Home LiteratureArticle Details
PMID: 17760503 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Insights into the genome of large sulfur bacteria revealed by analysis of single filaments.

PLoS biology ·Vol. 5 ·No. 9 ·2007-09-00 ·Pages e230

Mussmann M, Hu FZ, Richter M, de Beer D, Preisler A, Jørgensen BB, Huntemann M, Glöckner FO, Amann R, Koopman WJ, Lasken RS, Janto B, Hogg J, Stoodley P, Boissy R, Ehrlich GD

Abstract

Marine sediments are frequently covered by mats of the filamentous Beggiatoa and other large nitrate-storing bacteria that oxidize hydrogen sulfide using either oxygen or nitrate, which they store in intracellular vacuoles. Despite their conspicuous metabolic properties and their biogeochemical importance, little is known about their genetic repertoire because of the lack of pure cultures. Here, we present a unique approach to access the genome of single filaments of Beggiatoa by combining whole genome amplification, pyrosequencing, and optical genome mapping. Sequence assemblies were incomplete and yielded average contig sizes of approximately 1 kb. Pathways for sulfur oxidation, nitrate and oxygen respiration, and CO2 fixation confirm the chemolithoautotrophic physiology of Beggiatoa. In addition, Beggiatoa potentially utilize inorganic sulfur compounds and dimethyl sulfoxide as electron acceptors. We propose a mechanism of vacuolar nitrate accumulation that is linked to proton translocation by vacuolar-type ATPases. Comparative genomics indicates substantial horizontal gene transfer of storage, metabolic, and gliding capabilities between Beggiatoa and cyanobacteria. These capabilities enable Beggiatoa to overcome non-overlapping availabilities of electron donors and acceptors while gliding between oxic and sulfidic zones. The first look into the genome of these filamentous sulfur-oxidizing bacteria substantially deepens the understanding of their evolution and their contribution to sulfur and nitrogen cycling in marine sediments.

MeSH Terms
Actin Cytoskeleton/genetics Base Sequence Beggiatoa/genetics Genome, Bacterial Hydrogen Sulfide/metabolism Metabolic Networks and Pathways/genetics Nitrates/metabolism Oxidation-Reduction Oxygen/metabolism
Chemicals
Nitrates Oxygen Hydrogen Sulfide
Authors & Affiliations
16 authors, click to expand affiliations / ORCID
Mussmann Marc
Max Planck Institute for Marine Microbiology, Bremen, Germany. mussmann@mpi-bremen.de
Hu Fen Z
Richter Michael
de Beer Dirk
Preisler André
Jørgensen Bo B
Huntemann Marcel
Glöckner Frank Oliver
Amann Rudolf
Koopman Werner J H
Lasken Roger S
Janto Benjamin
Hogg Justin
Stoodley Paul
Boissy Robert
Ehrlich Garth D
References (77)
77 references, click to expand
  1. The potential value of indels as phylogenetic markers: position of trichomonads as a case study.
    Mol Biol Evol. 2002 Jun;19(6):972-7 PMID: 12032255
  2. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.
    J Mol Biol. 2001 Jan 19;305(3):567-80 PMID: 11152613
  3. High Nitrate Concentrations in Vacuolate, Autotrophic Marine Beggiatoa spp.
    Appl Environ Microbiol. 1996 Mar;62(3):954-8 PMID: 16535282
  4. Rotation, structure, and classification of prokaryotic V-ATPase.
    J Bioenerg Biomembr. 2005 Dec;37(6):405-10 PMID: 16691473
  5. A sequencing method based on real-time pyrophosphate.
    Science. 1998 Jul 17;281(5375):363, 365 PMID: 9705713
  6. Open source clustering software.
    Bioinformatics. 2004 Jun 12;20(9):1453-4 PMID: 14871861
  7. Sequence analysis and biochemical characterization of the nostopeptolide A biosynthetic gene cluster from Nostoc sp. GSV224.
    Gene. 2003 Jun 5;311:171-80 PMID: 12853152
  8. Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum.
    J Bacteriol. 2005 Feb;187(4):1392-404 PMID: 15687204
  9. [Regulation of metabolic and electron transport pathways in the freshwater bacterium Beggiatoa leptomitiformis D-402].
