Skip to main content

Advertisement

Log in

Unraveling the anti-biofilm potential of green algal sulfated polysaccharides against Salmonella enterica and Vibrio harveyi

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

One of the main reasons for the bacterial resistance to antibiotics is caused by biofilm formation of microbial pathogens during bacterial infections. Salmonella enterica and Vibrio harveyi are known to form biofilms and represent a major health concern worldwide, causing human infections responsible for morbidity and mortality. The current study aims to investigate the effect of purified sulfated polysaccharides (SPs) from Chlamydomonas reinhardtii (Cr) on planktonic and biofilm growth of these bacteria. The effect of Cr-SPs on bacterial planktonic growth was assessed by using the agar well diffusion method, which showed clear zones ranging from 13 to 26 mm in diameter from 0.5 to 8 mg/mL of Cr-SPs against both the bacteria. Time-kill activity and reduction in clonogenic propagation further help to understand the anti-microbial potential of Cr-SPs. The minimum inhibitory concentration of Cr-SPs against S. enterica and V. harveyi was as low as 440 μg/mL and 490 μg/mL respectively. Cr-SPs inhibited bacterial cell attachment up to 34.65–100% at 0.5–8 mg/mL in S. enterica and V. harveyi respectively. Cr-SPs also showed 2-fold decrease in the cell surface hydrophobicity, indicating their potential to prevent bacterial adherence. Interestingly, Cr-SPs efficiently eradicated the preformed biofilms. Increased reduction in total extracellular polysaccharide (EPS) and extracellular DNA (eDNA) content in a dose-dependent manner demonstrates Cr-SPs ability to interact and destroy the bacterial EPS layer. SEM analysis showed that Cr-SPs effectively distorted preformed biofilms and also induced morphological changes. Furthermore, Cr-SPs also showed anti-quorum-sensing potential by reducing bacterial urease and protease activities. These results indicate the potential of Cr-SPs as an anti-biofilm agent and will help to develop them as alternative therapeutics against biofilm-forming bacterial infections.

Key points

• Cr-SPs not only inhibited biofilm formation but also eradicated preformed biofilms.

• Cr-SPs altered bacterial cell surface hydrophobicity preventing biofilm formation.

• Cr-SPs efficiently degraded eDNA of the EPS layer disrupting mature biofilms.

• Cr-SPs reduced activity of quorum-sensing-mediated enzymes like protease and urease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abdullah MAA, El-baky RMA, Hassan HA, Abdelhafez E, Abuo-Rahma G (2016) Fluoroquinolones as urease inhibitors: anti Proteus mirabilis activity and molecular docking studies. Am J Microbiol Res 4:81–84

    CAS  Google Scholar 

  • The nature and extent of foodborne disease. In: J. Barros-Velázquez (ed) Antimicrobial food packaging; chapter 1. Academic Press, San Diego pp 1–10

  • Ale MT, Mikkelsen JD, Meyer AS (2011) Important determinants for Fucoidan bioactivity: a critical review of structure-function relations and extraction methods for fucose-containing sulfated polysaccharides from brown seaweeds. Mar Drugs 9:2106–2130

    CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Emran HM, Eibach D, Krumkamp R, Ali M, Baker S, Biggs HM, Bjerregaard-Andersen M, Breiman RF, Clemens JD, Crump JA, Espinoza LMC, Deerin J, Dekker DM, Sow AG, Hertz JT, Im J, Ibrango S, von Kalckreuth V, Kabore LP, Konings F, Løfberg SV, Meyer CG, Mintz ED, Montgomery JM, Olack B, Pak GD, Panzner U, Park SE, Razafindrabe JLT, Rabezanahary H, Rakotondrainiarivelo JP, Rakotozandrindrainy R, Raminosoa TM, Schütt-Gerowitt H, Sampo E, Soura AB, Tall A, Warren M, Wierzba TF, May J, Marks F (2016) A multicountry molecular analysis of Salmonella enterica Serovar Typhi with reduced susceptibility to ciprofloxacin in sub-Saharan Africa. Clin Infect Dis 62(suppl 1):S42–S46. https://doi.org/10.1093/cid/civ788

