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Anti-biofilm and Anti-quorum Sensing Activities of the Red Seaweed, Gracilaria changii and its Associated Bacteria

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Abstract

Antimicrobial resistance (AMR) is one of the biggest threats to global health and new therapeutic strategies with the potential to reduce AMR are urgently required. Biofilm formation provides advantages for pathogenic bacteria to protect themselves from antibiotics due to the low penetration of antibiotics into the biofilm. Seaweeds have been found to have a variety of bioactive compounds that prevent the attachment and inhibit the biofilm formation by pathogenic bacteria. This study assessed the anti-biofilm and anti-quorum sensing (AQS) activities from the red seaweed, Gracilaria changii, and its associated bacteria. Crude methanol extract of G. changii at 0.01- and 0.001 mg mL−1 resulted in a decrease in Vibrio campbelli BB120 biofilm formation. The crude extract of G. changii inhibited quorum sensing (QS) activity of the reporter strain Chromobacterium violaceum CV026 through inhibition of the purple violacein pigment production using disc diffusion assay. Thin-layer chromatography (TLC) overlay assay was performed to screen for the potential AQS metabolites from G. changii. Out of the six separated compounds, three compounds with the Rf values of 0.94, 0.57 and 0.28 showed QS inhibition zones. A bacterium isolated from the seaweed, Halomonas sp. promoted the bud formation of the seaweed and produce the highest amount of indole-3-acetic acid (IAA) compared to the other bacterial isolates This study shows that G. changii extract has anti-biofilm and AQS activities which could be a potential biocontrol agent. Furthermore, the symbiotic relationship between the Halomonas sp. and G. changii could also be used as growth promoting factor in seaweed cultivation.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Ali B, Hasnain S (2007) Potential of bacterial indoleacetic acid to induce adventitious shoots in plant tissue culture. Lett Appl Microbiol 45:128–133

    Article  CAS  PubMed  Google Scholar 

  • Balasubramanian V, Palanichamy S, Rajaram R (2011) Effects of certain seaweed extracts on the primary biofilm forming bacteria. J Mar Biol Assoc India 53:94–100

    Google Scholar 

  • Bassler BL, Wright M, Showalter RE, Silverman MR (1993) Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 9:773–786

    Article  CAS  PubMed  Google Scholar 

  • Brackman G, Hillaert U, Van Calenbergh S, Nelis HJ, Coenye T (2009) Use of quorum sensing inhibitors to interfere with biofilm formation and development in Burkholderia multivorans and Burkholderia cenocepacia. Res Microbiol 160:144–151

    Article  CAS  PubMed  Google Scholar 

  • Boominathan R, Devanesan S, AlSalhi MS, Balasubramanian A, Alkhalid IZ, Paul P, Singh AJAR (2022) Quorum quenching action of marine red alga Halemenia durvillei on biofilm forming Gram negative bacterial isolates from contact lens. Algal Res 64:102693

    Article  Google Scholar 

  • Cushnie TT, Cushnie B, Lamb AJ (2014) Alkaloids: an overview of their antibacterial, antibiotic-enhancing and antivirulence activities. Int J Antimicrob Agents 44:377–386

    Article  CAS  PubMed  Google Scholar 

  • Defoirdt T, Boon N, Bossier P, Verstraete W (2004) Disruption of bacterial quorum sensing: an unexplored strategy to fight infections in aquaculture. J Aquac 240:69–88

    Article  Google Scholar 

  • Defoirdt T, Thanh LD, Van Delsen B, De Schryver P, Sorgeloos P, Boon N, Bossier P (2011) N-acylhomoserine lactone-degrading Bacillus strains isolated from aquaculture animals. Aquaculture 311:258–260

    Article  CAS  Google Scholar 

  • Dobretsov S, Teplitski M, Paul V (2009) Mini-Review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25:413–427

    Article  CAS  PubMed  Google Scholar 

  • Dong W, Cai Y, Xu Z, Fu B, Chen Q, Cui Y, Ruan Z, Liang Y, Peng N, Zhao S (2020) Heterologous expression of AHL lactonase AiiK by Lactobacillus casei MCJΔ1 with great quorum quenching ability against Aeromonas hydrophila AH-1 and AH-4. Microb Cell Fact 19:191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duca DR, Glick BR (2020) Indole-3-acetic acid biosynthesis and its regulation in plant-associated bacteria. Appl Microbiol Biotechnol 104:8607–8619

    Article  CAS  PubMed  Google Scholar 

  • Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T (2013) The seaweed holobiont: understanding seaweed–bacteria interactions. FEMS Microbiol Rev 37:462–476

