Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter April 20, 2016

In vitro evaluation of indole-3-carboxaldehyde on Vibrio parahaemolyticus biofilms

  • Murugan Rajalaxmi , Vivekanandham Amsa Devi and Shunmugiah Karutha Pandian EMAIL logo
From the journal Biologia


This study was aimed to explore antibiofilm agents from the hitherto underexplored Palk Bay seawater bacteria. The cell free culture supernatant of the isolate Marinomonas sp. showed profound antibiofilm activity against Vibrio parahaemolyticus ATCC 17802. The active principle responsible for antibiofilm activity was identified as indole-3-carboxaldehyde (ICA) after bioassay guided purification and gas chromatography-mass spectrometry analysis. Further, in vitro antibiofilm activity of ICA was confirmed through light microscopy, confocal imaging, scanning electron microscopy and biofilm disruption studies. In addition, ICA efficiently reduced the swarming motility of the pathogen and promoted the swimming ability. Furthermore, the control of biofilms and swarming efficiency by quorum sensing pathway of the pathogen was modulated by ICA, which was substantiated using real-time analysis for opaR, cpsA, and lafA genes. This study divulged the efficacy of ICA as an antibiofilm agent against V. parahaemolyticus in vitro.


The authors thankfully acknowledge the Bioinformatics Infrastructure Facility funded by Department of Biotechnology, Government of India [Grant No. BT/BI/25/012/2012 (BIF)], the instrumentation facility provided by Department of Science and Technology, Government of India through PURSE [Grant No.SR/S9Z-23/2010/42 (G)] & FIST (Grant No.SR-FST/LSI-087/2008), and University Grants Commission, New Delhi, through SAP-DRS1 [Grant No.F.328/2011 (SAP-II)].


Armstrong E., Boyd K.G. & Burgess J.G. 2000. Prevention of marine biofouling using natural compounds from marine organisms. Biotechnol. Annu. Rev. 6: 221–241.10.1016/S1387-2656(00)06024-5Search in Google Scholar

Bell R., Carmeli S. & Sar N. 1994. Vibrindole A, a metabolite of the marine bacterium Vibrio parahaemolyticus, isolated from the toxic mucus of the boxfish Ostracion cubicus.J. Nat. Prod. 57: 1587–1590.10.1021/np50113a022Search in Google Scholar PubMed

Boles B.R. & McCarter L.L. 2002. Vibrio parahaemolyticus scrABC, a novel operon affecting swarming and capsular polysaccharide regulation. J. Bacteriol. 184: 5946–5954.10.1128/JB.184.21.5946-5954.2002Search in Google Scholar PubMed PubMed Central

Broberg C.A., Calder T.J. & Orth K. 2011. Vibrio parahaemolyticus cell biology and pathogenicity determinants. Microbes Infect. 13: 992–1001.10.1016/j.micinf.2011.06.013Search in Google Scholar PubMed PubMed Central

Ceccarelli D., Hasan N.A., Huq A. & Colwell R.R. 2013. Distribution and dynamics of epidemic and pandemic Vibrio parahaemolyticus virulence factors. Front. Cell Infect. Microbiol. 3: 97–105.10.3389/fcimb.2013.00097Search in Google Scholar PubMed PubMed Central

Chowdhury G., Ghosh S., Pazhani G.P., Paul B.K., Maji D., Mukhopadhyay A.K. & Ramamurthy T. 2013. Isolation and characterization of pandemic and non pandemic strains of Vibrio parahaemolyticus from an outbreak of diarrhea in North 24 Parganas, West Bengal, India. Foodborne Pathog. Dis. 10: 338–342.10.1089/fpd.2012.1340Search in Google Scholar PubMed

Elexon N., Yay R., Nor A.M., Kantilal H.K., Ubong A., Yoshitsugu N., Nishibuchi M. & Son R. 2014. Biofilm assessment of Vibrio parahaemolyticus from seafood using random amplified polymorphism DNA-PCR. Int. Food Res. J. 21: 59–65.Search in Google Scholar

Enos-Berlage J.L., Guvener Z.T., Keenan C.E. & Mc Carter L.L. 2005. Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus. Mol. Microbiol. 55: 1160–1182.10.1111/j.1365-2958.2004.04453.xSearch in Google Scholar PubMed

Fong J.C., Karplus K., Schoolnik G.K. & Yildiz F.H. 2006. Identification and characterization of RbmA, a novel protein required for the development of rugose colony morphology and biofilm structure in Vibrio cholerae.J.Bacteriol. 188: 1049– 1059.10.1128/JB.188.3.1049-1059.2006Search in Google Scholar PubMed PubMed Central