    Mikrobiologiia. 2005 Jul-Aug;74(4):452-9 PMID: 16211847
  10. Physiological and gene expression analysis of inhibition of Desulfovibrio vulgaris hildenborough by nitrite.
    J Bacteriol. 2004 Dec;186(23):7944-50 PMID: 15547266
  11. Use of reduced sulfur compounds by Beggiatoa sp.
    J Bacteriol. 1981 Jul;147(1):140-54 PMID: 7240091
  12. Sequencing genomes from single cells by polymerase cloning.
    Nat Biotechnol. 2006 Jun;24(6):680-6 PMID: 16732271
  13. Periplasmic and membrane-bound respiratory nitrate reductases in Thiosphaera pantotropha. The periplasmic enzyme catalyzes the first step in aerobic denitrification.
    FEBS Lett. 1990 Jun 4;265(1-2):85-7 PMID: 2365057
  14. The genome of deep-sea vent chemolithoautotroph Thiomicrospira crunogena XCL-2.
    PLoS Biol. 2006 Nov;4(12):e383 PMID: 17105352
  15. Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes.
    Microbiology. 1997 Sep;143 ( Pt 9):2891-902 PMID: 9308173
  16. Whole-genome shotgun optical mapping of Rhodospirillum rubrum.
    Appl Environ Microbiol. 2005 Sep;71(9):5511-22 PMID: 16151144
  17. Sulfur metabolism in Beggiatoa alba.
    J Bacteriol. 1987 Dec;169(12):5466-72 PMID: 3316186
  18. Prediction of effective genome size in metagenomic samples.
    Genome Biol. 2007;8(1):R10 PMID: 17224063
  19. Phylogeny and distribution of nitrate-storing Beggiatoa spp. in coastal marine sediments.
    Environ Microbiol. 2003 Jun;5(6):523-33 PMID: 12755720
  20. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence.
    Nucleic Acids Res. 1997 Mar 1;25(5):955-64 PMID: 9023104
  21. Genome sequence of the chemolithoautotrophic nitrite-oxidizing bacterium Nitrobacter winogradskyi Nb-255.
    Appl Environ Microbiol. 2006 Mar;72(3):2050-63 PMID: 16517654
  22. Rapid amplification of plasmid and phage DNA using Phi 29 DNA polymerase and multiply-primed rolling circle amplification.
    Genome Res. 2001 Jun;11(6):1095-9 PMID: 11381035
  23. The mechanism of nitrate transport across the tonoplast of barley root cells.
    Planta. 1992 Jul;187(4):554-7 PMID: 24178152
  24. Nitrogen, carbon, and sulfur metabolism in natural thioploca samples
    Appl Environ Microbiol. 1999 Jul;65(7):3148-57 PMID: 10388716
  25. Sulfite-oxido-reductase is involved in the oxidation of sulfite in Desulfocapsa sulfoexigens during disproportionation of thiosulfate and elemental sulfur.
    Biodegradation. 2003 Jun;14(3):189-98 PMID: 12889609
  26. Diversity and dynamics of a north atlantic coastal Vibrio community.
    Appl Environ Microbiol. 2004 Jul;70(7):4103-10 PMID: 15240289
  27. Dinucleotide relative abundance extremes: a genomic signature.
    Trends Genet. 1995 Jul;11(7):283-90 PMID: 7482779
  28. Heterotrophic carbon metabolism by Beggiatoa alba.
    J Bacteriol. 1981 Nov;148(2):572-83 PMID: 6117547
  29. The napF and narG nitrate reductase operons in Escherichia coli are differentially expressed in response to submicromolar concentrations of nitrate but not nitrite.
    J Bacteriol. 1999 Sep;181(17):5303-8 PMID: 10464201
  30. Cultivated Beggiatoa spp. define the phylogenetic root of morphologically diverse, noncultured, vacuolate sulfur bacteria.
    Can J Microbiol. 2006 Jun;52(6):591-8 PMID: 16788728
  31. Dense populations of a giant sulfur bacterium in Namibian shelf sediments.
    Science. 1999 Apr 16;284(5413):493-5 PMID: 10205058
  32. The spectrum of genomic signatures: from dinucleotides to chaos game representation.
    Gene. 2005 Feb 14;346:173-85 PMID: 15716010
  33. Use of Reduced Sulfur Compounds by Beggiatoa spp.: Enzymology and Physiology of Marine and Freshwater Strains in Homogeneous and Gradient Cultures.