  • Almeida FA, Pimentel-Filho NJ, Pinto UM, Mantovani HC, Oliveira LL, Vanetti MCD (2016) Acyl homoserine lactone-based quorum sensing stimulates biofilm formation by Salmonella Enteritidis in anaerobic conditions. Arch Microbiol 199(3):475–486. https://doi.org/10.1007/s00203-016-1313-6

    Article  CAS  PubMed  Google Scholar 

  • Aravindraja C, Valliammai A, Viszwapriya D, Pandian D, Karutha S (2017) Quorum sensing mediated virulence inhibition of an opportunistic human pathogen Serratia marcescens from unexplored marine sediment of Palk Bay through function driven metagenomic approach. Indian J Exp Biol 55:448–452

    CAS  Google Scholar 

  • Barbieri R, Coppo E, Marchese A, Daglia M, Sobarzo-SE NSF, Nabavi SM (2017) Phytochemicals for human disease: an update on plant-derived compounds antibacterial activity. Microbiol Res 196:44–68

    CAS  PubMed  Google Scholar 

  • Bazargani MM, Jens R (2015) Anti-biofilm activity of essential oils and plant extracts against Staphylococcus aureus and E. coli biofilms. Food Control 61:156–164

    Google Scholar 

  • Bhaskar SV (2017) Food borne diseases: disease burden. In: Food safety in the 21st century, 1st edn. Elsevier pp 3–12. https://doi.org/10.1016/B978-0-12-801773-900001-7

  • Boyd KM (2000) Disease, illness, sickness, health, healing and wholeness: exploring some elusive concepts. J Med Ethics: Medical Humanities 26:9–17. https://doi.org/10.1136/mh.26.1.9

    Article  Google Scholar 

  • Caccamese S, Azzolina R, Furnari G, Cormaci M, Grasso S (1981) Antimicrobial and antiviral activities of some marine algae from eastern Sicily. Bot Mar 24:365–368

    Google Scholar 

  • Camargo AC, Woodward JJ, Call DR, Luís AN (2017) Listeria monocytogenes in food processing facilities, food contamination, and human listeriosis: the Brazilian scenario. Foodborne Pathog Dis 14:623–636

    PubMed  Google Scholar 

  • Chari Nithya, Felix L, Selvaraj K, Renganathan K, Dhamodharan B, Manivel A, Naiyf SA, Arunachalam C, Sulaiman AA, Nooruddin T(2014) Biofilm inhibitory potential of Chlamydomonas sp. extract against Pseudomonas aeruginosa. J Algal Biomass Util 5:74–81

  • Chochlakis D, Varveraki SP, Kostalas DM, Carouzou CK, Psaroulaki A (2019) Infection due to Vibrio harveyi and Photobacterium Damselae following injury into a marine environment. Biomed J Sci Tech Res 22(2):16462–16466

  • Choi SM, Jang EJ, Cha JD (2015) Synergistic effect between fucoidan and antibiotics against clinic methicillin-resistant Staphylococcus aureus. Adv Biosci Biotechnol 6:55731

    Google Scholar 

  • Choudhary S, Save S, Vavilala LS (2018) Unravelling the inhibitory activity of Chlamydomonas reinhardtii sulphated polysaccharides against a-Synuclein fibrillation. Sci Report 8:5692

    Google Scholar 

  • Dalal R (2015) Screening and isolation of protease producing bacteria from soil collected from different areas of Burhanpur region (MP) India. Int J Curr Microbiol App Sci 4:597–606

    Google Scholar 

  • Das T, Sehar S, Koop L, Wong YK, Ahmed S, Siddiqui KS, Manefield M (2014) Influence of calcium in extracellular DNA mediated bacterial aggregation and biofilm formation. PLoS One 9:e91935

    PubMed  PubMed Central  Google Scholar 

  • Delago A, Mandabi A, Meijler MM (2016) Natural quorum sensing inhibitors–small molecules, big messages. Isr J Chem 56(5):310–320. https://doi.org/10.1002/ijch.201500052

