Home LiteratureArticle Details
PMID: 22582055 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Production of the antimicrobial secondary metabolite indigoidine contributes to competitive surface colonization by the marine roseobacter Phaeobacter sp. strain Y4I.

Applied and environmental microbiology ·Vol. 78 ·No. 14 ·2012-07-00 ·Pages 4771-80

Cude WN, Mooney J, Tavanaei AA, Hadden MK, Frank AM, Gulvik CA, May AL, Buchan A

Abstract

Members of the Roseobacter lineage of marine bacteria are prolific surface colonizers in marine coastal environments, and antimicrobial secondary metabolite production has been hypothesized to provide a competitive advantage to colonizing roseobacters. Here, we report that the roseobacter Phaeobacter sp. strain Y4I produces the blue pigment indigoidine via a nonribosomal peptide synthase (NRPS)-based biosynthetic pathway encoded by a novel series of genetically linked genes: igiBCDFE. A Tn5-based random mutagenesis library of Y4I showed a perfect correlation between indigoidine production by the Phaeobacter strain and inhibition of Vibrio fischeri on agar plates, revealing a previously unrecognized bioactivity of this molecule. In addition, igiD null mutants (igiD encoding the indigoidine NRPS) were more resistant to hydrogen peroxide, less motile, and faster to colonize an artificial surface than the wild-type strain. Collectively, these data provide evidence for pleiotropic effects of indigoidine production in this strain. Gene expression assays support phenotypic observations and demonstrate that igiD gene expression is upregulated during growth on surfaces. Furthermore, competitive cocultures of V. fischeri and Y4I show that the production of indigoidine by Y4I significantly inhibits colonization of V. fischeri on surfaces. This study is the first to characterize a secondary metabolite produced by an NRPS in roseobacters.

