How Clonal Is Clonal? Genome Plasticity across Multicellular Segments of a “Candidatus Marithrix sp.” Filament from Sulfidic, Briny Seafloor Sediments in the Gulf of Mexico

Salman-Carvalho, Verena; Fadeev, Eduard; Joye, Samantha B.; Teske, Andreas

doi:10.3389/fmicb.2016.01173

Title: How Clonal Is Clonal? Genome Plasticity across Multicellular Segments of a “Candidatus Marithrix sp.” Filament from Sulfidic, Briny Seafloor Sediments in the Gulf of Mexico

Journal Article · Wed Aug 03 00:00:00 EDT 2016 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2016.01173· OSTI ID:1628147

Salman-Carvalho, Verena ^[1]; Fadeev, Eduard ^[1]; Joye, Samantha B. ^[2]; Teske, Andreas ^[3]

Max Planck Inst. for Marine Microbiology, Bremen (Germany). HGF MPG Joint Research Group for Deep-Sea Ecology and Technology
Univ. of Georgia, Athens, GA (United States). Dept. of Marine Sciences
Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Marine Sciences

“Candidatus Marithrix” is a recently described lineage within the group of large sulfur bacteria (Beggiatoaceae, Gammaproteobacteria). This genus of bacteria comprises vacuolated, attached-living filaments that inhabit the sediment surface around vent and seep sites in the marine environment. A single filament is ca. 100 µm in diameter, several millimeters long, and consists of hundreds of clonal cells, which are considered highly polyploid. Based on these characteristics, “Candidatus Marithrix” was used as a model organism for the assessment of genomic plasticity along segments of a single filament using next generation sequencing to possibly identify hotspots of microevolution. Using six consecutive segments of a single filament sampled from a mud volcano in the Gulf of Mexico, we recovered ca. 90% of the “Candidatus Marithrix” genome in each segment. There was a high level of genome conservation along the filament with average nucleotide identities between 99.98 and 100%. Different approaches to assemble all reads into a complete consensus genome could not fill the gaps. Each of the six segment datasets encoded merely a few hundred unique nucleotides and 5 or less unique genes—the residual content was redundant in all datasets. Besides the overall high genomic identity, we identified a similar number of single nucleotide polymorphisms (SNPs) between the clonal segments, which are comparable to numbers reported for other clonal organisms. An increase of SNPs with greater distance of filament segments was not observed. The polyploidy of the cells was apparent when analyzing the heterogeneity of reads within a segment. Here, a strong increase in single nucleotide variants, or “intrasegmental sequence heterogeneity” (ISH) events, was observed. These sites may represent hotspots for genome plasticity, and possibly microevolution, since two thirds of these variants were not co-localized across the genome copies of the multicellular filament.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1628147

Journal Information:: Frontiers in Microbiology, Vol. 7; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (86)