    Article  CAS  Google Scholar 

  • Dibyajit L, Sudipta D, Rachayeeta D, Rachayeeta D, Moupriya N (2019) Elucidating the effect of anti-biofilm activity of bioactive compounds extracted from plants. J Biosci 44:52

    Google Scholar 

  • Di Martino P, Cafferini N, Joly B, Darfeuille-Michaud A (2003) Klebsiella pneumoniae type 3 pili facilitate adherence and biofilm formation on abiotic surfaces. Res Microbiol 154:9–16

    PubMed  Google Scholar 

  • Dodgson KS, Price RG (1962) A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem J 84:106–110

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    CAS  Google Scholar 

  • Eibach D, Al-Emran HM, Dekker DM, Krumkamp R, Adu-Sarkodie Y, Espinoza LMC, Ehmen C, Boahen K, Heisig P, Im J, Jaeger A, von Kalckreuth V, Pak GD, Panzner U, Park SE, Reinhardt A, Sarpong N, Schütt-Gerowitt H, Wierzba TF, Marks F, May J (2016) The emergence of reduced ciprofloxacin susceptibility in Salmonella enterica causing bloodstream infections in rural Ghana. Clin Infect Dis 62(suppl 1):S32–S36. https://doi.org/10.1093/cid/civ757

  • Follmer C (2010) Ureases as a target for the treatment of gastric and urinary infections. J Clin Pathol 63:424–430

    CAS  PubMed  Google Scholar 

  • Geier H, Mostowy S, Cangelosi GA, Behr MA, Timothy EF (2008) Autoinducer-2 triggers the oxidative stress response in Mycobacterium avium, leading to biofilm formation. Appl Environ Microbiol 74:1798–1804

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia-Lara B, Saucedo-Mora MA, Roldan-Sanchez JA, Perez-Eretza B, Ramasamy M, Lee J, Coria-Jimenez R, Tapia M, Varela-Guerrero VV, Garcia-Contreras R (2015) Inhibition of quorum-sensing-dependent virulence factors and biofilm formation of clinical and environmental Pseudomonas aeruginosa strains by ZnO nanoparticles. Lett Appl Microbiol 61(3):299–305. https://doi.org/10.1111/lam.12456

  • Getahun A, Abraham A, Alemayehu S, Solomon G, Bekele F, Dawit W, Håkan M (2004) Evaluation of direct colorimetric assay for rapid detection of rifampicin resistant Mycobacterium tuberculosis. J Clin Microbiol 42:871–873

    Google Scholar 

  • Giannella RA (1996) Salmonella. In: Baron, S (ed) Medical Microbiology, 4th edn. University of Texas Medical Branch at Galveston, Galveston, Galveston (TX) pp 1–7

  • Graziano TS, Cuzzullin MC, Franco GC, Schwartz-Filho HO, de Andrade ED, Groppo FC, Cogo-Müller K (2015) Statins and antimicrobial effects: simvastatin as a potential drug against Staphylococcus aureus biofilm. PLoS One 10:e0128098

    PubMed  PubMed Central  Google Scholar 

  • Horikawa M, Noro T, Kamei Y (1999) In vitro antimethicillin-resistant Staphylococcus aureus activity found in extracts of marine algae indigenous to the coastline of Japan. J Antibiot 52:186–189

    CAS  Google Scholar 

  • Hughes DT, Sperandio V (2008) Inter-kingdom signalling: communication between bacteria and their hosts. Nat Rev Microbiol 6(2):111–120. https://doi.org/10.1038/nrmicro1836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • IFT (2004) Institute of Food Technologist. Bacteria associated with foodborne disease. Food Tech Mag 58:20–21

    Google Scholar 

  • Jiao G, Yu G, Zhang J, Ewart SH (2011) Chemical structures and bioactivities of sulphated polysaccharides from marine algae. Mar Drugs 9:196–223

