Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Microbiology Resource Announcements
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Latest Articles
    • Archive
  • Types of Resources
    • Amplicon Sequence Collections
    • Culture Collections/Mutant Libraries
    • Databases and Software
    • Omics Data Sets
    • Other Genetic Resources
    • Genome Sequences
  • For Authors
    • Getting Started
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About MRA
    • Editor in Chief
    • Board of Editors
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Microbiology Resource Announcements
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Microbiology Resource Announcements
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Latest Articles
    • Archive
  • Types of Resources
    • Amplicon Sequence Collections
    • Culture Collections/Mutant Libraries
    • Databases and Software
    • Omics Data Sets
    • Other Genetic Resources
    • Genome Sequences
  • For Authors
    • Getting Started
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About MRA
    • Editor in Chief
    • Board of Editors
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
Prokaryotes

Draft Genome Sequence of Serratia sp. Strain ATCC 39006, a Model Bacterium for Analysis of the Biosynthesis and Regulation of Prodigiosin, a Carbapenem, and Gas Vesicles

Peter C. Fineran, Marina C. Iglesias Cans, Joshua P. Ramsay, Nabil M. Wilf, Desiree Cossyleon, Matthew B. McNeil, Neil R. Williamson, Rita E. Monson, S. Anette Becher, Jo-Ann L. Stanton, Kim Brügger, Steven D. Brown, George P. C. Salmond
Peter C. Fineran
Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealanda
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Marina C. Iglesias Cans
Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealanda
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Joshua P. Ramsay
Department of Biochemistry, University of Cambridge, Cambridge, United Kingdomb
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Nabil M. Wilf
Department of Biochemistry, University of Cambridge, Cambridge, United Kingdomb
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Desiree Cossyleon
Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealanda
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Matthew B. McNeil
Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealanda
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Neil R. Williamson
Department of Biochemistry, University of Cambridge, Cambridge, United Kingdomb
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Rita E. Monson
Department of Biochemistry, University of Cambridge, Cambridge, United Kingdomb
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
S. Anette Becher
AgResearch Ltd., Invermay Agricultural Centre, Mosgiel, New Zealandc
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jo-Ann L. Stanton
Department of Anatomy, University of Otago, Dunedin, New Zealandd
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Kim Brügger
EASIH, University of Cambridge, Addenbrooke's Hospital, Cambridge, United Kingdome
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Steven D. Brown
Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USAf
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
George P. C. Salmond
Department of Biochemistry, University of Cambridge, Cambridge, United Kingdomb
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/genomeA.01039-13
  • Article
  • Info & Metrics
  • PDF
Loading

ABSTRACT

Serratia sp. strain ATCC 39006 is a Gram-negative bacterium and a member of the Enterobacteriaceae that produces various bioactive secondary metabolites, including the tripyrrole red pigment prodigiosin and the β-lactam antibiotic 1-carbapenen-2-em-3-carboxylic acid (a carbapenem). This strain is the only member of the Enterobacteriaceae known to naturally produce gas vesicles, as flotation organelles. Here we present the genome sequence of this strain, which has served as a model for analysis of the biosynthesis and regulation of antibiotic production.