Evolution of MRSA During Hospital Transmission and Intercontinental Spread Harris, S. R.; Feil, E. J.; Holden, M. T. G. Science, Vol. 327, Issue 5964 https://doi.org/10.1126/science.1182395	journal	January 2010
Bacterial Sulfur Globules: Occurrence, Structure and Metabolism Dahl, Christiane; Prange, Alexander Inclusions in Prokaryotes https://doi.org/10.1007/3-540-33774-1_2	book	January 2006
QUAST: quality assessment tool for genome assemblies Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay Bioinformatics, Vol. 29, Issue 8 https://doi.org/10.1093/bioinformatics/btt086	journal	February 2013
Dense Populations of a Giant Sulfur Bacterium in Namibian Shelf Sediments Schulz, H. N. Science, Vol. 284, Issue 5413 https://doi.org/10.1126/science.284.5413.493	journal	April 1999
The Binning of Metagenomic Contigs for Microbial Physiology of Mixed Cultures Strous, Marc; Kraft, Beate; Bisdorf, Regina Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00410	journal	January 2012
Vacuolated Beggiatoa-like filaments from different hypersaline environments form a novel genus: Beggiatoa-like filaments form a novel genus Hinck, Susanne; Mußmann, Marc; Salman, Verena Environmental Microbiology, Vol. 13, Issue 12 https://doi.org/10.1111/j.1462-2920.2011.02513.x	journal	June 2011
The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps Joye, Samantha B.; Boetius, Antje; Orcutt, Beth N. Chemical Geology, Vol. 205, Issue 3-4 https://doi.org/10.1016/j.chemgeo.2003.12.019	journal	May 2004
Sulfide oxidation, nitrate respiration, carbon acquisition, and electron transport pathways suggested by the draft genome of a single orange Guaymas Basin Beggiatoa (Cand. Maribeggiatoa) sp. filament MacGregor, Barbara J.; Biddle, Jennifer F.; Harbort, Christopher Marine Genomics, Vol. 11 https://doi.org/10.1016/j.margen.2013.08.001	journal	September 2013
Large Sulfur Bacteria and the Formation of Phosphorite Schulz, H. N. Science, Vol. 307, Issue 5708 https://doi.org/10.1126/science.1103096	journal	January 2005
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data Kearse, M.; Moir, R.; Wilson, A. Bioinformatics, Vol. 28, Issue 12 https://doi.org/10.1093/bioinformatics/bts199	journal	April 2012
Mats of psychrophilic thiotrophic bacteria associated with cold seeps of the Barents Sea, supplement to: Grünke, Stefanie; Lichtschlag, Anna; de Beer, Dirk; Felden, Janine; Salman, Verena; Ramette, Alban; Schulz-Vogt, Heide N; Boetius, Antje (2012): Mats of psychrophilic thiotrophic bacteria associated with cold seeps of the Barents Sea. Biogeosciences, 9(8), 2947-2960 Grünke, Stefanie; Lichtschlag, Anna; de Beer, Dirk PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.786576	collection	January 2012
Biogeochemical signatures and microbial activity of different cold seep habitats along the Gulf of Mexico lower slope B., Joye, S.; W., Bowles, M.; A., Samarkin, V. Elsevier Science https://doi.org/10.5451/unibas-ep21224	text	January 2010
Compartmentalization of Gene Expression during Bacillus subtilis Spore Formation Hilbert, D. W.; Piggot, P. J. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 2 https://doi.org/10.1128/MMBR.68.2.234-262.2004	journal	June 2004
Vacuolate-attached filaments: highly productive Ridgeia piscesae epibionts at the Juan de Fuca hydrothermal vents Kalanetra, Karen M.; Nelson, Douglas C. Marine Biology, Vol. 157, Issue 4 https://doi.org/10.1007/s00227-009-1362-3	journal	December 2009
Assessment of whole genome amplification-induced bias through high-throughput, massively parallel whole genome sequencing Pinard, Robert; de Winter, Alex; Sarkis, Gary J. BMC Genomics, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2164-7-216	journal	August 2006
How often do duplicated genes evolve new functions? Walsh, J. B. Genetics, Vol. 139, Issue 1 https://doi.org/10.1093/genetics/139.1.421	journal	January 1995