    Appl Environ Microbiol. 1997 Oct;63(10):3957-64 PMID: 16535709
  34. Oxygen Responses and Mat Formation by Beggiatoa spp.
    Appl Environ Microbiol. 1985 Aug;50(2):373-82 PMID: 16346857
  35. Big bacteria.
    Annu Rev Microbiol. 2001;55:105-37 PMID: 11544351
  36. Enrichment and cultivation of Beggiatoa alba.
    J Bacteriol. 1961 Jan;81:99-106 PMID: 13698371
  37. Community structure and metabolism through reconstruction of microbial genomes from the environment.
    Nature. 2004 Mar 4;428(6978):37-43 PMID: 14961025
  38. Horizontal transfers confuse the prokaryotic phylogeny based on the HSP70 protein family.
    Mol Microbiol. 1999 Feb;31(3):1007-10 PMID: 10048042
  39. Mechanism of chimera formation during the Multiple Displacement Amplification reaction.
    BMC Biotechnol. 2007;7:19 PMID: 17430586
  40. Machine learning approaches for the prediction of signal peptides and other protein sorting signals.
    Protein Eng. 1999 Jan;12(1):3-9 PMID: 10065704
  41. Colorless Sulfur Bacteria, Beggiatoa spp. and Thiovulum spp., in O(2) and H(2)S Microgradients.
    Appl Environ Microbiol. 1983 Apr;45(4):1261-70 PMID: 16346268
  42. Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur.
    Microbiology. 1998 Jul;144 ( Pt 7):1881-94 PMID: 9695921
  43. Targeted access to the genomes of low-abundance organisms in complex microbial communities.
    Appl Environ Microbiol. 2007 May;73(10):3205-14 PMID: 17369337
  44. Growth Pattern and Yield of a Chemoautotrophic Beggiatoa sp. in Oxygen-Sulfide Microgradients.
    Appl Environ Microbiol. 1986 Aug;52(2):225-33 PMID: 16347121
  45. GenDB--an open source genome annotation system for prokaryote genomes.
    Nucleic Acids Res. 2003 Apr 15;31(8):2187-95 PMID: 12682369
  46. Symbiosis insights through metagenomic analysis of a microbial consortium.
    Nature. 2006 Oct 26;443(7114):950-5 PMID: 16980956
  47. Determination of the molecular mass of bacterial genomic DNA and plasmid copy number by high-pressure liquid chromatography.
    Appl Environ Microbiol. 1985 Oct;50(4):1007-13 PMID: 4083871
  48. The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles.
    Nature. 2006 Aug 24;442(7105):939-42 PMID: 16878138
  49. Uptake rates of oxygen and sulfide measured with individual Thiomargarita namibiensis cells by using microelectrodes.
    Appl Environ Microbiol. 2002 Nov;68(11):5746-9 PMID: 12406774
  50. Evidence for the microbial basis of a chemoautotrophic invertebrate community at a whale fall on the deep seafloor: bone-colonizing bacteria and invertebrate endosymbionts.
    Microsc Res Tech. 1997 Apr 15;37(2):162-70 PMID: 9145396
  51. Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism?
    Appl Environ Microbiol. 2001 Jul;67(7):2873-82 PMID: 11425697
  52. Distribution and diversity of natural product genes in marine and freshwater cyanobacterial cultures and genomes.
    Appl Environ Microbiol. 2005 Nov;71(11):7401-13 PMID: 16269782
  53. Deciphering the evolution and metabolism of an anammox bacterium from a community genome.
    Nature. 2006 Apr 6;440(7085):790-4 PMID: 16598256
  54. ARB: a software environment for sequence data.
    Nucleic Acids Res. 2004;32(4):1363-71 PMID: 14985472
  55. Comprehensive human genome amplification using multiple displacement amplification.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5261-6 PMID: 11959976
  56. Nitrate storage and retrieval in Beta vulgaris: Effects of nitrate and chloride on proton gradients in tonoplast vesicles.