GENOME ANNOUNCEMENT

Serratia sp. strain ATCC 39006 was originally isolated from Salicornia alterniflora and in channel water from a salt marsh in Cheesequake, NJ, in a search by the Squibb Chemical Company for bacteria producing new antibiotics (1). In addition to the β-lactam produced, identified as 1-carbapen-2-em-3-carboxylic acid (a carbapenem) (2), this strain synthesizes the red, linear tripyrrole pigment prodigiosin (2-methyl-3-pentyl-6-methoxyprodigiosin). Prodigiosin is a secondary metabolite with antimicrobial, anticancer, and immunosuppressant properties with derivatives in clinical trials (3, 4). Serratia sp. strain ATCC 39006 was used to determine the prodigiosin biosynthetic pathway, with implications for biosynthesis of the related compound, undecylprodigiosin, produced by Streptomyces coelicolor (4, 5). Furthermore, Serratia sp. strain ATCC 39006 has provided an excellent model for investigating the regulation of antibiotic biosynthesis in Gram-negative enterobacteria (4). The control of these secondary metabolites is complex and responds to quorum sensing (6–8), cyclic di-GMP signaling (9, 10), phosphate availability (7, 11), carbon source (12), Hfq (13), stationary phase (14), and drug efflux pump activity (15), among other factors. In addition, due to the ease of prodigiosin detection, this strain has been used to analyze conserved uncharacterized genes and gene products (16–18). For example, SdhE was recently investigated in this strain. SdhE is widely conserved in eukaryotes and Alpha-, Beta-, and Gammaproteobacteria and is essential for flavinylation and activation of succinate dehydrogenase, an enzyme central to the electron transport chain and the tricarboxylic acid cycle (17, 19, 20).

Serratia sp. strain ATCC 39006 is motile by means of flagella and can swarm over surfaces aided by the production of a biosurfactant (10). Surprisingly, this strain also produces gas vesicles, which are hollow intracellular proteinaceous organelles that control bacterial buoyancy and allow flotation toward air-liquid interfaces (21). This is the only known enterobacterium to utilize this form of taxis naturally (21). The secretion of plant cell wall-degrading enzymes is also a feature of this bacterium, and plant pathogenicity has been confirmed in potato tuber-rotting assays (6, 9). Furthermore, this strain is virulent in a Caenorhabditis elegans infection model (22). The genetic analysis of Serratia sp. strain ATCC 39006 has been greatly facilitated by the isolation of an efficient broad-host-range generalized transducing phage (23).

Genomic DNA of Serratia sp. strain ATCC 39006 was sequenced using the 454 GS FLX Titanium platform (Roche) (~18× coverage single-end data) and 36-bp Illumina single-end reads (GAIIx) (~439× coverage). The 454 data were de novo assembled (Newbler v2.3), giving 53 large contigs (99.9% of sequence) from 94 total contigs. These were assembled into 5 scaffolds using PCR and Sanger sequencing (3 contigs between 200 and 1,000 bp remained). Illumina reads were mapped using BWA 0.5.8, indels were detected using GATK (24), and the sequence was polished using a custom perl script.

The Serratia sp. strain ATCC 39006 genome is ~4.94 Mb (G+C content of 49.2%), with 4,413 protein-encoding genes, 7 rRNA operons, and 72 tRNAs (predicted using Prodigal [25]). This sequence will now enable further analysis of the diverse and interesting biological traits that have been defined in this unusual enterobacterium.

Nucleotide sequence accession numbers.This whole-genome shotgun project has been deposited at DDBJ/EMBL/GenBank under the accession number AWXH00000000. The version described in this paper is version AWXH01000000.

ACKNOWLEDGMENTS

We thank Miriam Land (ORNL) for maintaining the Microbial Annotation Genome Pipeline and Sagar Utturkar (University of Tennessee) for assistance with depositing the genome sequence into GenBank.

This work was supported by a University of Otago research grant; the BBSRC, United Kingdom; the Deans Bequest Fund, Otago School of Medical Sciences; the Marsden Fund of the Royal Society of New Zealand (RSNZ); and the BioEnergy Science Center, which is a Department of Energy (DOE) Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. P.C.F. was supported by a Rutherford Discovery Fellowship (RSNZ), J.P.R. by a Herchel Smith Postdoctoral Fellowship from the University of Cambridge, N.M.W. by a Gates Cambridge Scholarship, and M.B.M. and J.P.R. by University of Otago Career Development Postdoctoral Fellowships. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. DOE under contract DE-AC05-00OR22725.

FOOTNOTES

    • Received 1 November 2013.
    • Accepted 11 November 2013.
    • Published 12 December 2013.
  • Copyright © 2013 Fineran et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 3.0 Unported license.