Big Bacteria Schulz, Heide N.; Jørgensen, Bo Barker Annual Review of Microbiology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev.micro.55.1.105	journal	October 2001
BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons Alikhan, Nabil-Fareed; Petty, Nicola K.; Ben Zakour, Nouri L. BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-402	journal	August 2011
DNA Replication and Genomic Architecture of Very Large Bacteria Angert, Esther R. Annual Review of Microbiology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-micro-090110-102827	journal	October 2012
Whole-genome multiple displacement amplification from single cells Spits, Claudia; Le Caignec, Cédric; De Rycke, Martine Nature Protocols, Vol. 1, Issue 4 https://doi.org/10.1038/nprot.2006.326	journal	November 2006
Spatial Structure and Activity of Sedimentary Microbial Communities Underlying a Beggiatoa spp. Mat in a Gulf of Mexico Hydrocarbon Seep G., Lloyd, Karen; F., Biddle, Jennifer; B., Albert, Daniel The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/9tra-t647	text	January 2010
Biogeochemical signatures and microbial activity of different cold-seep habitats along the Gulf of Mexico deep slope Joye, Samantha B.; Bowles, Marshall W.; Samarkin, Vladimir A. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 57, Issue 21-23 https://doi.org/10.1016/j.dsr2.2010.06.001	journal	November 2010
The Genera Leucothrix and Thiothrix Harold, Ruth; Stanier, R. Y. Bacteriological Reviews, Vol. 19, Issue 2 https://doi.org/10.1128/br.19.2.49-64.1955	journal	June 1955
Phylogenetic and morphologic complexity of giant sulphur bacteria Salman, Verena; Bailey, Jake V.; Teske, Andreas Antonie van Leeuwenhoek, Vol. 104, Issue 2 https://doi.org/10.1007/s10482-013-9952-y	journal	June 2013
Single-Cell (Meta-)Genomics of a Dimorphic Candidatus Thiomargarita nelsonii Reveals Genomic Plasticity Flood, Beverly E.; Fliss, Palmer; Jones, Daniel S. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00603	journal	May 2016
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
In situ phenotypic heterogeneity among single cells of the filamentous bacterium Candidatus Microthrix parvicella Sheik, Abdul R.; Muller, Emilie EL; Audinot, Jean-Nicolas The ISME Journal, Vol. 10, Issue 5 https://doi.org/10.1038/ismej.2015.181	journal	October 2015
Chemoautotrophic growth of a marine Beggiatoa in sulfide-gradient cultures Nelson, Douglas C.; Jannasch, Holger W. Archives of Microbiology, Vol. 136, Issue 4 https://doi.org/10.1007/bf00425214	journal	December 1983
Single-cell Sequencing of Thiomargarita Reveals Genomic Flexibility for Adaptation to Dynamic Redox Conditions Winkel, Matthias; Salman-Carvalho, Verena; Woyke, Tanja Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00964	journal	June 2016
Polyploidy and polyteny in the gigantic eubacterium Epulopiscium fishelsoni Bresler, V.; Fishelson, L. Marine Biology, Vol. 143, Issue 1 https://doi.org/10.1007/s00227-003-1055-2	journal	July 2003
In situ fluxes and zonation of microbial activity in surface sediments of the Håkon Mosby Mud Volcano de Beer, Dirk; Sauter, Eberhard; Niemann, Helge Limnology and Oceanography, Vol. 51, Issue 3 https://doi.org/10.4319/lo.2006.51.3.1315	journal	May 2006
The energetics of genome complexity Lane, Nick; Martin, William Nature, Vol. 467, Issue 7318 https://doi.org/10.1038/nature09486	journal	October 2010
Calcite-accumulating large sulfur bacteria of the genus Achromatium in Sippewissett Salt Marsh Salman, Verena; Yang, Tingting; Berben, Tom The ISME Journal, Vol. 9, Issue 11 https://doi.org/10.1038/ismej.2015.62	journal	April 2015
Rapid and precise δ ¹³ C measurement of dissolved inorganic carbon in natural waters using liquid chromatography coupled to an isotope-ratio mass spectrometer: Rapid isotopic analysis of DIC Brandes, Jay A. Limnology and Oceanography: Methods, Vol. 7, Issue 11 https://doi.org/10.4319/lom.2009.7.730	journal	October 2009