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones BD, Lockatell CV, Johnson DE, Warren JW, Mobley HL (1990) Construction of a urease negative mutant of Proteus mirabilis: analysis of virulence in a mouse model of ascending urinary tract infection. Infect Immun 58:1120–1123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jun JY, Jung MJ, Jeong IH, Yamazaki K, Kawai Y, Kim BM (2018) Antimicrobial and anti-biofilm activities of sulfated polysaccharides from marine algae against dental plaque bacteria. Mar Drug 16:301

    Google Scholar 

  • Kamble P, Sanith C, Lopus M, Vavilala S (2018) Chemical characteristics, antioxidant and anticancer potential of sulfated polysaccharides from Chlamydomonas reinhardtii. J Appl Phycol 30:1641–1653

    CAS  Google Scholar 

  • Kauffmann F, Moller U (1955) On amino acid decarboxylases of Salmonella types and on the KCN test. Acta Pathol Microbial Scand 36:173–178

    CAS  Google Scholar 

  • Kearns DB (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 2010(8):634–644

    Google Scholar 

  • Kim SH, Park C, Lee EJ, Banga WS, Kim YJ, Kim JS (2017) Biofilm formation of Campylobacter strains isolated from raw chickens and its reduction with DNase I treatment. Food Control 71:94–100

    CAS  Google Scholar 

  • Kim W, Killam T, Sood V, Surette MG (2003) Swarm-cell differentiation in Salmonella enterica serovar typhimurium results in elevated resistance to multiple antibiotics. J Bacteriol 185:3111–3117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marathe K, Bundale S,  Nashikkar N, Upadhyay A (2018) Influence of linoleic acid on quorum sensing in Proteus mirabilis and Serratia marcescens. Bios Biotech Res Asia 15:661–670

  • Lade H, Paul D, Kweon JH (2014) Quorum quenching mediated approaches for control of membrane biofouling. Int J Biol Sci 10:550–565. https://doi.org/10.7150/ijbs.9028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lappann M, Claus H, Van AT, Harmsen M, Elias J, Molin S, Vogel U (2010) A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis. Mol Microbiol 75:1355–1371

    CAS  PubMed  Google Scholar 

  • Li LY, Li LQ, Guo CH (2010) Evaluation of in vitro antioxidant and antibacterial activities of Laminaria japonica polysaccharides. J Med Plant Res 4:2194–2198

    CAS  Google Scholar 

  • Liao S, Klein MI, Heim KP, Fan Y, Bitoun JP, Ahn SJ, Burne RA, Koo H, Brady LJ, Wen ZT (2014) Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery. J Bacteriol 196:2355–2366

    PubMed  PubMed Central  Google Scholar 

  • Lillehoj H, Liu Y, Calsamiglia S, Fernandez-Miyakawa ME, Chi F, Cravens RL, Oh S, Gay CG (2018) Phytochemicals as antibiotic alternatives to promote growth and enhance host health. Vet Res 49:76

    PubMed  PubMed Central  Google Scholar 

  • Lu WJ, Lin HJ, Hsu PH, Lai M, Chiu JY, Lin HTV (2019) Brown and red seaweeds serve as potential efflux pump inhibitors for drug-resistant Escherichia coli. Evid Based Complement Alternat Med 2019:1836982

    PubMed  PubMed Central  Google Scholar 

  • MacFaddin J (1980) Biochemical tests for identification of medical bacteria, 2nd edn. Baltimore, Williams and Wilkins

    Google Scholar 

  • Mahsa RO, Mohsen A, Mojtaba A, Shokri SK, Mozafari AN, Doghaheh PH (2015) Allicin from garlic inhibits the biofilm formation and urease activity of Proteus mirabilis in vitro. FEMS Microbiol Lett 362(9): fnv049. https://doi.org/10.1093/femsle/fnv049

  • Manikandan S, Ganesapandian S, Singh M, Sangeetha N, Kumaraguru AK (2011) Antimicrobial activity of seaweeds against multi drug resistant strains. Int J Pharmacol 7:522–526

    Google Scholar 

  • Manuel M, Christian J, Susan MB, Aaron N, Sarah T, Joachim R, Karl EK, Andrew C, Stefan S (2009) A novel regulatory protein involved in motility of Vibrio cholerae. J Bacteriol 191:7027–7038

