Home LiteratureArticle Details
PMID: 21908640 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Partial genome assembly for a candidate division OP11 single cell from an anoxic spring (Zodletone Spring, Oklahoma).

Applied and environmental microbiology ·Vol. 77 ·No. 21 ·2011-11-00 ·Pages 7804-14

Youssef NH, Blainey PC, Quake SR, Elshahed MS

Abstract

Members of candidate division OP11 are widely distributed in terrestrial and marine ecosystems, yet little information regarding their metabolic capabilities and ecological role within such habitats is currently available. Here, we report on the microfluidic isolation, multiple-displacement-amplification, pyrosequencing, and genomic analysis of a single cell (ZG1) belonging to candidate division OP11. Genome analysis of the ∼270-kb partial genome assembly obtained showed that it had no particular similarity to a specific phylum. Four hundred twenty-three open reading frames were identified, 46% of which had no function prediction. In-depth analysis revealed a heterotrophic lifestyle, with genes encoding endoglucanase, amylopullulanase, and laccase enzymes, suggesting a capacity for utilization of cellulose, starch, and, potentially, lignin, respectively. Genes encoding several glycolysis enzymes as well as formate utilization were identified, but no evidence for an electron transport chain was found. The presence of genes encoding various components of lipopolysaccharide biosynthesis indicates a Gram-negative bacterial cell wall. The partial genome also provides evidence for antibiotic resistance (β-lactamase, aminoglycoside phosphotransferase), as well as antibiotic production (bacteriocin) and extracellular bactericidal peptidases. Multiple mechanisms for stress response were identified, as were elements of type I and type IV secretion systems. Finally, housekeeping genes identified within the partial genome were used to demonstrate the OP11 affiliation of multiple hitherto unclassified genomic fragments from multiple database-deposited metagenomic data sets. These results provide the first glimpse into the lifestyle of a member of a ubiquitous, yet poorly understood bacterial candidate division.

