Diverse profiles of N-acyl-homoserine lactone molecules found in cnidarians

FEMS Microbiology Ecology

Volumn 87, Issue 2, 2014, Pages 315-329

  Ransome, Emma ^a,b   Munn, Colin B ^b   Halliday, Nigel ^c   Cámara, Miguel ^c   Tait, Karen ^a  

^a PLYMOUTH MARINE LABORATORY   (United Kingdom)

^b UNIVERSITY OF PLYMOUTH   (United Kingdom)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Autoinducers; Coral microbiology; DGGE; LC MS MS; Microbial regulation; Sea anemone

Indexed keywords

BACTERIAL RNA; GAMMA BUTYROLACTONE DERIVATIVE; RNA 16S;

ANIMAL; ARTICLE; AUTOINDUCERS; BACTERIUM; CNIDARIA; CORAL MICROBIOLOGY; DGGE; GENETICS; LC-MS/MS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MICROBIAL REGULATION; MICROBIOLOGY; QUORUM SENSING; SEA ANEMONE; THIN LAYER CHROMATOGRAPHY;

AUTOINDUCERS; CORAL MICROBIOLOGY; DGGE; LC-MS/MS; MICROBIAL REGULATION; SEA ANEMONE;

ACYL-BUTYROLACTONES; ANIMALS; BACTERIA; CHROMATOGRAPHY, LIQUID; CHROMATOGRAPHY, THIN LAYER; CNIDARIA; MASS SPECTROMETRY; QUORUM SENSING; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S;

EID: 84895075193     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12226     Document Type: Article

References (75)