MetAMOS: a modular and open source metagenomic assembly and analysis pipeline Treangen, Todd J.; Koren, Sergey; Sommer, Daniel D. Genome Biology, Vol. 14, Issue 1 https://doi.org/10.1186/gb-2013-14-1-r2	journal	January 2013
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008
Dimorphism in methane seep-dwelling ecotypes of the largest known bacteria Bailey, Jake V.; Salman, Verena; Rouse, Gregory W. The ISME Journal, Vol. 5, Issue 12 https://doi.org/10.1038/ismej.2011.66	journal	June 2011
Compartmentalization and organelle formation in bacteria Cornejo, Elias; Abreu, Nicole; Komeili, Arash Current Opinion in Cell Biology, Vol. 26 https://doi.org/10.1016/j.ceb.2013.12.007	journal	February 2014
Niche differentiation among mat-forming, sulfide-oxidizing bacteria at cold seeps of the Nile Deep Sea Fan (Eastern Mediterranean Sea): Niche differentiation among sulfide oxidizers GrÜNke, S.; Felden, J.; Lichtschlag, A. Geobiology, Vol. 9, Issue 4 https://doi.org/10.1111/j.1472-4669.2011.00281.x	journal	April 2011
Mobile Elements in a Single-Filament Orange Guaymas Basin Beggiatoa (“Candidatus Maribeggiatoa”) sp. Draft Genome: Evidence for Genetic Exchange with Cyanobacteria J., MacGregor, Barbara; F., Biddle, Jennifer; Andreas, Teske, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/3g5f-3y06	text	January 2013
Role of bacterial mats in oxygen-deficient marine basins and coastal upwelling regimes: Preliminary report Williams, Loretta Ann; Reimers, Clare Geology, Vol. 11, Issue 5 https://doi.org/10.1130/0091-7613(1983)11<267:ROBMIO>2.0.CO;2	journal	January 1983
Single-cell genomic sequencing using Multiple Displacement Amplification Lasken, Roger S. Current Opinion in Microbiology, Vol. 10, Issue 5 https://doi.org/10.1016/j.mib.2007.08.005	journal	October 2007
Extreme polyploidy in a large bacterium Mendell, J. E.; Clements, K. D.; Choat, J. H. Proceedings of the National Academy of Sciences, Vol. 105, Issue 18 https://doi.org/10.1073/pnas.0707522105	journal	April 2008
Ultrastructure of Thiothrix spp. and “Type 021N” Bacteria Williams, Terry M.; Unz, Richard F.; Doman, J. Thomas Applied and Environmental Microbiology, Vol. 53, Issue 7 https://doi.org/10.1128/aem.53.7.1560-1570.1987	journal	July 1987
The Evolutionary Consequences of Polyploidy Otto, Sarah P. Cell, Vol. 131, Issue 3 https://doi.org/10.1016/j.cell.2007.10.022	journal	November 2007
ARB: a software environment for sequence data Ludwig, W. Nucleic Acids Research, Vol. 32, Issue 4 https://doi.org/10.1093/nar/gkh293	journal	February 2004
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
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
DNA damage and repair Friedberg, Errol C. Nature, Vol. 421, Issue 6921 https://doi.org/10.1038/nature01408	journal	January 2003
Why Close a Bacterial Genome? The Plasmid of Alteromonas Macleodii HOT1A3 is a Vector for Inter-Specific Transfer of a Flexible Genomic Island Fadeev, Eduard; De Pascale, Fabio; Vezzi, Alessandro Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00248	journal	March 2016
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Multiple self-splicing introns in the 16S rRNA genes of giant sulfur bacteria Salman, V.; Amann, R.; Shub, D. A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 11 https://doi.org/10.1073/pnas.1120192109	journal	February 2012
Multiple displacement amplification compromises quantitative analysis of metagenomes Yilmaz, Suzan; Allgaier, Martin; Hugenholtz, Philip Nature Methods, Vol. 7, Issue 12 https://doi.org/10.1038/nmeth1210-943	journal	November 2010
Patterns and variability in geochemical signatures and microbial activity within and between diverse cold seep habitats along the lower continental slope, Northern Gulf of Mexico Bowles, Marshall; Hunter, Kimberley S.; Samarkin, Vladimir Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 129 https://doi.org/10.1016/j.dsr2.2016.02.011	journal	July 2016