MeSH Terms
Bacteria, Anaerobic/genetics,isolation & purification Bacteriocins/genetics Cluster Analysis DNA, Bacterial/chemistry,genetics DNA, Ribosomal/chemistry,genetics Drug Resistance, Bacterial Genome, Bacterial Gram-Negative Bacteria/genetics,isolation & purification Heterotrophic Processes Hot Springs/microbiology Membrane Transport Proteins/genetics Oklahoma Open Reading Frames Phylogeny RNA, Ribosomal, 16S/genetics Sequence Analysis, DNA Sequence Homology
Chemicals
Bacteriocins DNA, Bacterial DNA, Ribosomal Membrane Transport Proteins RNA, Ribosomal, 16S
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Youssef Noha H
Department of Microbiology and Molecular Genetics, Oklahoma State University, Stillwater, OK 74074, USA.
Blainey Paul C
Quake Stephen R
Elshahed Mostafa S
References (61)
61 references, click to expand
  1. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific.
    PLoS Biol. 2007 Mar;5(3):e77 PMID: 17355176
  2. Bacterial diversity and sulfur cycling in a mesophilic sulfide-rich spring.
    Appl Environ Microbiol. 2003 Sep;69(9):5609-21 PMID: 12957951
  3. Changes in microbial community composition and geochemistry during uranium and technetium bioimmobilization.
    Appl Environ Microbiol. 2007 Sep;73(18):5885-96 PMID: 17630297
  4. Novel division level bacterial diversity in a Yellowstone hot spring.
    J Bacteriol. 1998 Jan;180(2):366-76 PMID: 9440526
  5. One bacterial cell, one complete genome.
    PLoS One. 2010 Apr 23;5(4):e10314 PMID: 20428247
  6. Comprehensive human genome amplification using multiple displacement amplification.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5261-6 PMID: 11959976
  7. Novel polyphenol oxidase mined from a metagenome expression library of bovine rumen: biochemical properties, structural analysis, and phylogenetic relationships.
    J Biol Chem. 2006 Aug 11;281(32):22933-42 PMID: 16740638
  8. MEROPS: the peptidase database.
    Nucleic Acids Res. 2010 Jan;38(Database issue):D227-33 PMID: 19892822
  9. "Candidatus Cloacamonas acidaminovorans": genome sequence reconstruction provides a first glimpse of a new bacterial division.
    J Bacteriol. 2008 Apr;190(7):2572-9 PMID: 18245282
  10. Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell.
    Proc Natl Acad Sci U S A. 2008 Apr 8;105(14):5555-60 PMID: 18391199
  11. Genome streamlining in a cosmopolitan oceanic bacterium.
    Science. 2005 Aug 19;309(5738):1242-5 PMID: 16109880
  12. Digital PCR provides sensitive and absolute calibration for high throughput sequencing.
    BMC Genomics. 2009 Mar 19;10:116 PMID: 19298667
  13. Environmental genome shotgun sequencing of the Sargasso Sea.
    Science. 2004 Apr 2;304(5667):66-74 PMID: 15001713
  14. Clustal W and Clustal X version 2.0.
    Bioinformatics. 2007 Nov 1;23(21):2947-8 PMID: 17846036
  15. The integrated microbial genomes system: an expanding comparative analysis resource.
    Nucleic Acids Res. 2010 Jan;38(Database issue):D382-90 PMID: 19864254
  16. Fine-scale bacterial beta diversity within a complex ecosystem (Zodletone Spring, OK, USA): the role of the rare biosphere.
    PLoS One. 2010 Aug 26;5(8):e12414 PMID: 20865128
  17. Digital MDA for enumeration of total nucleic acid contamination.
    Nucleic Acids Res. 2011 Mar;39(4):e19 PMID: 21071419
  18. Inverted repeat structure of the human genome: the X-chromosome contains a preponderance of large, highly homologous inverted repeats that contain testes genes.
    Genome Res. 2004 Oct;14(10A):1861-9 PMID: 15466286
  19. The versatile bacterial type IV secretion systems.
    Nat Rev Microbiol. 2003 Nov;1(2):137-49 PMID: 15035043
  20. The Pfam protein families database.
    Nucleic Acids Res. 2010 Jan;38(Database issue):D211-22 PMID: 19920124
  21. Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis.
    PLoS One. 2011 Feb 22;6(2):e16626 PMID: 21364937
  22. The Pfam protein families database.
    Nucleic Acids Res. 2002 Jan 1;30(1):276-80 PMID: 11752314
  23. Metagenomic discovery of biomass-degrading genes and genomes from cow rumen.
    Science. 2011 Jan 28;331(6016):463-7 PMID: 21273488
  24. A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export.
    Mol Microbiol. 1995 Apr;16(2):229-40 PMID: 7565085
  25. The InterPro database, an integrated documentation resource for protein families, domains and functional sites.
    Nucleic Acids Res. 2001 Jan 1;29(1):37-40 PMID: 11125043
  26. Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation.
    Appl Environ Microbiol. 1998 Oct;64(10):3869-77 PMID: 9758812
  27. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases.
    Nucleic Acids Res. 2010 Jan;38(Database issue):D473-9 PMID: 19850718
  28. 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
  29. Secretion of beta-lactamase requires the carboxy end of the protein.
    Cell. 1980 Jul;20(3):749-60 PMID: 6448092
  30. Nanoliter reactors improve multiple displacement amplification of genomes from single cells.