REFERENCES

  1. 1.↵
    1. Parker WL,
    2. Rathnum ML,
    3. Wells JS Jr.,
    4. Trejo WH,
    5. Principe PA,
    6. Sykes RB
    . 1982. SQ 27,860, a simple carbapenem produced by species of Serratia and Erwinia. J. Antibiot. 35:653–660.
    OpenUrlCrossRefPubMed
  2. 2.↵
    1. Coulthurst SJ,
    2. Barnard AM,
    3. Salmond GP
    . 2005. Regulation and biosynthesis of carbapenem antibiotics in bacteria. Nat. Rev. Microbiol. 3:295–306.
    OpenUrlCrossRefPubMedWeb of Science
  3. 3.↵
    1. Williamson NR,
    2. Fineran PC,
    3. Gristwood T,
    4. Chawrai SR,
    5. Leeper FJ,
    6. Salmond GP
    . 2007. Anticancer and immunosuppressive properties of bacterial prodiginines. Future Microbiol. 2:605–618.
    OpenUrlCrossRefPubMedWeb of Science
  4. 4.↵
    1. Williamson NR,
    2. Fineran PC,
    3. Leeper FJ,
    4. Salmond GP
    . 2006. The biosynthesis and regulation of bacterial prodiginines. Nat. Rev. Microbiol. 4:887–899.
    OpenUrlCrossRefPubMed
  5. 5.↵
    1. Williamson NR,
    2. Simonsen HT,
    3. Ahmed RA,
    4. Goldet G,
    5. Slater H,
    6. Woodley L,
    7. Leeper FJ,
    8. Salmond GP
    . 2005. Biosynthesis of the red antibiotic, prodigiosin, in Serratia: identification of a novel 2-methyl-3-n-amyl-pyrrole (MAP) assembly pathway, definition of the terminal condensing enzyme, and implications for undecylprodigiosin biosynthesis in Streptomyces. Mol. Microbiol. 56:971–989.
    OpenUrlCrossRefPubMed
  6. 6.↵
    1. Fineran PC,
    2. Slater H,
    3. Everson L,
    4. Hughes K,
    5. Salmond GP
    . 2005. Biosynthesis of tripyrrole and beta-lactam secondary metabolites in Serratia: integration of quorum sensing with multiple new regulatory components in the control of prodigiosin and carbapenem antibiotic production. Mol. Microbiol. 56:1495–1517.
    OpenUrlCrossRefPubMedWeb of Science
  7. 7.↵
    1. Slater H,
    2. Crow M,
    3. Everson L,
    4. Salmond GP
    . 2003. Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways. Mol. Microbiol. 47:303–320.
    OpenUrlCrossRefPubMedWeb of Science
  8. 8.↵
    1. Thomson NR,
    2. Crow MA,
    3. McGowan SJ,
    4. Cox A,
    5. Salmond GP
    . 2000. Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol. Microbiol. 36:539–556.
    OpenUrlCrossRefPubMedWeb of Science
  9. 9.↵
    1. Fineran PC,
    2. Williamson NR,
    3. Lilley KS,
    4. Salmond GP
    . 2007. Virulence and prodigiosin antibiotic biosynthesis in Serratia are regulated pleiotropically by the GGDEF/EAL domain protein, PigX. J. Bacteriol. 189:7653–7662.
    OpenUrlAbstract/FREE Full Text
  10. 10.↵
    1. Williamson NR,
    2. Fineran PC,
    3. Ogawa W,
    4. Woodley LR,
    5. Salmond GP
    . 2008. Integrated regulation involving quorum sensing, a two-component system, a GGDEF/EAL domain protein and a post-transcriptional regulator controls swarming and RhlA-dependent surfactant biosynthesis in Serratia. Environ. Microbiol. 10:1202–1217.
    OpenUrlCrossRefPubMed
  11. 11.↵
    1. Gristwood T,
    2. Fineran PC,
    3. Everson L,
    4. Williamson NR,
    5. Salmond GP
    . 2009. The PhoBR two-component system regulates antibiotic biosynthesis in Serratia in response to phosphate. BMC Microbiol. 9:112.
    OpenUrlCrossRefPubMed
  12. 12.↵
    1. Fineran PC,
    2. Everson L,
    3. Slater H,
    4. Salmond GP
    . 2005. A GntR family transcriptional regulator (PigT) controls gluconate-mediated repression and defines a new, independent pathway for regulation of the tripyrrole antibiotic, prodigiosin, in Serratia. Microbiology 151:3833–3845.
    OpenUrlCrossRefPubMedWeb of Science
  13. 13.↵
    1. Wilf NM,
    2. Williamson NR,
    3. Ramsay JP,
    4. Poulter S,
    5. Bandyra KJ,
    6. Salmond GP
    . 2011. The RNA chaperone, Hfq, controls two luxR-type regulators and plays a key role in pathogenesis and production of antibiotics in Serratia sp. ATCC 39006. Environ. Microbiol. 13:2649–2666.
    OpenUrlPubMed
  14. 14.↵
    1. Wilf NM,
    2. Salmond GP