1. Ainsworth TD & Hoegh-Guldberg O (2009) Bacterial communities closely associated with coral reef tissues vary under experimental and natural reef conditions and thermal stress. Aquat Biol 4: 289-296.
2. Alagely A, Krediet CJ, Ritchie KB & Teplitski M (2011) Signalling-mediated-cross-talk modulates swarming and biofilm formation in a coral pathogens Serratia marcescens. ISME J 5: 1609-1620.
3. Azam F & Worden A (2004) Oceanography: microbes, molecules, and marine ecosystems. Science 12: 1622-1624.
4. Bourne D & Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7: 1162-1174.
5. Bourne D, Iida Y, Uthicke S & Smith-Keune C (2008) Changes in coral-associated microbial communities during a bleaching event. ISME J 2: 350-363.
6. Clarke KR & Gorley RN (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E Plymouth.
7. Decho AW, Visscher PT, Ferry J, Kawaguchi T, He L, Przekop KM, Norman RS & Reid RP (2009) Autoinducers extracted from microbial mats reveal a surprising diversity of N-acyl-homoserine lactones (AHLs) and abundance changes that may relate to diel pH. Environ Microbiol 11: 409-420.
8. Diggle SP, Crusz SA & Cámara M (2007) Quorum sensing. Curr Biol 17: R907-R910.
9. Dobretsov S, Dahms HU, Yili H, Wahl M & Qian PY (2007) The effect of quorum sensing blockers on the formation of marine microbial communities and larval attachment. FEMS Microbiol Ecol 60: 177-188.
10. Dobretsov S, Teplitski M & Paul V (2009) Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25: 413-427.
11. Duerkop BA, Varga J, Chandler JR, Peterson SB, Herman JP, Churchill MEA, Parsek MR, Nierman WC & Greenberg EP (2009) Quorum-sensing control of antibiotic synthesis in Burkholderia thailandensis. J Bacteriol 191: 3909-3918.
12. Dunne M (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15: 155-166.
13. Fuqua C & Greenberg EP (2002) Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3: 685-695.
14. Fuqua C & Winans SC (1996) Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes. J Bacteriol 178: 435-444.
15. Givskov M, de Nys R, Manefeld M, Gram L, Maximilien R, Eberl L, Molin S, Steinberg PD & Kjelleberg S (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J Bacteriol 178: 6618-6622.
16. Golberg K, Eltzov E, Shnit-Orland M, Marks RS & Kushmaro A (2011) Characterization of quorum sensing signals in coral-associated bacteria. Microb Ecol 61: 783-792.
17. Gram L, Grossart HP, Schlingloff A & Kiørboe T (2002) Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl Environ Microbiol 68: 4111-4116.
18. Hasegawa H, Chatterjee A, Cui Y & Chatterjee AK (2005) Elevated temperature enhances virulence of Erwinia carotovora subsp. carotovora strain EC153 to plants and stimulates production of the quorum sensing signal, N-acyl homoserine lactone, and extracellular proteins. Appl Environ Microbiol 71: 4655-4663.
19. Hmelo L & Van Mooy BAS (2009) Kinetic constraints on acylated homoserine lactone-based quorum sensing in marine environments. Aquat Microb Ecol 54: 127-133.
20. Horswill AR, Stoodlet P, Stewart PS & Parsek MR (2007) The effect of the chemical, biological and physical environment on quorum sensing in structured microbial communities. Anal Bioanal Chem 387: 371-380.
21. Huang YL, Dobretsov S, Ki JS, Yang LH & Qian PY (2007) Presence of acyl-homoserine lactone in subtidal biofilm and the implication in larval behavioural response in the polychaete Hydroides elegans. Microb Ecol 54: 384-392.
22. Huang Y, Ki JS, Case RJ & Qian PY (2008) Diversity and acyl-homoserine lactone production among subtidal biofilm-forming bacteria. Aquat Microb Ecol 52: 185-193.
23. Hunt LR, Smith SM, Downum KR & Mydlarz LD (2012) Microbial regulation in gorgonian corals. Mar Drugs 10: 1225-1243.
24. Joint I, Tait K, Callow ME, Callow JA, Milton D, Williams P & Cámara M (2002) Cell-to-cell communication across the Prokaryotic-Eukaryotic boundary. Science 298: 1207.
25. Karthikeyan MM, Ananthan G & Balasubramanian T (2009) Antimicrobial activity of crude extracts of some Ascidians (Urochordata: Ascidiacea) from Palk Strait, (Southeast Coast of India). World J Fish Mar Sci 1: 262-267.
26. Knowlton N & Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 164 (suppl 4): S51-S62.
