msn246	journal	October 2008
Mutator genomes decay, despite sustained fitness gains, in a long-term experiment with bacteria Couce, Alejandro; Caudwell, Larissa Viraphong; Feinauer, Christoph Proceedings of the National Academy of Sciences, Vol. 114, Issue 43 https://doi.org/10.1073/pnas.1705887114	journal	October 2017
Extraordinary expansion of a Sorangium cellulosum genome from an alkaline milieu Han, Kui; Li, Zhi-feng; Peng, Ran Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep02101	journal	July 2013
Diversity and Evolution of Myxobacterial Type IV Pilus Systems Sharma, Gaurav; Burrows, Lori L.; Singer, Mitchell Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01630	journal	July 2018
The energy-conserving electron transfer system used by D esulfovibrio alaskensis strain G20 during pyruvate fermentation involves reduction of endogenously formed fumarate and cytoplasmic and membrane-bound complexes, Hdr-Flox and Rnf : Fermentative monoculture/coculture growth of G20 on pyruvate Meyer, Birte; Kuehl, Jennifer V.; Price, Morgan N. Environmental Microbiology, Vol. 16, Issue 11 https://doi.org/10.1111/1462-2920.12405	journal	March 2014
MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm Wu, Yu-Wei; Tang, Yung-Hsu; Tringe, Susannah G. Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-26	journal	August 2014
Endospore-enriched sequencing approach reveals unprecedented diversity of Firmicutes in sediments: Endospore-forming enrichment Wunderlin, Tina; Junier, Thomas; Roussel-Delif, Ludovic Environmental Microbiology Reports, Vol. 6, Issue 6 https://doi.org/10.1111/1758-2229.12179	journal	June 2014
Single-Cell Genomics Reveals a Diverse Metabolic Potential of Uncultivated Desulfatiglans-Related Deltaproteobacteria Widely Distributed in Marine Sediment Jochum, Lara M.; Schreiber, Lars; Marshall, Ian P. G. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02038	journal	September 2018
Exemplar Abstract for Anaeromyxobacter dehalogenans Sanford et al. 2002. Parker, Charles Thomas; Taylor, Dorothea; Garrity, George M. https://doi.org/10.1601/ex.15190	dataset	January 2013
The Genome of the Fungal-Interactive Soil Bacterium Burkholderia terrae BS001—A Plethora of Outstanding Interactive Capabilities Unveiled Haq, Irshad Ul; Graupner, Katharina; Nazir, Rashid Genome Biology and Evolution, Vol. 6, Issue 7 https://doi.org/10.1093/gbe/evu126	journal	June 2014
Rapid identification of high-confidence taxonomic assignments for metagenomic data MacDonald, Norman J.; Parks, Donovan H.; Beiko, Robert G. Nucleic Acids Research, Vol. 40, Issue 14 https://doi.org/10.1093/nar/gks335	journal	April 2012
A Highly Polymorphic Receptor Governs Many Distinct Self-Recognition Types within the Myxococcales Order Cao, Pengbo; Wei, Xueming; Awal, Ram Prasad mBio, Vol. 10, Issue 1 https://doi.org/10.1128/mbio.02751-18	journal	February 2019
Effects of site-directed mutagenesis of mglA on motility and swarming of Myxococcus xanthus Fremgen, Sarah A.; Burke, Neal S.; Hartzell, Patricia L. BMC Microbiology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2180-10-295	journal	November 2010
Comparing the Similarity of Different Groups of Bacteria to the Human Proteome Trost, Brett; Pajon, Rolando; Jayaprakash, Teenus PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0034007	journal	April 2012
A New Comparative-Genomics Approach for Defining Phenotype-Specific Indicators Reveals Specific Genetic Markers in Predatory Bacteria Pasternak, Zohar; Ben Sasson, Tom; Cohen, Yossi PLOS ONE, Vol. 10, Issue 11 https://doi.org/10.1371/journal.pone.0142933	journal	November 2015
Effects of Genic Base Composition on Growth Rate in G+C-rich Genomes Kelkar, Yogeshwar D.; Phillips, Daniel S.; Ochman, Howard G3 Genes\|Genomes\|Genetics, Vol. 5, Issue 6 https://doi.org/10.1534/g3.115.016824	journal	June 2015
A Comparative Genomic Analysis of Energy Metabolism in Sulfate Reducing Bacteria and Archaea Pereira, Inês A. Cardoso; Ramos, Ana Raquel; Grein, Fabian Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00069	journal	January 2011
Evolution of genome base composition and genome size in bacteria Nishida, Hiromi Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00420	journal	January 2012
High frequency of phylogenetically diverse reductive dehalogenase-homologous genes in deep subseafloor sedimentary metagenomes Kawai, Mikihiko; Futagami, Taiki; Toyoda, Atsushi Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00080	journal	January 2014
Corrigendum: Diversity of reductive dehalogenase genes from environmental samples and enrichment cultures identified with degenerate primer PCR screens Hug, Laura A.; Edwards, Elizabeth A. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00030	journal	February 2015
Complete genome sequence of Haliangium ochraceum type strain (SMP-2T) Ivanova, Natalia; Daum, Chris; Lang, Elke Standards in Genomic Sciences, Vol. 2, Issue 1 https://doi.org/10.4056/sigs.69.1277	journal	January 2010
Local genic base composition impacts protein production and cellular fitness Quandt, Erik M.; Traverse, Charles C.; Ochman, Howard PeerJ, Vol. 6 https://doi.org/10.7717/peerj.4286	journal	January 2018
Exemplar Abstract for Anaeromyxobacter dehalogenans Sanford et al. 2002. Parker, Charles Thomas; Mannor, Kara; Garrity, George M. https://doi.org/10.1601/ex.3705	dataset	January 2013

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genomics
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Title: The Mosaic Genome of Anaeromyxobacter dehalogenans Strain 2CP-C Suggests an Aerobic Common Ancestor to the Delta-Proteobacteria

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Title: **The Mosaic Genome of Anaeromyxobacter dehalogenans Strain 2CP-C Suggests an Aerobic Common Ancestor to the Delta-Proteobacteria**