Unusual polyphosphate inclusions observed in a marine Beggiatoa strain Brock, Jörg; Rhiel, Erhard; Beutler, Martin Antonie van Leeuwenhoek, Vol. 101, Issue 2 https://doi.org/10.1007/s10482-011-9640-8	journal	September 2011
Massive natural occurrence of unusually large bacteria (Beggiatoa sp.) at a hydrothermal deep-sea vent site Jannasch, Holger W.; Nelson, Douglas C.; Wirsen, Carl O. Nature, Vol. 342, Issue 6251 https://doi.org/10.1038/342834a0	journal	December 1989
Characterization of a deep-sea microbial mat from an active cold seep at the Milano mud volcano in the Eastern Mediterranean Sea Heijs, Sander K.; Sinninghe DamstÃ©, Jaap S.; Forney, Larry J. FEMS Microbiology Ecology, Vol. 54, Issue 1 https://doi.org/10.1016/j.femsec.2005.02.007	journal	September 2005
High Nitrate Concentrations in Vacuolate, Autotrophic Marine Beggiatoa spp. McHatton, S. C.; Barry, J. P.; Jannasch, H. W. Applied and environmental microbiology, Vol. 62, Issue 3 https://doi.org/10.1128/aem.62.3.954-958.1996	journal	January 1996
Elimination of deleterious mutations in plastid genomes by gene conversion Khakhlova, Olga; Bock, Ralph The Plant Journal, Vol. 46, Issue 1 https://doi.org/10.1111/j.1365-313X.2006.02673.x	journal	April 2006
Characterization of Large, Autotrophic Beggiatoa spp. Abundant at Hydrothermal Vents of the Guaymas Basin † Nelson, Douglas C.; Wirsen, Carl O.; Jannasch, Holger W. Applied and Environmental Microbiology, Vol. 55, Issue 11 https://doi.org/10.1128/aem.55.11.2909-2917.1989	journal	January 1989
Spatial Structure and Activity of Sedimentary Microbial Communities Underlying a Beggiatoa spp. Mat in a Gulf of Mexico Hydrocarbon Seep Lloyd, Karen G.; Albert, Daniel B.; Biddle, Jennifer F. PLoS ONE, Vol. 5, Issue 1 https://doi.org/10.1371/journal.pone.0008738	journal	January 2010
RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes Brettin, Thomas; Davis, James J.; Disz, Terry Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep08365	journal	February 2015
Insights into the Genome of Large Sulfur Bacteria Revealed by Analysis of Single Filaments Mußmann, Marc; Hu, Fen Z.; Richter, Michael PLoS Biology, Vol. 5, Issue 9 https://doi.org/10.1371/journal.pbio.0050230	journal	August 2007
Genomic DNA Amplification from a Single Bacterium Raghunathan, A.; Ferguson, H. R.; Bornarth, C. J. Applied and Environmental Microbiology, Vol. 71, Issue 6 https://doi.org/10.1128/AEM.71.6.3342-3347.2005	journal	June 2005
High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi Holt, Kathryn E.; Parkhill, Julian; Mazzoni, Camila J. Nature Genetics, Vol. 40, Issue 8 https://doi.org/10.1038/ng.195	journal	July 2008
Salinimonas marina sp. nov. Isolated from Jeju Island Marine Sediment Kim, Minji; Lee, Ki-Eun; Cha, In-Tae Current Microbiology, Vol. 78, Issue 8 https://doi.org/10.1007/s00284-021-02576-9	journal	June 2021
Mats of psychrophilic thiotrophic bacteria associated with cold seeps of the Barents Sea Grünke, S.; Lichtschlag, A.; de Beer, D. Biogeosciences, Vol. 9, Issue 8 https://doi.org/10.5194/bg-9-2947-2012	journal	January 2012
Filamentous sulfide-oxidizing bacteria at hydrocarbon seeps of the Gulf of Mexico Larkin, John M.; Henk, Margaret C. Microscopy Research and Technique, Vol. 33, Issue 1 https://doi.org/10.1002/(SICI)1097-0029(199601)33:1<23::AID-JEMT4>3.0.CO;2-1	journal	January 1996
Comparison of Sequencing Utility Programs Aronesty, Erik The Open Bioinformatics Journal, Vol. 7, Issue 1 https://doi.org/10.2174/1875036201307010001	journal	January 2013
Mobile Elements in a Single-Filament Orange Guaymas Basin Beggiatoa (“Candidatus Maribeggiatoa”) sp. Draft Genome: Evidence for Genetic Exchange with Cyanobacteria MacGregor, Barbara J.; Biddle, Jennifer F.; Teske, Andreas Applied and Environmental Microbiology, Vol. 79, Issue 13 https://doi.org/10.1128/AEM.03821-12	journal	April 2013