    Article  CAS  PubMed  Google Scholar 

  • Fernandes N, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2012) Community structure and functional gene profile of bacteria on healthy and diseased thalli of the red seaweed Delisea pulchra. PLoS One 7:e50854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fouladynezhad N, Afsah-Hejri L, Rukayadi Y, Abdulkarim SM, Marian MN, Son R (2013) Assessing biofilm formation by Listeria monocytogenes. Int Food Res J 20:987–990

    CAS  Google Scholar 

  • Givskov M, de Nys R, Manefield 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • González F, Silva M (2001) Biodiversidad química de maroalgas marinas. In: Alveal K. & T. Antezana (eds). Sustentabilida de la biodiversidad, un problema actual. Bases científìcotécnicas, teorizaciones y proyecciones. University of Concepcion, Chile, pp 415–496

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indole acetic acid. Plant Physiol 26:192–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Hollants J (2012) Endophytic bacteria within the green siphonous seaweed Bryopsis: exploration of a partnership. PhD thesis, Ghent University

  • Issac Abraham SVP, Palani A, Ramaswamy BR, Shunmugiah KP, Arumugam VR (2011) Antiquorum sensing and antibiofilm potential of Capparis spinosa. Arch Med Res 42:658–668

    Article  PubMed  Google Scholar 

  • Jha B, Kavita K, Westphal J, Hartmann A, Schmitt-Kopplin P (2013) Quorum sensing inhibition by Asparagopsis taxiformis, a marine macro alga: separation of the compound that interrupts bacterial communication. Mar Drugs 11:253–265

    Article  PubMed  PubMed Central  Google Scholar 

  • Reinke J (1903) Symbiose von Volvox und Azotobacter. Ber Deut Bot Gesellsch 21:481–483

    Google Scholar 

  • Kalia VC, Kumar P (2015) Potential applications of quorum sensing inhibitors in diverse field. In: Kalia VC (ed) quorum sensing vs quorum quenching: a battle with no end in sight. Springer, India, pp 359–370

    Chapter  Google Scholar 

  • Karnjana K, Nobsathian S, Soowannayan C, Zhao W, Tang YJ, Wongprasert K (2020) Purification and evaluation of N-benzyl cinnamamide from red seaweed Gracilaria fisheri as an inhibitor of Vibrio harveyi AI-2 quorum sensing. Mar Drugs 18:80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keshtacher-Liebson E, Hadar Y, Chen Y (1995) Oligotrophic bacteria enhance algal growth under iron-deficient conditions. Appl Environ Microbiol 61:2439–2441

    Article  CAS  Google Scholar 

  • Kim JS, Kim YH, Seo YW, Park S (2007) Quorum sensing inhibitors from the red alga, Ahnfeltiopsis flabelliformis. Biotechnol Bioprocess Eng 12:308–311

    Article  CAS  Google Scholar 

  • Kumar S, Sahoo D, Kumar P, Ganesan P (2018) Seaweeds as feed supplements for livestock and aquaculture: A review. J Anim Sci Technol 60:1–14

    CAS  Google Scholar 

  • Kolanjinathan K, Saranraj P (2014) Pharmacological efficacy of marine seaweed Gracilaria edulis extracts against clinical pathogens. Glob J Pharmacol 8:268–274

    Google Scholar 

  • Lozano GL, Guan C, Cao Y, Borlee BR, Broderick NA, Stabb EV, Handelsman J (2020) A chemical counterpunch: Chromobacterium violaceum ATCC 31532 produces violacein in response to translation-inhibiting antibiotics. mBio 11:e00948–20

  • Manefield M, de Nys R, Kumar N, Read R, Givskov M, Steinberg PD, Kjelleberg S (1999) Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL) mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145:283–291

    Article  CAS  PubMed  Google Scholar 

  • Maruyama A, Maeda M, Simidu U (1986) Occurrence of plant hormone (cytokinin)-producing bacteria in the sea. J Appl Bacteriol 61:569–574

    Article  CAS  Google Scholar 

  • Maruyama A, Yamaguchi I, Maeda M, Shimizu U (1988) Evidence of cytokinin production by a marine bacterium and its taxonomic characteristics. Can J Microbiol 34:829–833

    Article  CAS  Google Scholar 

  • Miyashita K, Beppu F, Hosokawa M, Liu X, Wang S (2020) Nutraceutical characteristics of the brown seaweed carotenoid fucoxanthin. Arch Biochem Biophys 686:108364