    Proc Natl Acad Sci U S A. 1985 Jun;82(11):3683-7 PMID: 16593570
  57. Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum.
    Mol Microbiol. 2006 Nov;62(3):794-810 PMID: 16995898
  58. Evidence of giant sulphur bacteria in Neoproterozoic phosphorites.
    Nature. 2007 Jan 11;445(7124):198-201 PMID: 17183268
  59. Anaerobic sulfide oxidation with nitrate by a freshwater Beggiatoa enrichment culture.
    Appl Environ Microbiol. 2006 Jul;72(7):4755-60 PMID: 16820468
  60. Specific single-cell isolation and genomic amplification of uncultured microorganisms.
    Appl Microbiol Biotechnol. 2007 Mar;74(4):926-35 PMID: 17109170
  61. Large sulfur bacteria and the formation of phosphorite.
    Science. 2005 Jan 21;307(5708):416-8 PMID: 15662012
  62. Genomic DNA amplification from a single bacterium.
    Appl Environ Microbiol. 2005 Jun;71(6):3342-7 PMID: 15933038
  63. Impact of bacterial NO3(-) transport on sediment biogeochemistry.
    Appl Environ Microbiol. 2005 Nov;71(11):7575-7 PMID: 16269807
  64. Pathways and microbiology of thiosulfate transformations and sulfate reduction in a marine sediment (kattegat, denmark).
    Appl Environ Microbiol. 1991 Mar;57(3):847-56 PMID: 16348450
  65. Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum.
    Arch Microbiol. 1998 Jul;170(1):59-68 PMID: 9639604
  66. The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans.
    J Bacteriol. 2006 Feb;188(4):1473-88 PMID: 16452431
  67. Genome sequencing in microfabricated high-density picolitre reactors.
    Nature. 2005 Sep 15;437(7057):376-80 PMID: 16056220
  68. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea.
    Science. 2000 Sep 15;289(5486):1902-6 PMID: 10988064
  69. Whole genome amplification: abundant supplies of DNA from precious samples or clinical specimens.
    Trends Biotechnol. 2003 Dec;21(12):531-5 PMID: 14624861
  70. Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins.
    Mol Microbiol. 2001 Oct;42(2):279-92 PMID: 11703654
  71. Diel Migrations of Microorganisms within a Benthic, Hypersaline Mat Community.
    Appl Environ Microbiol. 1994 May;60(5):1500-11 PMID: 16349251
  72. Clustered genes related to sulfate respiration in uncultured prokaryotes support the theory of their concomitant horizontal transfer.
    J Bacteriol. 2005 Oct;187(20):7126-37 PMID: 16199583
  73. Application of tetranucleotide frequencies for the assignment of genomic fragments.
    Environ Microbiol. 2004 Sep;6(9):938-47 PMID: 15305919
  74. Vacuolar H(+)-pyrophosphatase.
    Biochim Biophys Acta. 2000 May 1;1465(1-2):37-51 PMID: 10748246
  75. Specificity of respiratory pathways involved in the reduction of sulfur compounds by Salmonella enterica.
    Microbiology. 2002 Nov;148(Pt 11):3631-8 PMID: 12427953
  76. Organic carbon utilization by obligately and facultatively autotrophic beggiatoa strains in homogeneous and gradient cultures.
    Appl Environ Microbiol. 1996 Mar;62(3):947-53 PMID: 16535281
  77. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms.
    Appl Environ Microbiol. 2000 Jun;66(6):2541-7 PMID: 10831436
Article Info
Journal
PLoS biology
Abbr.
PLoS Biol
ISSN
1545-7885
DOI
10.1371/journal.pbio.0050230
Email
mussmann@mpi-bremen.de
Published
2007-09-00
Pages
e230
Language
English
Region
United States
NLM ID
101183755
PMCID
PMC1951784
Subset
IM
Grants
NIDCD NIH HHS · R01 DC002148 · United States
NIDCD NIH HHS · R01 DC004173 · United States
NIDCD NIH HHS · DC02148 · United States
NIDCD NIH HHS · DC04173 · United States
External Links
PubMed source DOI: 10.1371/journal.pbio.0050230 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2