27. Kurahashi M & Yokota A (2006) Endozoicomonas elysicola gen. nov., sp. nov., a γ-proteobacterium isolated from the sea slug Elysia ornata. Syst Appl Microbiol 30: 202-206.
28. Kvennefors EC, Sampayo E, Kerr C, Vieira G, Roff G & Barnes AC (2012) Regulation of bacterial communities through antimicrobial activity in the coral holobiont. Microb Ecol 63: 605-618.
29. Latour X, Diallo S, Chevalier S, Morin D, Smadja B, Burini J, Haras D & Orange N (2007) Thermoregulation of N-acyl homoserine lactone-based quorum sensing in the soft rot bacterium Pectobacterium atrosepticum. Appl Environ Microbiol 73: 4078-4081.
30. Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 300: 217-252.
31. Littman R, Willis B, Pfeffer C & Bourne D (2009) Diversities of coral-associated bacteria differ with location, but not species, for three acroporid corals on the Great Barrier Reef. FEMS Microbiol Ecol 68: 152-163.
32. Martínez-Garcia M, Díaz-Valdés M, Wanner G, Ramos-Esplá A & Antón J (2007) Microbial community associated with the colonial ascidian Cystodytes dellechiajei. Environ Microbiol 9: 521-534.
33. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollés G, Rolfe BG & Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. P Natl Acad Sci USA 100: 1444-1449.
34. Miller M, Skorupski K, Lenz D, Taylor R & Bassler B (2002) Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110: 303-314.
35. Mohamed NM, Cicirelli EM, Kan J, Chen F, Fuqua C & Hill RT (2008) Diversity and quorum-sensing signal production of Proteobacteria associated with marine sponges. Environ Microbiol 10: 75-86.
36. Mouchka ME, Hewson I & Harvell CD (2010) Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol 50: 662-674.
37. Mühling M, Woolven-Allen J, Murrell JC & Joint I (2008) Improved group-specific PCR primers for denaturing gradient gel electrophoresis analysis of the genetic diversity of complex microbial communities. ISME J 2: 379-392.
38. Nissimov J, Rosenberg E & Munn CB (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 292: 210-215.
39. Ortori CA, Dubern J-F, Chhabra SR, Cámara M, Hardie K, Williams P & Barrett DA (2011) Simultaneous quantitative profiling of N-acyl-L-homoserine lactone and 2-alkyl-4(1H)-quinolone families of quorum-sensing signalling molecules using LC-MS/MS. Anal Bioanal Chem 399: 839-850.
40. Raina J, Tapiolas D, Willis BL & Bourne DG (2009) Coral-associated bacteria and their role in biogeochemical cycling of sulphur. Appl Environ Microbiol 75: 3492-3501.
41. Rasmussen TB, Manefield M, Andersen JB, Eberl L, Anthoni U, Christophersen C, Steinberg P, Kjelleberg S & Givskov M (2000) How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology 146: 3237-3244.
42. Rice SA, Koh KS, Queck SY, Labbate M, Lam KW & Kjelleberg S (2005) Biofilm formation and sloughing in Serratia marcescens are controlled by quorum sensing and nutrient cues. J Bacteriol 187: 3477-3485.
43. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322: 1-14.
44. Ritchie KB & Smith GW (1997) Physiological comparison of bacterial communities from various species of scleractinian corals. Proc 8th Int Coral Reef Symp 1: 521-526.
45. Rohwer F, Breitbart M, Jara J, Azam F & Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20: 85-91.
46. Rohwer F, Seguritan V, Azam F & Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243: 1-10.
47. Romero M, Avendaño-Herrera R, Magariños B, Cámara M & Otero A (2011) Acyl homoserine lactone production and degradation by the fish pathogen Tenacibaculum maritimum, a member of the Cytophaga-Flavobacterium-Bacteroides (CFB) division. FEMS Microbiol Lett 304: 131-139.
48. Romero M, Martin-Cuadrado A, Roca-Rivada A, Cabello AM & Otero A (2011) Quorum quenching in cultivable bacteria from dense marine coastal microbial communities. FEMS Microbiol Ecol 75: 205-217.
49. Ruby EG & Lee KH (1998) The Vibrio fischeri-Euprymna scolopes light organ association: current ecological paradigms. Appl Environ Microbiol 64: 805-812.
50. Schaefer AL, Taylor TA, Beatty JT & Greenberg EP (2002) Long-chain Acyl-homoserine lactone quorum-sensing regulation of Rhodobacter capsulatus gene transfer agent production. J Bacteriol 184: 6515-6521.
51. Schuett C, Doepke H, Grathoff A & Gedde M (2007) Bacterial aggregates in the tentacles of the sea anemone Metridium senile. Helgol. Mar Res 61: 211-216.