Microevolution of Burkholderia pseudomallei during an Acute Infection Limmathurotsakul, Direk; Holden, Matthew T. G.; Coupland, Paul Journal of Clinical Microbiology, Vol. 52, Issue 9 https://doi.org/10.1128/jcm.01219-14	journal	June 2014
Morphological Survey of Microbial Mats Near Deep-Sea Thermal Vents † Jannasch, Holger W.; Wirsen, Carl O. Applied and Environmental Microbiology, Vol. 41, Issue 2 https://doi.org/10.1128/aem.41.2.528-538.1981	journal	January 1981
Massive natural occurrence of unusually large bacteria (Beggiatoa sp.) at a hydro-thermal deep-sea vent site Jannasch, Holger W.; Nelson, Douglas C.; Wirsen, Carl O. Nature, Vol. 343, Issue 6256 https://doi.org/10.1038/343390b0	journal	January 1990
Subtidal Gastropods Consume Sulfur-Oxidizing Bacteria: Evidence from Coastal Hydrothermal Vents Stein, J. L. Science, Vol. 223, Issue 4637 https://doi.org/10.1126/science.223.4637.696	journal	February 1984
Microscopic examination and fatty acid characterization of filamentous bacteria colonizing substrata around subtidal hydrothermal vents Jacq, E.; Prieur, D.; Nichols, P. Archives of Microbiology, Vol. 152, Issue 1 https://doi.org/10.1007/BF00447013	journal	June 1989
Filamentous sulfur bacteria, Beggiatoa spp., in arctic marine sediments (Svalbard, 79°N): Filamentous sulfur bacteria in arctic sediments Jørgensen, Bo Barker; Dunker, Rita; Grünke, Stefanie FEMS Microbiology Ecology https://doi.org/10.1111/j.1574-6941.2010.00918.x	journal	June 2010
Spatial heterogeneity and underlying geochemistry of phylogenetically diverse orange and white Beggiatoa mats in Guaymas Basin hydrothermal sediments McKay, Luke J.; MacGregor, Barbara J.; Biddle, Jennifer F. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 67 https://doi.org/10.1016/j.dsr.2012.04.011	journal	September 2012
The Enigmatic Cytoarchitecture of Epulopiscium spp. Angert, Esther R. Microbiology Monographs https://doi.org/10.1007/7171_027	book	January 2006
Phylogenetic analysis of Beggiatoa spp. from organic rich sediment of Tokyo Bay, Japan Kojima, Hisaya; Fukui, Manabu Water Research, Vol. 37, Issue 13 https://doi.org/10.1016/s0043-1354(03)00206-9	journal	July 2003
Novel, Attached, Sulfur-Oxidizing Bacteria at Shallow Hydrothermal Vents Possess Vacuoles Not Involved in Respiratory Nitrate Accumulation Kalanetra, Karen M.; Huston, Sherry L.; Nelson, Douglas C. Applied and Environmental Microbiology, Vol. 70, Issue 12 https://doi.org/10.1128/AEM.70.12.7487-7496.2004	journal	December 2004
Temporal separation of cell division and diazotrophy in the marine diazotrophic cyanobacterium Trichodesmium erythraeum IMS101 Sandh, Gustaf; El-Shehawy, Rehab; DÃez, Beatriz FEMS Microbiology Letters, Vol. 295, Issue 2 https://doi.org/10.1111/j.1574-6968.2009.01608.x	journal	June 2009
Ploidy and gene conversion in Archaea Soppa, Jörg Biochemical Society Transactions, Vol. 39, Issue 1 https://doi.org/10.1042/BST0390150	journal	January 2011
The Genus Thiomargarita Schulz, Heide N. The Prokaryotes https://doi.org/10.1007/0-387-30746-X_47	book	January 2006
Distribution of colorless sulfur bacteria (Beggiatoa spp.) in a coastal marine sediment J�rgensen, B. B. Marine Biology, Vol. 41, Issue 1 https://doi.org/10.1007/BF00390577	journal	January 1977
Sphingopyxis jiangsuensis sp. nov. Isolated From the Surface Water of the Yellow Sea Gao, Zeng-Yu; Xue, Hua-Peng; Wang, Lu Current Microbiology, Vol. 79, Issue 7 https://doi.org/10.1007/s00284-022-02895-5	journal	June 2022
DNA–DNA hybridization values and their relationship to whole-genome sequence similarities Klappenbach, Joel A.; Goris, Johan; Vandamme, Peter International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 1 https://doi.org/10.1099/ijs.0.64483-0	journal	January 2007