    Article  CAS  PubMed  Google Scholar 

  • McCarter LL (1998) OpaR, a homolog of Vibrio harveyi LuxR, controls opacity of Vibrio parahaemolyticus. J Bacteriol 180:3166–3173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McClean KH, Michael KW, Leigh F, Adrian T, Siri Ram C, Miguel C, Mavis D (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143:3703–3711

    Article  CAS  PubMed  Google Scholar 

  • Milton DL, Hardman A, Camara M, Chhabra SR, Bycroft BW, Stewart GS, Williams P (1997) Quorum sensing in Vibrio anguillarum: characterization of the vanI/vanR locus and identification of the autoinducer N-(3-oxodecanoyl)-L-homoserine lactone. J Bacteriol 179:3004–3012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muthukrishnan S, Shariff M, Ina-Salwany MY, Yusoff FM, Natrah I (2022) Expression of AHPND toxin genes (pirAB), quorum sensing master regulator gene (luxR) and transmembrane transcriptional regulator gene (toxR) in Vibrio parahaemolyticus and Vibrio harveyi during infection of Penaeus vannamei (Bonne, 1931). Aquaculture 551:737895

    Article  CAS  Google Scholar 

  • Natrah FMI, Defoirdt T, Sorgeloos P, Bossier P (2011) Disruption of bacterial cell-to-cell communication by marine organisms and its relevance to aquaculture. Mar Biotechnol 13:109–126

    Article  CAS  Google Scholar 

  • Natrah I, Muthukrishnan S, Bossier P (2022) Quorum quenching bacteria as probiotics. In: Austin B, Sharifuzzaman SM (eds) Probiotics in Aquaculture. Springer, Cham, pp 165–191

    Chapter  Google Scholar 

  • Norziah MH, Ching CY (2000) Nutritional composition of edible seaweed Gracilaria changii. Food Chem 68:69–76

    Article  CAS  Google Scholar 

  • Park JW, Cho YC, Nam BH, Jin HY, Sohn CH, Hong YK (1998) RAPD identification of genetic variation in seaweeds Hizikia fusiformis (Fucales, Phaeophyta). J Mar Biotechnol 6:62–64

    CAS  Google Scholar 

  • Prabhakaran S, Rajaram R, Balasubramanian V, Mathivanan K (2012) Antifouling potentials of extracts from seaweeds, seagrasses and mangroves against primary biofilm forming bacteria. Asian Pac J Trop Biomed 2:S316–S322

    Article  Google Scholar 

  • Provasoli L (1958) Effect of plant hormones on Ulva. Biol Bull 114:375–384

    Article  CAS  Google Scholar 

  • Rasmussen TB, Manefield M, Andersen JB, Eberl L, Anthoni U, Christopherse C, Steinberg P, Kjelleberg S, Givskov M (2000) How Delisa pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology 146:3237–3244

    Article  CAS  PubMed  Google Scholar 

  • Rima M, Trognon J, Latapie L, Chbani A, Roques C, El Garah F (2022) Seaweed extracts: a promising source of antibiofilm agents with distinct mechanisms of action against Pseudomonas aeruginosa . Mar Drugs 20:92

  • Sasidharan S, Darah I, Jain K (2009) Screening antimicrobial activity of various extracts of Gracilaria changii. Pharm Biol 47:72–76

    Article  Google Scholar 

  • Sasidharan S, Darah I, Jain K (2011) In vitro and in situ antiyeast activity of Gracilaria changii methanol extract against Candida albicans. Eur Rev Med Pharmacol Sci 15:1020–1026

    CAS  PubMed  Google Scholar 

  • Sfanos K, Harmody D, Dang P, Ledger A, Pomponi S, McCarthy P, Lopez JA (2005) Molecular systematic survey of cultured microbial associates of deep-water marine invertebrates. Syst Appl Microbiol 28:242–264

    Article  CAS  PubMed  Google Scholar 

  • Silva A, Silva SA, Carpena M, Garcia-Oliveira P, Gullón P, Barroso MF, Prieto MA, Simal-Gandara J (2020) Macroalgae as a source of valuable antimicrobial compounds: extraction and applications. Antibiotics 9:642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh RP (2013) Isolation and characteratization of exopolysaccharides from seaweed associated bacteria Bacillus licheniformis. Carbohydr Polym 84:1019–1026

    Article  Google Scholar 

  • Singh RP, Reddy CRK (2014) Seaweed-microbial interactions: Key functions of seaweed-associated bacteria. FEMS Microbiol Ecol 88:213–230

  • Singh RP, Mantri VA, Reddy CRK, Jha B (2011a) Isolation of seaweed-associated bacteria and their morphogenesis-inducing capability in axenic cultures of the green alga Ulva fasciata. Aquat Biol 12:13–21