    . 2012. The stationary phase sigma factor, RpoS, regulates the production of a carbapenem antibiotic, a bioactive prodigiosin and virulence in the enterobacterial pathogen Serratia sp. ATCC 39006. Microbiology 158:648–658.
    OpenUrlCrossRefPubMedWeb of Science
  15. 15.↵
    1. Gristwood T,
    2. Fineran PC,
    3. Everson L,
    4. Salmond GP
    . 2008. PigZ, a TetR/AcrR family repressor, modulates secondary metabolism via the expression of a putative four-component resistance-nodulation-cell-division efflux pump, ZrpADBC, in Serratia sp. ATCC 39006. Mol. Microbiol. 69:418–435.
    OpenUrlCrossRefPubMed
  16. 16.↵
    1. Gristwood T,
    2. McNeil MB,
    3. Clulow JS,
    4. Salmond GP,
    5. Fineran PC
    . 2011. PigS and PigP regulate prodigiosin biosynthesis in Serratia via differential control of divergent operons, which include predicted transporters of sulfur-containing molecules. J. Bacteriol. 193:1076–1085.
    OpenUrlAbstract/FREE Full Text
  17. 17.↵
    1. McNeil MB,
    2. Clulow JS,
    3. Wilf NM,
    4. Salmond GP,
    5. Fineran PC
    . 2012. SdhE is a conserved protein required for flavinylation of succinate dehydrogenase in bacteria. J. Biol. Chem. 287:18418–18428.
    OpenUrlAbstract/FREE Full Text
  18. 18.↵
    1. McNeil MB,
    2. Iglesias-Cans MC,
    3. Clulow JS,
    4. Fineran PC
    . 2013. YgfX (CptA) is a multimeric membrane protein that interacts with the succinate dehydrogenase assembly factor SdhE (YgfY). Microbiology 159:1352–1365.
    OpenUrlCrossRefPubMedWeb of Science
  19. 19.↵
    1. McNeil MB,
    2. Fineran PC
    . 2013. Prokaryotic assembly factors for the attachment of flavin to complex II. Biochim. Biophys. Acta 1827:637–647.
    OpenUrlCrossRefPubMed
  20. 20.↵
    1. McNeil MB,
    2. Fineran PC
    . 2013. The conserved RGxxE motif of the bacterial FAD Assembly factor SdhE is required for succinate dehydrogenase flavinylation and activity. Biochemistry 52:7628–7640.
    OpenUrlCrossRefPubMed
  21. 21.↵
    1. Ramsay JP,
    2. Williamson NR,
    3. Spring DR,
    4. Salmond GP
    . 2011. A quorum-sensing molecule acts as a morphogen controlling gas vesicle organelle biogenesis and adaptive flotation in an enterobacterium. Proc. Natl. Acad. Sci. U. S. A. 108:14932–14937.
    OpenUrlAbstract/FREE Full Text
  22. 22.↵
    1. Coulthurst SJ,
    2. Kurz CL,
    3. Salmond GP
    . 2004. luxS mutants of Serratia defective in autoinducer-2-dependent “quorum sensing” show strain-dependent impacts on virulence and production of carbapenem and prodigiosin. Microbiology 150:1901–1910.
    OpenUrlCrossRefPubMedWeb of Science
  23. 23.↵
    1. Evans TJ,
    2. Crow MA,
    3. Williamson NR,
    4. Orme W,
    5. Thomson NR,
    6. Komitopoulou E,
    7. Salmond GP
    . 2010. Characterization of a broad-host-range flagellum-dependent phage that mediates high-efficiency generalized transduction in, and between, Serratia and Pantoea. Microbiology 156:240–247.
    OpenUrlCrossRefPubMed
  24. 24.↵
    1. McKenna A,
    2. Hanna M,
    3. Banks E,
    4. Sivachenko A,
    5. Cibulskis K,
    6. Kernytsky A,
    7. Garimella K,
    8. Altshuler D,
    9. Gabriel S,
    10. Daly M,
    11. DePristo MA
    . 2010. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20:1297–1303.
    OpenUrlAbstract/FREE Full Text
  25. 25.↵
    1. Hyatt D,
    2. Chen GL,
    3. Locascio PF,
    4. Land ML,
    5. Larimer FW,
    6. Hauser LJ
    . 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119.
    OpenUrlCrossRefPubMed
View Abstract
PreviousNext
Back to top
Download PDF
Citation Tools
Draft Genome Sequence of Serratia sp. Strain ATCC 39006, a Model Bacterium for Analysis of the Biosynthesis and Regulation of Prodigiosin, a Carbapenem, and Gas Vesicles
Peter C. Fineran, Marina C. Iglesias Cans, Joshua P. Ramsay, Nabil M. Wilf, Desiree Cossyleon, Matthew B. McNeil, Neil R. Williamson, Rita E. Monson, S. Anette Becher, Jo-Ann L. Stanton, Kim Brügger, Steven D. Brown, George P. C. Salmond
Genome Announcements Dec 2013, 1 (6) e01039-13; DOI: 10.1128/genomeA.01039-13