Cited By (3)

Filamentous Giant Beggiatoaceae from the Guaymas Basin Are Capable of both Denitrification and Dissimilatory Nitrate Reduction to Ammonium Schutte, Charles A.; Teske, Andreas; MacGregor, Barbara J. Applied and Environmental Microbiology, Vol. 84, Issue 15 https://doi.org/10.1128/aem.02860-17	journal	May 2018
Genomic features of “Candidatus Venteria ishoeyi”, a new sulfur-oxidizing macrobacterium from the Humboldt Sulfuretum off Chile Fonseca, Alexis; Ishoey, Thomas; Espinoza, Carola PLOS ONE, Vol. 12, Issue 12 https://doi.org/10.1371/journal.pone.0188371	journal	December 2017
Filamentous giant Beggiatoaceae from the Guaymas Basin are capable of both denitrification and dissimilatory nitrate reduction to ammonium B. J., MacGregor,; P., Hach,; V., Salman-Carvalho, American Society for Microbiology https://doi.org/10.17615/7rmc-f896	text	January 2018

Figures / Tables (7)

Table 2 (Continued)(p. 10)

Similar Records

Single-cell sequencing of Thiomargarita reveals genomic flexibility for adaptation to dynamic redox conditions

Journal Article · Tue Jun 21 00:00:00 EDT 2016 · Frontiers in Microbiology · OSTI ID:1628147

Winkel, Matthias; Salman-Carvalho, Verena; Woyke, Tanja; +5 more

Whole genome sequencing analyses of Listeria monocytogenes that persisted in a milkshake machine for a year and caused illnesses in Washington State

Journal Article · Thu Jun 15 00:00:00 EDT 2017 · BMC Microbiology · OSTI ID:1628147

Li, Zhen; Pérez-Osorio, Ailyn; Wang, Yu; +5 more

Whole Genome Sequence Analysis Using JSpecies Tool Establishes Clonal Relationships between Listeria monocytogenes Strains from Epidemiologically Unrelated Listeriosis Outbreaks

Journal Article · Mon Mar 07 00:00:00 EST 2016 · PLoS ONE · OSTI ID:1628147

Burall, Laurel S.; Grim, Christopher J.; Mammel, Mark K.; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Microbiology
“Candidatus Marithrix
” filamentous sulfur bacteria
polyploidy
single nucleotide polymorphism
microevolution