Polyphenols from olive mill waste affect biofilm formation and motility in Escherichia coli K-12

Olive mill wastes are sources of phenolic compounds with a wide array of biological activities, including antimicrobial effects. A potential option for bioremediation to overcome ecological problems is the reutilization of these natural compounds in food production. The aim of this work was to gain a better understanding of the antimicrobial mode of action of a phenols extract from olive vegetation water (PEOVW) at molecular level by studying Escherichia coli as a model microorganism. Genome‐wide transcriptional analysis was performed on E. coli K‐12 exposed to PEOVW. The repression of genes for flagellar synthesis and the involvement of genes linked to biofilm formation and stress response were observed. Sub‐inhibitory concentrations of PEOVW significantly decreased biofilm formation, swarming and swimming motility, thus confirming the gene expression data. This study provides interesting insights on the molecular action of PEOVW on E. coli K‐12. Given these anti‐biofilm properties and considering that biofilm formation is a serious problem for the food industry and human health, PEOVW has proved to be a high‐value natural product.

[1]  Liang Zhang,et al.  An optimized RNA amplification method for prokaryotic expression profiling analysis , 2010, Applied Microbiology and Biotechnology.

[2]  Achinto Saha,et al.  New Role of (−)-Epicatechin in Enhancing the Induction of Growth Inhibition and Apoptosis in Human Lung Cancer Cells by Curcumin , 2010, Cancer Prevention Research.

[3]  S. K. Pandian,et al.  Eugenol (an essential oil of clove) acts as an antibacterial agent against Salmonella typhi by disrupting the cellular membrane. , 2010, Journal of ethnopharmacology.

[4]  W. Liang,et al.  9) TM4 Microarray Software Suite , 2006 .

[5]  Reinhard Guthke,et al.  More than just a metabolic regulator - elucidation and validation of new targets of PdhR in Escherichia coli , 2011, BMC Systems Biology.

[6]  M. Schembri,et al.  Global gene expression in Escherichia coli biofilms , 2003, Molecular microbiology.

[7]  J. Curiel,et al.  Food phenolics and lactic acid bacteria. , 2009, International journal of food microbiology.

[8]  I. Gentle,et al.  Issues in determining factors influencing bacterial attachment: a review using the attachment of Escherichia coli to abiotic surfaces as an example , 2009, Letters in applied microbiology.

[9]  Michael Niaounakis,et al.  Olive Processing Waste Management: Literature Review and Patent Survey , 2006 .

[10]  Woojun Park,et al.  Antipathogenic properties of green tea polyphenol epigallocatechin gallate at concentrations below the MIC against enterohemorrhagic Escherichia coli O157:H7. , 2009, Journal of food protection.

[11]  Thomas K. Wood,et al.  YliH (BssR) and YceP (BssS) Regulate Escherichia coli K-12 Biofilm Formation by Influencing Cell Signaling , 2006, Applied and Environmental Microbiology.

[12]  J. Selbig,et al.  Metabolomic and transcriptomic stress response of Escherichia coli , 2010, Molecular systems biology.

[13]  L. Bret,et al.  Indole can act as an extracellular signal to regulate biofilm formation of Escherichia coli and other indole-producing bacteria. , 2003, Canadian journal of microbiology.

[14]  N. Russell,et al.  Bioremediation and biovalorisation of olive-mill wastes , 2009, Applied Microbiology and Biotechnology.

[15]  Suzanne M. Paley,et al.  Browsing metabolic and regulatory networks with BioCyc. , 2012, Methods in molecular biology.

[16]  M. Gasson,et al.  Antimicrobial activity of flavonoids extracted from bergamot (Citrus bergamia Risso) peel, a byproduct of the essential oil industry , 2007, Journal of applied microbiology.

[17]  Steven C. Huber,et al.  The Orphan Gene ybjN Conveys Pleiotropic Effects on Multicellular Behavior and Survival of Escherichia coli , 2011, PloS one.

[18]  W. Liang,et al.  TM4 microarray software suite. , 2006, Methods in enzymology.

[19]  G. Morozzi,et al.  Health and sensory properties of virgin olive oil hydrophilic phenols: agronomic and technological aspects of production that affect their occurrence in the oil. , 2004, Journal of chromatography. A.

[20]  T. Wood,et al.  Stationary-Phase Quorum-Sensing Signals Affect Autoinducer-2 and Gene Expression in Escherichia coli , 2004, Applied and Environmental Microbiology.

[21]  Chankyu Park,et al.  Transcriptional Activation of the Aldehyde Reductase YqhD by YqhC and Its Implication in Glyoxal Metabolism of Escherichia coli K-12 , 2010, Journal of bacteriology.

[22]  Jessica D. Schiffman,et al.  Biodegradable polymer (PLGA) coatings featuring cinnamaldehyde and carvacrol mitigate biofilm formation. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[23]  Q. She,et al.  A Putative ABC Transporter Is Involved in Negative Regulation of Biofilm Formation by Listeria monocytogenes , 2008, Applied and Environmental Microbiology.