    Google Scholar 

  • Marudhupandi T, Kumar TTA (2013) Antibacterial effect of fucoidan from Sargassum wightii against the chosen human bacterial pathogens. Int Curr Pharm J 2:156–158

    Google Scholar 

  • Montanaro L, Alessandro P, Livia V, Ravaioli S, Campoccia D, Speziale P, Carla RA (2011) Extracellular DNA in biofilms. Int J Artificial Organs 34:824–831

    CAS  Google Scholar 

  • Nadell CD, Bassler BL (2011) A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc Natl Acad Sci 108:14181–14185

  • Nguyen UT, Burrows LL (2014) DNase I and proteinase K impair Listeria monocytogenes biofilm formation and induce dispersal of pre-existing biofilms. Int J Food Microbiol 187:26–32

    CAS  PubMed  Google Scholar 

  • Ni N, Li M, Wang J, Wang B (2009) Inhibitors and antagonists of bacterial quorum sensing. Med Res Rev 29(1):65–124. https://doi.org/10.1002/med.20145Return

    Article  CAS  PubMed  Google Scholar 

  • Osunla CA, Okoh AI (2017) Vibrio Pathogens: A Public Health Concern in Rural Water Resources in Sub-Saharan Africa. Int J Envt Res Public Health 14:1188. https://doi.org/10.3390/ijerph14101188

  • Packiavathy IASV, Pandian SK, Priya S, Ravi AV (2011) Inhibition of biofilm development of uropathogens by curcumin–an anti-quorum sensing agent from Curcuma longa. Food Chem 148:453–460

    Google Scholar 

  • Panigrahi GP, Rane AR, Vavilala SL, Choudhary S (2019) Deciphering the anti-Parkinson’s activity of sulfated polysaccharides from Chlamydomonas reinhardtii on the α-synuclein mutants A30P, A53T, E46K, E57K and E35K. J Biochem 166:463–474

    CAS  PubMed  Google Scholar 

  • Patel S (2012) Therapeutic importance of sulfated polysaccharides from seaweeds: updating the recent findings. 3 Biotech 2:171–815

    PubMed Central  Google Scholar 

  • Paluch E, Rewak-Soroczyńska J, Jędrusik I, Mazurkiewicz E, Jermakow K (2020) Prevention of biofilm formation by quorum quenching. Appl Microbiol Biotechnol 104. https://doi.org/10.1007/s00253-020-10349-w

  • Pierre G, Sopena V, Juin C, Mastouri A, Graber M, Maugard T (2011) Antibacterial activity of a sulfated galactan extracted from the marine alga Chaetomorpha aerea against Staphylococcus aureus. Biotechnol Bioprocess Eng 16:937–945

    CAS  Google Scholar 

  • Pinto NCC, Silva JB, Menegati LM, Guedes MCMR, Marques LB, Silva TPD, Melo RCN, Souza-Fagundes EM, Salvador MJ, Scio E, Fabri RL (2017) Cytotoxicity and bacterial membrane destabilization induced by Annona squamosa L. extracts. Anais Acad Bras Cienc 89:2053–2073

    CAS  Google Scholar 

  • Prywer J, Torzewska A (2012) Effect of curcumin against Proteus mirabilis during crystallization of struvite from artificial urine. Evid Based Complement Alternat Med 3:1–7

    Google Scholar 

  • Radzig MA, Nadtochenko VA, Koksharova OA, Kiwi J, Lipasova VA, Khmel IA (2013) Antibacterial effects of silver nanoparticles gram-negative bacteria: influence on the growth and biofilms formation, mechanisms of action. Colloid Surf B: Biointerfaces 102:300–306. https://doi.org/10.1016/j.colsurfb.2012.07.039

    Article  CAS  PubMed  Google Scholar 

  • Rampioni G, Leoni L, Williams P (2014) The art of antibacterial warfare: deception through interference with quorum sensing–mediated communication. Bioorg Chem 55:60–68. https://doi.org/10.1016/j.bioorg.2014.04.005