52. Sharif DI, Gallo J, Smith CJ & Dudley E (2008) Quorum sensing in Cyanobacteria: N-octanoyl-homoserine lactone release and response, by the epilithic colonial cyanobacterium Gloeothece PCC6909. ISME J 2: 1171-1182.
53. Sharp KH, Distel D & Paul VJ (2011) Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME J 6: 790-801.
54. Shaw PD, Ping G, Daly SL, Cha C, Cronan JE, Rinehart KL & Farrand SK (1997) Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. P Natl Acad Sci USA 94: 6036-6041.
55. Shnit-Orland M & Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defence. FEMS Microbiol Ecol 67: 371-380.
56. Skindersoe ME, Ettinger-Epstein P, Rasmussen TB, Bjarnsholt T, De Nys R & Givskov M (2008) Quorum sensing antagonism from marine organisms. Mar Biotechnol 10: 56-63.
57. Tait K & Havenhand J (2013) Investigating a possible role for the bacterial signal molecules N-acylhomoserine lactones in Balanus improvisus cyprid settlement. Mol Ecol 22: 2588-2602.
58. Tait K, Joint I, Daykin M, Milton DL, Williams P & Cámara M (2005) Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms. Environ Microbiol 7: 229-240.
59. Tait K, Williamson H, Atkinson S, Williams P, Cámara M & Joint I (2009) Turnover of quorum sensing signal molecules modulates cross-kingdom signalling. Environ Microbiol 11: 1792-1802.
60. Tait K, Hutchinson Z, Thompson FL & Munn CB (2010) Quorum sensing signal production and inhibition by coral-associated vibrios. Environ Microbiol Rep 2: 145-150.
61. Tamura K, Dudley J, Nei M & Kumar S (2007) MEGA 4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
62. Taylor MW, Schupp PJ, Baillie HJ, Charlton TS, de Nys R, Kjelleberg S & Steinberg PD (2004) Evidence for acyl homoserine lactone signal production in bacteria associated with marine sponges. Appl Environ Microbiol 70: 4387-4389.
63. Teplitski M & Ritchie K (2009) How feasible is the biological control of coral diseases? Trends Ecol Evol 24: 378-385.
64. Thakur NL, Thakur NL, Indap MM, Pandit RA, Datar VV & Müller WEG (2004) Antiangiogenic, antimicrobial, and cytotoxic potential of sponge-associated bacteria. Mar Biotech 7: 245-252.
65. Thenmozhi R, Nithyanand P, Rathna J & Pandian SK (2009) Antibiofilm activity of coral-associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunol Med Microbiol 57: 284-294.
66. Twigg MS, Tait K, Williams P, Atkinson S & Cámara M (2013) Interference with the germination and growth of Ulva zoospores by quorum sensing molecules produced by Ulva-associated epiphytic bacteria. Environ Microbiol DOI: 10.1111/1462-2920.12203. [Epub ahead of print].
67. Valle A, Bailey MJ, Whiteley AS & Manefield M (2004) N-acyl-L-homoserine lactones (AHLs) affect microbial community composition and function in activated sludge. Environ Microbiol 6: 424-433.
68. Wagner-Döbler I, Thiel V, Eberl L, Allgaier M, Bodor A, Meyer S, Ebner S, Hennig A, Pukall R & Schulz S (2005) Discovery of complex mixtures of novel long-chain quorum sensing signals in free-living and host-associated marine alphaproteobacteria. ChemBioChem 6: 2195-2206.
69. Weinberger F, Beltran J, Correa JA, Lion U, Pohnert G, Kumar N, Steinberg P, Kloareg B & Potin P (2007) Spore release in Acrochaetium sp. (Rhodophyta) is bacterially controlled. J Phycol 43: 235-241.
70. Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M & Pringle JR (2008) Cell biology in model systems as the key to understanding corals. Trends Ecol Evol 23: 369-376.
71. Williams P (2007) Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 153: 3923-3938.
72. Williams P, Camara M, Hardman A, Swift S, Milton D, Hope VL, Winzer K, Middleton B, Pritchard DI & Bycroft BW (2000) Quorum sensing and the population-dependent control of virulence. Philos Trans R Soc Lond B Biol Sci 355: 667-680.
73. Yang CS, Chen MH, Arun AB, Chen CA, Wang JT & Chen EM (2010) Endozoicomonas montiporae sp. nov., isolated from the encrusting pore coral Montipora aequituberculata. Int J Syst Evol Microbiol 60: 1158-1162.
74. Yates EA, Philipp B, Buckley C et al. (2002) N-acylhomoserine lactones undergo lactonlysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect Immun 70: 5635-5646.
75. Zhu J & Mekalanos JJ (2003) Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5: 647-656.