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print
Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Microbiology Resource Announcements article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Draft Genome Sequence of Serratia sp. Strain ATCC 39006, a Model Bacterium for Analysis of the Biosynthesis and Regulation of Prodigiosin, a Carbapenem, and Gas Vesicles
(Your Name) has forwarded a page to you from Microbiology Resource Announcements
(Your Name) thought you would be interested in this article in Microbiology Resource Announcements.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Draft Genome Sequence of Serratia sp. Strain ATCC 39006, a Model Bacterium for Analysis of the Biosynthesis and Regulation of Prodigiosin, a Carbapenem, and Gas Vesicles
Peter C. Fineran, Marina C. Iglesias Cans, Joshua P. Ramsay, Nabil M. Wilf, Desiree Cossyleon, Matthew B. McNeil, Neil R. Williamson, Rita E. Monson, S. Anette Becher, Jo-Ann L. Stanton, Kim Brügger, Steven D. Brown, George P. C. Salmond
Genome Announcements Dec 2013, 1 (6) e01039-13; DOI: 10.1128/genomeA.01039-13
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • GENOME ANNOUNCEMENT
    • ACKNOWLEDGMENTS
    • FOOTNOTES
    • REFERENCES
  • Info & Metrics
  • PDF

Related Articles

Cited By...

About

  • About MRA
  • Editor in Chief
  • Board of Editors
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • Getting Started
  • Submit a Manuscript
  • Author Warranty
  • Ethics
  • Contact Us
  • ASM Author Center

Follow #MRAJournal

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

Online ISSN: 2576-098X