    Article  CAS  PubMed  Google Scholar 

  • Rattiyaphorn P, Chitchanok A, Sakawrat K, Taweechaisupapong S, Chareonsudjai P, Chareonsudjai S (2019) Extracellular DNA facilitates bacterial adhesion during Burkholderia pseudomallei biofilm formation. PLoS One 14:e0213288

    Google Scholar 

  • Rauf A, Uddin G, Siddiqui BS, Khan A, Farooq U, Khan F, Majid SB, Khan SB (2017) Bioassay guided isolation of novel and selective urease inhibitors from Diospyros lotus. Chin J Nat Med 15:865–870

    PubMed  Google Scholar 

  • Ruby EG (1996) Lessons from a cooperative, bacterial-animal association: the Vibrio fischeri-Euprymna scolopes light organ symbiosis. Annu Rev Microbiol 50:591–624

  • Rutherford ST, Bassler BL (2012) Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harbor Perspect Med 2:a012427

    Google Scholar 

  • Sasirekha B, Megha DM, Sharath Chandra MS, Soujanya R (2015) Study on effect of different plant extracts on microbial biofilms. Asian J Biotechnol 7:1–12. https://doi.org/10.3923/ajbkr.2015

    Article  CAS  Google Scholar 

  • Seedevi P, Moovendhan M, Viramani S, Shanmugam A (2016) Bioactive potential and structural characterization of sulphated polysaccharide from seaweed (Gracilaria corticata). Carbohydr Polym 155:516–524

    PubMed  Google Scholar 

  • Serena G, Coral GG, Elisa MM, Claudio JV, Felipe L (2018) Biofilms in the food industry: health aspects and control methods. Front Microbiol 9:898

    Google Scholar 

  • Sethupathy S, Ananthi S, Selvaraj A, Shanmuganathan B, Vigneshwari L, Balamurugan K, Mahalingam S, Pandian S (2017) Vanillic acid from Actinidia deliciosa impedes virulence in Serratia marcescens by affecting S-layer, flagellin and fatty acid biosynthesis proteins. Sci Rep 7:16328

    PubMed  PubMed Central  Google Scholar 

  • Sethupathy S, Shanmuganathan B, Kasi PD, Pandian SK (2016) Alpha-bisabolol from brown macroalga Padina gymnospora mitigates biofilm formation and quorum sensing controlled virulence factor production in Serratia marcescens. J Appl Phycol 28:1987–1996

    CAS  Google Scholar 

  • Shannon EM, Jennie M, Elaine S, Frederick JA, Martyn K, Sarah JB, Timothy FJ, Aamir F, Robert M (2010) The global burden of nontyphoidal Salmonella Gastroenteritis. Clin Inf Dis 50:882–889. https://doi.org/10.1086/650733

    Article  Google Scholar 

  • Singh OV (2017) Foodborne pathogens and antibiotic resistance. Publisher: John Wiley & Sons Inc, Boston

  • Sirisha VL, Mahuya S, D’Souza SJ (2014) Menadione-induced caspase dependent programmed cell death in the green chlorophyte Chlamydomonas reinhardtii. J Phycol 50:587–601

    CAS  PubMed  Google Scholar 

  • Sorongon ML, Bloodgood RA, Burchard RP (1991) Hydrophobicity, adhesion, and surface-exposed proteins of gliding bacteria. App Envt Microbiol 57:3193–3199

    CAS  Google Scholar 

  • Srinivasan R, Devi KR, Kannappan A, Pandian SK, Ravi AV (2016) Piper betle and its bioactive metabolite phytol mitigates quorum sensing mediated virulence factors and biofilm of nosocomial pathogen Serratia marcescens in vitro. J Ethnopharmacol 193:592–603

    CAS  PubMed  Google Scholar 

  • Stevens DL, Bisno AL, Chambers HF, Dellinger EP, Goldstein EJ, Gorbach SL et al (2014) Practice guidelines for diagnosis and management of skin and soft tissue infections update by the Infectious Diseases Society of America. Clin Infect Dis 59(2):e10–e52

    PubMed  Google Scholar 

  • Stewart PS (2002) Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 292:107–113