Gowrishankar S., Poornima B. & Pandian S.K. 2014. Inhibitory efficacy of cyclo (L-leucyl-L-prolyl) from mangrove rhizosphere bacterium Bacillus amyloliquefaciens (MMS-50) towards cariogenic properties of Streptococcus mutans.Res. Microbiol. 165: 278–289.10.1016/j.resmic.2014.03.004Search in Google Scholar PubMed

Hollenbeck E.C., Fong J.C., Lim J.Y., Yildiz F.H., Fuller G.G. & Cegelski L. 2014. Molecular determinants of mechanical properties of Vibrio cholerae biofilms at the air-liquid interface. Biophys. J. 107: 2245–2252.10.1016/j.bpj.2014.10.015Search in Google Scholar PubMed PubMed Central

Kirov S.M. 2003. Bacteria that express lateral flagella enable dissection of the multifunctional roles of flagella in pathogenesis. FEMS Microbiol. Lett. 224: 151–15910.1016/S0378-1097(03)00445-2Search in Google Scholar

Kaneko T. & Colwell R.R. 1975. Adsorption of Vibrio parahaemolyticus onto chitin and copepods. Appl. Microbiol. 29: 269–274.10.1128/am.29.2.269-274.1975Search in Google Scholar PubMed PubMed Central

Lee J., Bansal T., Jayaraman A., Bentley W.E. & Wood T.K. 2007. Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl. Environ. Microbiol. 73: 4100–4109.10.1128/AEM.00360-07Search in Google Scholar PubMed PubMed Central

Lee J.H., Cho M.H. & Lee J. 2011. 3-Indolylacetonitrile decreases Escherichia coliO157:H7 biofilm formation and Pseudomonas aeruginosa virulence. Environ. Microbiol. 13: 62–73.10.1111/j.1462-2920.2010.02308.xSearch in Google Scholar PubMed

Lee J.H. & Lee J. 2010. Indole as an intercellular signal in microbial communities. FEMS Microbiol. Rev. 34: 426–444.10.1111/j.1574-6976.2009.00204.xSearch in Google Scholar PubMed

Mansson M., Gram L. & Larsen T.Q. 2011. Production of bioactive secondary metabolites by marine Vibrionaceae. Mar. Drugs 9: 1440–1468.10.3390/md9091440Search in Google Scholar PubMed PubMed Central

McCarter LL. 1998. OpaR, a homolog of Vibrio harveyi LuxR, controls opacity of Vibrio parahaemolyticus. J. Bacteriol. 180: 3166–3173.10.1128/JB.180.12.3166-3173.1998Search in Google Scholar PubMed PubMed Central

Melander R.J., Minivielle M.J. & Melander C. 2014. Controlling bacterial behavior with indole-containing natural products and derivatives. Tetrahedron 70: 6363–6372.10.1016/j.tet.2014.05.089Search in Google Scholar PubMed PubMed Central

Minivielle M.J., Bunders C.A. & Melander C. 2013. Indole/triazole conjugates are selective inhibitors and inducers of bacterial biofilms. Medchemcomm. 4: 916–919.10.1039/c3md00064hSearch in Google Scholar

Mueller R.S., Beyhan S., Saini S.G., Yildiz F.H. & Bartlett D.H. 2009. Indole acts as an extracellular cue regulating gene expression in Vibrio cholerae. J. Bacteriol. 191: 3504–3516.10.1128/JB.01240-08Search in Google Scholar PubMed PubMed Central

Nithya C., Devi M.G. & Pandian S.K. 2011. A novel compound from the marine bacterium Bacillus pumilus S6-15 inhibits biofilm formation in Gram-positive and Gram-negative species. Biofouling 27: 519–528.10.1080/08927014.2011.586127Search in Google Scholar PubMed

Newton A., Kendall M., Vugia D.J., Henao O.L. & Mahon B.E. 2012. Increasing rates of vibriosis in the United States, 19962010: review of surveillance data from 2 systems. Clin. Infect. Dis. 54: 391–395.10.1093/cid/cis243Search in Google Scholar PubMed PubMed Central

Purdy A., Rohwer F., Edwards R., Azam F. & Barlett D.H. 2005. A glimpse into the expanded genome content of Vibrio cholerae through identification of genes present in environmental strains. J. Bacteriol. 187: 2992–3001.10.1128/JB.187.9.2992-3001.2005Search in Google Scholar PubMed PubMed Central