    PLoS Genet. 2007 Sep;3(9):1702-8 PMID: 17892324
  31. Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth.
    Proc Natl Acad Sci U S A. 2007 Jul 17;104(29):11889-94 PMID: 17620602
  32. Novel pathways for biosynthesis of nucleotide-activated glycero-manno-heptose precursors of bacterial glycoproteins and cell surface polysaccharides.
    Microbiology (Reading). 2002 Jul;148(Pt 7):1979-1989 PMID: 12101286
  33. Prokaryotic toxin-antitoxin stress response loci.
    Nat Rev Microbiol. 2005 May;3(5):371-82 PMID: 15864262
  34. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.
    Appl Environ Microbiol. 2006 Jul;72(7):5069-72 PMID: 16820507
  35. Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities.
    Appl Environ Microbiol. 2002 Apr;68(4):1994-2007 PMID: 11916723
  36. Phylogenetic and metabolic diversity of Planctomycetes from anaerobic, sulfide- and sulfur-rich Zodletone Spring, Oklahoma.
    Appl Environ Microbiol. 2007 Aug;73(15):4707-16 PMID: 17545322
  37. Transcription regulation and environmental adaptation in bacteria.
    Trends Microbiol. 2003 Jun;11(6):248-53 PMID: 12823939
  38. KEGG for representation and analysis of molecular networks involving diseases and drugs.
    Nucleic Acids Res. 2010 Jan;38(Database issue):D355-60 PMID: 19880382
  39. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics.
    Nucleic Acids Res. 2009 Jan;37(Database issue):D233-8 PMID: 18838391
  40. Tandem repeats finder: a program to analyze DNA sequences.
    Nucleic Acids Res. 1999 Jan 15;27(2):573-80 PMID: 9862982
  41. New perspective on uncultured bacterial phylogenetic division OP11.
    Appl Environ Microbiol. 2004 Feb;70(2):845-9 PMID: 14766563
  42. Environmental whole-genome amplification to access microbial populations in contaminated sediments.
    Appl Environ Microbiol. 2006 May;72(5):3291-301 PMID: 16672469
  43. A bioinformatician's guide to metagenomics.
    Microbiol Mol Biol Rev. 2008 Dec;72(4):557-78, Table of Contents PMID: 19052320
  44. Complete-fosmid and fosmid-end sequences reveal frequent horizontal gene transfers in marine uncultured planktonic archaea.
    ISME J. 2011 Aug;5(8):1291-302 PMID: 21346789
  45. Structure and role of coupling proteins in conjugal DNA transfer.
    Res Microbiol. 2002 May;153(4):199-204 PMID: 12066890
  46. Whole genome amplification and de novo assembly of single bacterial cells.
    PLoS One. 2009 Sep 02;4(9):e6864 PMID: 19724646
  47. Assessment of the diversity, abundance, and ecological distribution of members of candidate division SR1 reveals a high level of phylogenetic diversity but limited morphotypic diversity.
    Appl Environ Microbiol. 2009 Jun;75(12):4139-48 PMID: 19395567
  48. Extrachromosomal resistance in gram-negative organisms: the evolution of beta-lactamase.
    Trends Microbiol. 1994 Oct;2(10):357-60 PMID: 7850201
  49. Characterization of large-insert DNA libraries from soil for environmental genomic studies of Archaea.
    Environ Microbiol. 2004 Sep;6(9):970-80 PMID: 15305922
  50. Novelty and uniqueness patterns of rare members of the soil biosphere.
    Appl Environ Microbiol. 2008 Sep;74(17):5422-8 PMID: 18606799
  51. Enzymatic "combustion": the microbial degradation of lignin.
    Annu Rev Microbiol. 1987;41:465-505 PMID: 3318677
  52. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity.
    J Bacteriol. 1998 Sep;180(18):4765-74 PMID: 9733676
  53. Rfam: updates to the RNA families database.
    Nucleic Acids Res. 2009 Jan;37(Database issue):D136-40 PMID: 18953034
  54. Artemis: sequence visualization and annotation.
    Bioinformatics. 2000 Oct;16(10):944-5 PMID: 11120685
  55. Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community.
    ISME J. 2010 May;4(5):660-72 PMID: 20182523
  56. NCBI BLAST: a better web interface.
    Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W5-9 PMID: 18440982
  57. Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities.
    Nat Biotechnol. 2006 Oct;24(10):1263-9 PMID: 16998472
  58. The crystal structure of aminoglycoside-3'-phosphotransferase-IIa, an enzyme responsible for antibiotic resistance.
    J Mol Biol. 2003 Mar 21;327(2):491-506 PMID: 12628253
  59. Real-time DNA sequencing from single polymerase molecules.
    Science. 2009 Jan 2;323(5910):133-8 PMID: 19023044
  60. A rare SAR11 fosmid clone confirming genetic variability in the 'Candidatus Pelagibacter ubique' genome.
    ISME J. 2008 Jul;2(7):790-3 PMID: 18496576
  61. Genomic and functional adaptation in surface ocean planktonic prokaryotes.
    Nature. 2010 Nov 4;468(7320):60-6 PMID: 21048761
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
1098-5336
Published
2011-11-00
Epub
2011-00-09
Pages
7804-14
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC3209139
Subset
IM
Grants
NHGRI NIH HHS · R01 HG004863 · United States
NHGRI NIH HHS · 5R01HG004863-02 · United States
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