  • Teanpaisan R (2016) Screening for antibacterial and biofilm activity in Thai medicinal plant extracts against oral microorganisms. J Tradit Complement Med 7:172–177

    PubMed  PubMed Central  Google Scholar 

  • Thongkao K, Sudjaroen Y (2017) Vibrio harveyi, V. parahaemolyticus, and V. vulnificus detection in Thai shellfishes by the triplex PCR method. Ann Trop Med Public Health 10:417–422

  • Trentin Dda S, Giordani RB, Zimmer KR, da Silva AG, da Silva MV, Correia MT, Baumvol IJ, Macedo AJ (2011) Potential of medicinal plants from the Brazilian semi-arid region (Caatinga) against Staphylococcus epidermidis planktonic and biofilm lifestyles. J Ethnopharmacol 137:327–335

    PubMed  Google Scholar 

  • Vishwakarma J, Parmar V, Vavilala SL (2019) Nitrate stress induced bioactive sulfated polysaccharides from Chlamydomonas reinhardtii. Biomed Res J 6:7–16

    Google Scholar 

  • Vishwakarma J, Vavilala SL (2019) Evaluating the antibacterial and antibiofilm potential of sulfated polysaccharides extracted from green algae Chlamydomonas reinhardtii. J Appl Microbiol 127:1004–1017

    CAS  PubMed  Google Scholar 

  • Wagih S, Reda G, Gehan I, Elzanaty ME (2017) Antibacterial activity of some seaweed extracts against multidrug resistant urinary tract bacteria and analysis of their virulence genes. Int J Curr Microbiol App Sci 6:2569–2586

    Google Scholar 

  • Walters M, Sperandio V (2006) Quorum sensing in Escherichia coli and Salmonella. Int J Med Microbiol 296:125–131. https://doi.org/10.1016/j.ijmm.2006.01.04.1

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Jin Q, Xiang H, Wang W, Guo N, Zhang K, Tang X, Meng R, Feng H, Liu L, Wang X, Liang J, Shen F, Xing M, Deng X, Yu L (2011) Transcriptional and functional analysis of the effects of magnolol: inhibition of autolysis and biofilms in Staphylococcus aureus. PLoS One 6:e26833

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whitchurch CB, Tolker NT, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Sci 295:1487

    CAS  Google Scholar 

  • World Health Organization (2019) https://www.who.int/en/news-room/fact-sheets/detail/food-safety

  • Xavier KB, Bassler BL (2005) Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J Bacteriol 187(1):238–248. https://doi.org/10.1128/JB.187.1.238-248.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waters CM, Bassler BL (2006) The Vibrio harveyi quorum-sensing system uses shared regulatory components to discriminate between multiple autoinducers. Genes Dev 20(19):2754–2767. https://doi.org/10.1101/gad.1466506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan X, Gu S, Shi Y, Cui X, Wen S, Ge J (2017) The effect of emodin on Staphylococcus aureus strains in planktonic form and biofilm formation in vitro. Arch Microbiol 199:1267–1275

    CAS  PubMed  Google Scholar 

  • Zapopozhets TS, Besednova NN, Loenko IN (1995) Antibacterial and immunomodulating activity of fucoidan. Antibiot Chemother 40:9–13

    CAS  Google Scholar 

  • Zhou Y, Kong Y, Kundu S, Cirillo JD, Liang H (2012) Antibacterial activities of gold and silver nanoparticles against Escherichia coli and Bacillus Calmette-Guerin. J Nanobiotechnol 10:19

    CAS  Google Scholar 

Download references

Acknowledgments

This work is supported by Department of Atomic Energy, India.

Author contribution statement

Dr. Vavilala—concept, data analysis, and editing the manuscript; Ms. Vishwakarma—performed the experiments and analyzed the data.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sirisha V.L.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights and informed consent

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vishwakarma, J., V.L, S. Unraveling the anti-biofilm potential of green algal sulfated polysaccharides against Salmonella enterica and Vibrio harveyi. Appl Microbiol Biotechnol 104, 6299–6314 (2020). https://doi.org/10.1007/s00253-020-10653-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-020-10653-5

Keywords

Navigation