MeSH Terms
Aliivibrio fischeri/drug effects,growth & development,physiology Anti-Infective Agents/chemistry,isolation & purification,metabolism,pharmacology Antibiosis Bacterial Proteins/genetics,metabolism DNA Transposable Elements Gene Expression Regulation, Bacterial Gene Library Microbial Sensitivity Tests Mutation Peptide Synthases/genetics,metabolism Piperidones/chemistry,isolation & purification,metabolism,pharmacology Rhodobacteraceae/genetics,isolation & purification,metabolism,physiology Roseobacter/classification,genetics,metabolism,physiology Seawater/microbiology
Chemicals
Anti-Infective Agents Bacterial Proteins DNA Transposable Elements Piperidones indigoidine Peptide Synthases non-ribosomal peptide synthase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Cude W Nathan
Department of Microbiology, University of Tennessee, Knoxville, TN, USA.
Mooney Jason
Tavanaei Arash A
Hadden Mary K
Frank Ashley M
Gulvik Christopher A
May Amanda L
Buchan Alison
References (58)
58 references, click to expand
  1. Formation of the blue pigment indigoidine by phytopathogenic erwinia.
    Appl Microbiol. 1966 Nov;14(6):870-2 PMID: 16349687
  2. Surface attachment induced production of antimicrobial compounds by marine epiphytic bacteria using modified roller bottle cultivation.
    Mar Biotechnol (NY). 2002 Sep;4(4):356-66 PMID: 14961247
  3. Roseobacter algicola sp. nov., a new marine bacterium isolated from the phycosphere of the toxin-producing dinoflagellate Prorocentrum lima.
    Int J Syst Bacteriol. 1995 Apr;45(2):290-6 PMID: 7537061
  4. INDIGOIDINE AND OTHER BACTERIAL PIGMENTS RELATED TO 3,3'-BIPYRIDYL.
    Arch Mikrobiol. 1965 May 28;51:71-84 PMID: 14347925
  5. A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli.
    J Gen Microbiol. 1973 Jan;74(1):77-91 PMID: 4632978
  6. Bacteria of the Roseobacter clade show potential for secondary metabolite production.
    Microb Ecol. 2007 Jul;54(1):31-42 PMID: 17351813
  7. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankiabacteria.
    Proc Natl Acad Sci U S A. 2008 Mar 25;105(12):4928-32 PMID: 18316735
  8. Chemotaxis in bacteria.
    Science. 1966 Aug 12;153(3737):708-16 PMID: 4957395
  9. The biosynthesis and regulation of bacterial prodiginines.
    Nat Rev Microbiol. 2006 Dec;4(12):887-99 PMID: 17109029
  10. Quorum sensing, virulence and secondary metabolite production in plant soft-rotting bacteria.
    Philos Trans R Soc Lond B Biol Sci. 2007 Jul 29;362(1483):1165-83 PMID: 17360277
  11. Diversity, ecology, and genomics of the Roseobacter clade: a short overview.
    Arch Microbiol. 2008 Jun;189(6):531-9 PMID: 18253713
  12. Bacterial motility on a surface: many ways to a common goal.
    Annu Rev Microbiol. 2003;57:249-73 PMID: 14527279
  13. Tropodithietic acid production in Phaeobacter gallaeciensis is regulated by N-acyl homoserine lactone-mediated quorum sensing.
    J Bacteriol. 2011 Dec;193(23):6576-85 PMID: 21949069
  14. Selection and evaluation of reference genes for improved interrogation of microbial transcriptomes: case study with the extremophile Acidithiobacillus ferrooxidans.
    BMC Mol Biol. 2009 Jun 25;10:63 PMID: 19555508
  15. Diverse organization of genes of the beta-ketoadipate pathway in members of the marine Roseobacter lineage.
    Appl Environ Microbiol. 2004 Mar;70(3):1658-68 PMID: 15006791
  16. Genetic dissection of tropodithietic acid biosynthesis by marine roseobacters.
    Appl Environ Microbiol. 2008 Mar;74(5):1535-45 PMID: 18192410
  17. Antibacterial activity of marine culturable bacteria collected from a global sampling of ocean surface waters and surface swabs of marine organisms.
    Mar Biotechnol (NY). 2010 Aug;12(4):439-51 PMID: 19823914
  18. Bacterial biofilms in nature and disease.
    Annu Rev Microbiol. 1987;41:435-64 PMID: 3318676
  19. Culture conditions of Roseobacter strain 27-4 affect its attachment and biofilm formation as quantified by real-time PCR.
    Appl Environ Microbiol. 2006 Apr;72(4):3011-5 PMID: 16598009
  20. Surface colonization by marine roseobacters: integrating genotype and phenotype.
    Appl Environ Microbiol. 2009 Oct;75(19):6027-37 PMID: 19666726
  21. Ecology, inhibitory activity, and morphogenesis of a marine antagonistic bacterium belonging to the Roseobacter clade.
    Appl Environ Microbiol. 2005 Nov;71(11):7263-70 PMID: 16269767
  22. Production of antibacterial compounds and biofilm formation by Roseobacter species are influenced by culture conditions.
    Appl Environ Microbiol. 2007 Jan;73(2):442-50 PMID: 17098910
  23. Phaeobacter and Ruegeria species of the Roseobacter clade colonize separate niches in a Danish Turbot (Scophthalmus maximus)-rearing farm and antagonize Vibrio anguillarum under different growth conditions.
    Appl Environ Microbiol. 2008 Dec;74(23):7356-64 PMID: 18952864
  24. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis.
    Nat Chem. 2011 Apr;3(4):331-5 PMID: 21430694
  25. Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes.
    Appl Microbiol Biotechnol. 2010 May;86(6):1659-70 PMID: 20352425
  26. Expression of tropodithietic acid biosynthesis is controlled by a novel autoinducer.
    J Bacteriol. 2010 Sep;192(17):4377-87 PMID: 20601479
  27. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data.
    Genome Biol. 2007;8(2):R19 PMID: 17291332