[24]  A. Bren,et al.  How Signals Are Heard during Bacterial Chemotaxis: Protein-Protein Interactions in Sensory Signal Propagation , 2000, Journal of bacteriology.

[25]  S. Sayadi,et al.  Changes in microbial and soil properties following amendment with treated and untreated olive mill wastewater. , 2006, Microbiological research.

[26]  Søren Molin,et al.  Global impact of mature biofilm lifestyle on Escherichia coli K‐12 gene expression , 2003, Molecular microbiology.

[27]  C. Prigent-Combaret,et al.  Complex Regulatory Network Controls Initial Adhesion and Biofilm Formation in Escherichia coli via Regulation of thecsgD Gene , 2001, Journal of bacteriology.

[28]  M. Servili,et al.  Functional milk beverage fortified with phenolic compounds extracted from olive vegetation water, and fermented with functional lactic acid bacteria. , 2011, International journal of food microbiology.

[29]  N. Tufenkji,et al.  The Swarming Motility of Pseudomonas aeruginosa Is Blocked by Cranberry Proanthocyanidins and Other Tannin-Containing Materials , 2011, Applied and Environmental Microbiology.

[30]  G. Smirnova,et al.  Influence of polyphenols on Escherichia coli resistance to oxidative stress. , 2009, Free radical biology & medicine.

[31]  Pablo Tamayo,et al.  Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Yongjun Feng,et al.  Indole Affects Biofilm Formation in Bacteria , 2010, Indian Journal of Microbiology.

[33]  T. Wood,et al.  Motility influences biofilm architecture in Escherichia coli , 2006, Applied Microbiology and Biotechnology.

[34]  G. Schoolnik,et al.  The bundle‐forming pili of enteropathogenic Escherichia coli: transcriptional regulation by environmental signals , 1996, Molecular microbiology.

[35]  A Roig,et al.  An overview on olive mill wastes and their valorisation methods. , 2006, Waste management.

[36]  B. de Las Rivas,et al.  Genome-wide transcriptomic responses of a human isolate of Lactobacillus plantarum exposed to p-coumaric acid stress. , 2012, Molecular nutrition & food research.

[37]  Miroslaw Cygler,et al.  Genetic selection designed to stabilize proteins uncovers a chaperone called Spy , 2011, Nature Structural &Molecular Biology.

[38]  T. Abee,et al.  Bacterial SOS response: a food safety perspective. , 2011, Current opinion in biotechnology.

[39]  Kees Sonneveld,et al.  Antimicrobial properties of basil and its possible application in food packaging. , 2003, Journal of agricultural and food chemistry.

[40]  Brad T. Sherman,et al.  Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources , 2008, Nature Protocols.

[41]  M. Winterhalter,et al.  The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria , 2008, Nature Reviews Microbiology.

[42]  P. Watnick,et al.  Identification of novel stage‐specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development , 2005, Molecular microbiology.

[43]  J. Wain,et al.  Exposure of Escherichia coli and Salmonella enterica serovar Typhimurium to triclosan induces a species-specific response, including drug detoxification. , 2009, The Journal of antimicrobial chemotherapy.

[44]  R. Perry,et al.  Polyamines Are Essential for the Formation of Plague Biofilm , 2006, Journal of bacteriology.

[45]  M. D'Archivio,et al.  Bioavailability of the Polyphenols: Status and Controversies , 2010, International journal of molecular sciences.

[46]  M. Humphrys,et al.  NsrR targets in the Escherichia coli genome: new insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility , 2009, Molecular microbiology.

[47]  T. Wood,et al.  YcfR (BhsA) Influences Escherichia coli Biofilm Formation through Stress Response and Surface Hydrophobicity , 2007, Journal of bacteriology.

[48]  R. Tibshirani,et al.  Significance analysis of microarrays applied to the ionizing radiation response , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[49]  F. Soyer,et al.  Antimicrobial and antioxidant activities of Turkish extra virgin olive oils. , 2010, Journal of agricultural and food chemistry.

[50]  Jung-Ae Kim,et al.  Apple Flavonoid Phloretin Inhibits Escherichia coli O157:H7 Biofilm Formation and Ameliorates Colon Inflammation in Rats , 2011, Infection and Immunity.

[51]  Luis H. Reyes,et al.  Genomic Library Screens for Genes Involved in n-Butanol Tolerance in Escherichia coli , 2011, PloS one.

[52]  M. A. De la Cruz,et al.  The Complexities of Porin Genetic Regulation , 2010, Journal of Molecular Microbiology and Biotechnology.

[53]  A. Ehrenreich DNA microarray technology for the microbiologist: an overview , 2006, Applied Microbiology and Biotechnology.

[54]  P. Cioni,et al.  Effects of oregano, carvacrol and thymol on Staphylococcus aureus and Staphylococcus epidermidis biofilms. , 2007, Journal of medical microbiology.