    Article  Google Scholar 

  • Singh RP, Bijo J, Baghel RS, Reddy CRK, Jha B (2011b) Role of bacterial isolates in enhancing the bud induction in the industrially important red alga Gracilaria dura. FEMS Microbiol Ecol 76:381–392

    Article  CAS  PubMed  Google Scholar 

  • Spoerner M, Wichard T, Bachhuber T, Stratmann J, Oertel W (2012) Growth and thallus morphogenesis of Ulva mutabilis (Chlorophyta) depends on a combination of two bacterial species excreting regulatory factors. J Phycol 48:1433–1447

    Article  PubMed  Google Scholar 

  • Spring S, Brinkmann N, Murrja M, Spröer C, Reitner J, Klenk HP (2015) High diversity of culturable prokaryotes in a lithifying hypersaline microbial mat. Geomicrobiol J 32:332–346

    Article  CAS  Google Scholar 

  • Swift S, Karlyshev AV, Fish L, Durant EL, Winson MK, Chhabra SRAM, Stewart GSAB (1997) Quorum Sensing in Aeromonas hydrophila and Aeromonas salmonicida : identification of the LuxRI homologs AhyRI and AsaRI and their cognate N -acylhomoserine lactone signal molecules. J Bacteriol 179:5271–5281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 38:3022–3027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang J, Wang W, Chu W (2020) Antimicrobial and anti-quorum sensing activities of phlorotannins from seaweed (Hizikia fusiforme). Front Cell Infect Microbiol 30:586750

    Article  Google Scholar 

  • Vadassery DH, Pillai D (2020) Quorum quenching potential of Enterococcus faecium QQ12 isolated from gastrointestinal tract of Oreochromis niloticus and its application as a probiotic for the control of Aeromonas hydrophila infection in goldfish Carassius auratus (Linnaeus 1758). Braz J Microbiol 51:1333–1343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wahl M, Goecke F, Labes A, Dobretsov S, Weinberger F (2012) The second skin: ecological role of epibiotic biofilms on marine organisms. Front Microbiol 3:292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitehead NA, Barnard AML, Slater H, Simpson NJL, Salmond GPC (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25:365–404

    Article  CAS  PubMed  Google Scholar 

  • Wijesinghe WAJP, Jeon YJ, Lee HG (2017) Seaweeds as potential ingredients for the development of new functional foods: A review. Food Res Int 99:1066–1075

    Google Scholar 

  • Zerrifi S, El Khalloufi F, Oudra B, Vasconcelos V (2018) Seaweed bioactive compounds against pathogens and microalgae: potential uses on pharmacology and harmful algae bloom control. Mar Drugs 16:55

    Article  PubMed  PubMed Central  Google Scholar 

  • Zoppellari F, Malusà E, Chitarra W, Lovisolo C, Spanna F, Bardi L (2014) Improvement of drought tolerance in maize (Zea mays L.) by selected rhizospheric microorganisms. Ital J Agrometeorol 18:5–18

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Funding

The authors recognized and acknowledged the financial support from the Ministry of Higher Education Malaysia through the Fundamental Research Grant Sheme (FRGS) with the project number FRGS/1/2018/WAB09/UPM/02/3.

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Authors and Affiliations

  1. Aquatic Animal Health and Therapeutics Laboratory (AquaHealth), Institute of Bioscience, Universiti Putra Malaysia, 43400 UPM, Serdang, Selangor, Malaysia

    Sarmila Muthukrishnan & I. Natrah

  2. Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia, 43400 UPM, Serdang, Selangor, Malaysia

    Nurul Izzati Muthar, Muta Harah Zakaria & I. Natrah

  3. Department of Food Sciences, Faculty of Food Sciences and Technology, Universiti Putra Malaysia, 43400 UPM, Serdang, Selangor, Malaysia

    Muta Harah Zakaria & Yaya Rukayadi

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  1. Sarmila Muthukrishnan
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  3. Muta Harah Zakaria
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  5. I. Natrah
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Contributions

Sarmila Muthukrishnan wrote the main manuscript text; Nurul Izzati Muthar conducted the experiments; Natrah Ikhsan, Muta Harah Zakaria and Yaya Rukayadi designed the experiments; and all the authors reviewed the manuscript.

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Correspondence to I. Natrah.

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Muthukrishnan, S., Muthar, N.I., Zakaria, M.H. et al. Anti-biofilm and Anti-quorum Sensing Activities of the Red Seaweed, Gracilaria changii and its Associated Bacteria. J Appl Phycol 35, 2555–2566 (2023). https://doi.org/10.1007/s10811-023-03035-7

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