Qian P.Y., Li Z., Xu Y., Li Y. & Fusetani N. 2015. Mini-review: marine natural products and their synthetic analogs as antifouling compounds: 2009-2014. Biofouling 31: 101–122.10.1080/08927014.2014.997226Search in Google Scholar PubMed

Rabin N., Zheng Y., Opoku-Temeng C., Du Y., Bonsu E. & Sintim H.Q. 2015. Agents that inhibit bacterial biofilm formation. Future Med. Chem. 7: 647–671.10.4155/fmc.15.7Search in Google Scholar PubMed

Sahilah A.M., Laila R.A., Sallehuddin H.M., Osman H., Aminah A. & Ahmad Azuhairi A. 2014. Antibiotic resistance and molecular typing among cockle (Anadara granosa)strains of Vibrio parahaemolyticus by polymerase chain reaction (PCR)-based analysis. World J. Microbiol. Biotechnol. 30: 649–659.10.1007/s11274-013-1494-ySearch in Google Scholar PubMed

Salini R. & Pandian S.K. 2015. Interference of quorum sensing in urinary pathogen Serratia marcescens by Anethum graveolens. Pathog. Dis. 73: ftv038.10.1093/femspd/ftv038Search in Google Scholar PubMed

Salini R., Sindhulakshmi M., Poongothai T. & Pandian S.K. 2015. Inhibition of quorum sensing mediated biofilm development and virulence in uropathogens by Hyptis suaveolens.Antonie van Leeuwenhoek 107: 1095–1106.10.1007/s10482-015-0402-xSearch in Google Scholar PubMed

Sayem S.M., Manzo E., Ciavatta L., Tramice A., Cordone A., Zanfardino A., De Felice M. & Varcamonti M. 2011. Antibiofilm activity of an exopolysaccharide from a sponge-associated strain of Bacilluslicheniformis. Microb. Cell. Fact. 10: 74–85.10.1186/1475-2859-10-74Search in Google Scholar PubMed PubMed Central

Shaw K.S., Rosenberg Goldstein R.E., He X., Jacibs J.M., Crump B.C. & Sapkota A.R. 2014. Antimicrobial susceptibility of Vibrio vulnificus and Vibrio parahaemolyticusrecovered from recreational and commercial areas of Chesapeake Bay and Maryland Coastal Bays. PLoS One 9: e89616.10.1371/journal.pone.0089616Search in Google Scholar PubMed PubMed Central

Su Y.C. & Liu C. 2007. Vibrio parahaemolyticus: a concern of seafood safety. Food Microbiol. 24: 549–558.10.1016/ in Google Scholar PubMed

Veluri R., Oka I., Wagner-Dobler & Laatsch H. 2003. New indole alkaloids from the North sea bacterium Vibrio parahaemolyticus Bio249. J. Nat. Prod. 66: 1520–1523.10.1021/np030288gSearch in Google Scholar PubMed

Watnick P.I. & Kolter R. 1999. Steps in the development of a Vibrio cholerae biofilm. Mol. Microbiol. 34: 586–595.10.1046/j.1365-2958.1999.01624.xSearch in Google Scholar PubMed PubMed Central

Whitaker W.B., Richards G.P. & Boyd E.F. 2014. Loss of sigma factor RpoN increases intestinal colonization of Vibrio parahaemolyticus in an adult mouse model. Infect. Immun. 82: 544–556.10.1128/IAI.01210-13Search in Google Scholar PubMed PubMed Central

Yeung P.S. & Boor K.J. 2004. Epidemiology pathogenesis and prevention of food borne Vibrioparahaemolyticus infections. Foodborne Pathog. Dis. 1: 74–88.10.1089/153531404323143594Search in Google Scholar PubMed


biofilm inhibitory concentration


cell-free culture supernatant


confocal laser scanning microscopy


2,6-di-O-palmitoyl-L-ascorbic acid


gas chromatography mass spectrometry




Luria Bertani


light microscopy


minimal inhibitory concentration


marine Luria Bertani


optical density


quorum sensing


stearic acid


scanning electron microscopy


Zobell marine broth.

Received: 2015-12-19
Accepted: 2016-3-18
Published Online: 2016-4-20
Published in Print: 2016-3-1

© 2016 Institute of Molecular Biology, Slovak Academy of Sciences

Downloaded on 30.11.2023 from
Scroll to top button