  28. Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition.
    J Bacteriol. 2011 Jul;193(14):3606-17 PMID: 21602354
  29. Production of microbial secondary metabolites: regulation by the carbon source.
    Crit Rev Microbiol. 2010 May;36(2):146-67 PMID: 20210692
  30. Phaeobacter caeruleus sp. nov., a blue-coloured, colony-forming bacterium isolated from a marine electroactive biofilm.
    Int J Syst Evol Microbiol. 2009 May;59(Pt 5):1209-14 PMID: 19406821
  31. Inactivation of Vibrio anguillarum by attached and planktonic Roseobacter cells.
    Appl Environ Microbiol. 2010 Apr;76(7):2366-70 PMID: 20118354
  32. Genome characteristics of a generalist marine bacterial lineage.
    ISME J. 2010 Jun;4(6):784-98 PMID: 20072162
  33. Roseobacter gallaeciensis sp. nov., a new marine bacterium isolated from rearings and collectors of the scallop Pecten maximus.
    Int J Syst Bacteriol. 1998 Apr;48 Pt 2:537-42 PMID: 9731295
  34. Key aromatic-ring-cleaving enzyme, protocatechuate 3,4-dioxygenase, in the ecologically important marine Roseobacter lineage.
    Appl Environ Microbiol. 2000 Nov;66(11):4662-72 PMID: 11055908
  35. Leucoindigoidine formation by an Arthrobacter species and its oxidation to indigoidine by other micro-organisms.
    Biochim Biophys Acta. 1968 Mar 11;156(2):429-31 PMID: 4868094
  36. Antagonistic activity of bacteria isolated from organic aggregates of the German Wadden Sea.
    FEMS Microbiol Ecol. 2004 Mar 1;47(3):387-96 PMID: 19712327
  37. Phaeobacter daeponensis sp. nov., isolated from a tidal flat of the Yellow Sea in Korea.
    Int J Syst Evol Microbiol. 2007 Apr;57(Pt 4):856-861 PMID: 17392219
  38. Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes.
    Proc Natl Acad Sci U S A. 1990 May;87(9):3513-7 PMID: 2185473
  39. Biofilm formation as microbial development.
    Annu Rev Microbiol. 2000;54:49-79 PMID: 11018124
  40. Competitive induction and enhancement of indole and a diketopiperazine in marine bacteria.
    Mar Biotechnol (NY). 2004 May-Jun;6(3):215-20 PMID: 15136911
  41. pecS: a locus controlling pectinase, cellulase and blue pigment production in Erwinia chrysanthemi.
    Mol Microbiol. 1994 Mar;11(6):1127-39 PMID: 8022282
  42. Phenazines affect biofilm formation by Pseudomonas aeruginosa in similar ways at various scales.
    Res Microbiol. 2010 Apr;161(3):187-91 PMID: 20123017
  43. Genetic approaches to study of biofilms.
    Methods Enzymol. 1999;310:91-109 PMID: 10547784
  44. Antagonistic interactions among coral-associated bacteria.
    Environ Microbiol. 2010 Jan;12(1):28-39 PMID: 19691500
  45. Selection and identification of autochthonous potential probiotic bacteria from turbot larvae (Scophthalmus maximus) rearing units.
    Syst Appl Microbiol. 2004 May;27(3):360-71 PMID: 15214642
  46. Bacterial primary colonization and early succession on surfaces in marine waters as determined by amplified rRNA gene restriction analysis and sequence analysis of 16S rRNA genes.
    Appl Environ Microbiol. 2000 Feb;66(2):467-75 PMID: 10653705
  47. Cross-ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters.
    Appl Environ Microbiol. 2008 Jan;74(1):52-60 PMID: 17965206
  48. Characterization of indigoidine biosynthetic genes in Erwinia chrysanthemi and role of this blue pigment in pathogenicity.
    J Bacteriol. 2002 Feb;184(3):654-65 PMID: 11790734
  49. Environmental biology of the marine Roseobacter lineage.
    Annu Rev Microbiol. 2006;60:255-80 PMID: 16719716
  50. The two-component, ATP-dependent Clp protease of Escherichia coli. Purification, cloning, and mutational analysis of the ATP-binding component.
    J Biol Chem. 1988 Oct 15;263(29):15226-36 PMID: 3049606
  51. Microbial colonization and competition on the marine alga Ulva australis.
    Appl Environ Microbiol. 2006 Aug;72(8):5547-55 PMID: 16885308
  52. Additional evidence that juvenile oyster disease is caused by a member of the Roseobacter group and colonization of nonaffected animals by Stappia stellulata-like strains.
    Appl Environ Microbiol. 2000 Sep;66(9):3924-30 PMID: 10966410
  53. Bacterial biofilms: a common cause of persistent infections.
    Science. 1999 May 21;284(5418):1318-22 PMID: 10334980
  54. Cloning and characterization of a Streptomyces single module type non-ribosomal peptide synthetase catalyzing a blue pigment synthesis.
    J Biol Chem. 2007 Mar 23;282(12):9073-81 PMID: 17237222
  55. Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria.
    Arch Microbiol. 2002 Sep;178(3):193-201 PMID: 12189420
  56. Antibiotic production by a Roseobacter clade-affiliated species from the German Wadden Sea and its antagonistic effects on indigenous isolates.
    Appl Environ Microbiol. 2004 Apr;70(4):2560-5 PMID: 15066861
  57. Overview of the marine roseobacter lineage.
    Appl Environ Microbiol. 2005 Oct;71(10):5665-77 PMID: 16204474
  58. Antagonistic interactions among marine pelagic bacteria.
    Appl Environ Microbiol. 2001 Nov;67(11):4975-83 PMID: 11679315
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
1098-5336
DOI
10.1128/AEM.00297-12
Published
2012-07-00
Epub
2012-00-11
Pages
4771-80
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC3416362
Subset
IM
External Links
PubMed source DOI: 10.1128/AEM.00297-12 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