Basic and applied aspects of microbial adhesion at the hydrocarbon:water interface.

Microbial hydrophobicity has been studied since 1924. During the last decade, various techniques have become available for measuring hydrophobic surface properties of microbial cells. This has led to a surge in investigations suggesting a role for hydrophobicity in adhesion of bacteria to an array of surfaces (oral surfaces, mineral particles, fatty meat, epithelial cells, phagocytes, biomaterials), partitioning at interfaces, as well as gliding mobility. The present manuscript comprises a critical, chronological look at the origins of microbial hydrophobicity research, its development, origins, and applications. Emphasis is placed on microbial adhesion to hydrocarbons, a technique with which the author has the most experience and research interest.

[1]  M. Rosenberg,et al.  Separation of amphipathic proteins based on adsorption to hexadecane:water interfaces. , 1986, Preparative biochemistry.

[2]  P. M. Foegeding,et al.  Comparison of coats and surface‐dependent properties of Bacillus cereus T prepared in two sporulation environments , 1988 .

[3]  T. Kanamoto,et al.  Surface hydrophobicity, adherence, and aggregation of cell surface protein antigen mutants of Streptococcus mutans serotype c , 1990, Infection and immunity.

[4]  E. Beachey,et al.  Hydrophobic interactions of group A streptococci with hexadecane droplets , 1983, Journal of bacteriology.

[5]  G. Goma,et al.  Mechanism of enhanced oxygen transfer in fermentation using emulsified oxygen‐vectors , 1990, Biotechnology and bioengineering.

[6]  D. Lichtenberg,et al.  A kinetic approach to bacterial adherence to hydrocarbon , 1985 .

[7]  J. Pijck,et al.  Bioluminescence Assay for Measuring the Number of Bacteria Adhering to the Hydrocarbon Phase in the BATH Test , 1988, Applied and environmental microbiology.

[8]  R. Ellen,et al.  Bacteroides gingivalis-Actinomyces viscosus cohesive interactions as measured by a quantitative binding assay , 1987, Infection and immunity.

[9]  L. Öhman,et al.  NON-SPECIFIC AND SPECIFIC RECOGNITION MECHANISMS OF BACTERIAL AND MAMMALIAN CELL MEMBRANES , 1985 .

[10]  D. A. Carter,et al.  Cell surface mutants of Streptococcus sanguis with altered adherence properties. , 1988, Oral microbiology and immunology.

[11]  A. Matsumoto,et al.  Surface Properties of Staphylococcus aureus Affecting Chemiluminescence Response of Human Phagocytes , 1990, Microbiology and immunology.

[12]  E. Rosenberg,et al.  Role of adherence in growth of Acinetobacter calcoaceticus RAG-1 on hexadecane , 1981, Journal of bacteriology.

[13]  E. Rosenberg,et al.  Oil tankers and pollution: a microbiological approach. , 1977, Annual review of microbiology.

[14]  M. Coulter,et al.  Utilization of a Continuous Streptococcal Surface to Measure Interbacterial Adherence in vitro and in vivo , 1988, Journal of dental research.

[15]  E. Rosenberg,et al.  Emulsifier of Arthrobacter RAG-1: specificity of hydrocarbon substrate , 1979, Applied and environmental microbiology.

[16]  E. Bayer,et al.  Adherence of Acinetobacter calcoaceticus RAG-1 to human epithelial cells and to hexadecane , 1981, Infection and immunity.

[17]  E. Weiss,et al.  Desorption of adherent bacteria from a solid hydrophobic surface by oil , 1983 .

[18]  N. Georgopapadakou,et al.  Routes of quinolone permeation in Escherichia coli , 1988, Antimicrobial Agents and Chemotherapy.

[19]  K. Marshall,et al.  Interfaces in Microbial Ecology , 1976 .

[20]  E. Rosenberg,et al.  Sequential growth of bacteria on crude oil. , 1975, Applied microbiology.

[21]  L. Erickson,et al.  Characteristics of hydrocarbon uptake in cultures with two liquid phases , 1977, Biotechnology and bioengineering.

[22]  D. Hart,et al.  Changes in the hydrophobic-hydrophilic cell surface character of Halomonas elongata in response to NaCl , 1988, Journal of bacteriology.

[23]  A. J. Godfrey,et al.  Cell surface changes in Pseudomonas aeruginosa PAO4069 in response to treatment with 6-aminopenicillanic acid , 1989, Antimicrobial Agents and Chemotherapy.

[24]  N. Cheville,et al.  Penetration and intracellular growth of Brucella abortus in nonphagocytic cells in vitro , 1990, Infection and immunity.

[25]  Mel Rosenberg,et al.  Hydrophobic interactions: role in bacterial adhesion , 1986 .

[26]  E. Rosenberg,et al.  Emulsifier of Arthrobacter RAG-1: isolation and emulsifying properties , 1979, Applied and environmental microbiology.

[27]  M. Rosenberg Concentration of larvicidal Bacillus spores at the water surface by adherence to oil droplets , 1986 .

[28]  J. Tomás,et al.  Isolation and characterization of Klebsiella pneumoniae unencapsulated mutants , 1989, Journal of clinical microbiology.

[29]  K A Dill,et al.  The meaning of hydrophobicity. , 1990, Science.

[30]  C. E. Rice,et al.  The Behaviour of Acid-fast Bacteria in Oil and Water Systems , 1931, Journal of Bacteriology.

[31]  R. E. Lincoln,et al.  Separation and Concentration of Bacterial Spores and Vegetative Cells by Foam Flotation , 1958, Applied microbiology.

[32]  Eugene Rosenberg,et al.  Adherence of bacteria to hydrocarbons: A simple method for measuring cell‐surface hydrophobicity , 1980 .

[33]  S. Rumelt,et al.  Clearance of Serratia marcescens from blood in mice: role of hydrophobic versus mannose-sensitive interactions , 1988, Infection and immunity.

[34]  A. Gaudin,et al.  Separation of Microorganisms by Flotation , 1960, Applied microbiology.

[35]  R. Colwell,et al.  Microbial degradation of hydrocarbons in the environment. , 1990, Microbiological reviews.

[36]  M. V. van Loosdrecht,et al.  The role of bacterial cell wall hydrophobicity in adhesion , 1987, Applied and environmental microbiology.

[37]  M. Rosenberg,et al.  Effect of Cetylpyridinium Chloride on Microbial Adhesion to Hexadecane and Polystyrene , 1990, Applied and environmental microbiology.

[38]  Z. Skobe,et al.  Association of fimbriae with the hydrophobicity of Streptococcus sanguis FC-1 and adherence to salivary pellicles , 1983, Infection and immunity.

[39]  M. Drucker,et al.  Bacterial adherence to intravenous catheters and needles and its influence by cannula type and bacterial surface hydrophobicity. , 1986, The Journal of laboratory and clinical medicine.

[40]  S. M. Barnett,et al.  Microbial growth on hydrocarbons—some experimental results , 1975 .

[41]  R. Wolkin,et al.  Selection for Nonadherent or Nonhydrophobic Mutants Co-selects for Nonspreading Mutants of Cytophaga johnsonae and Other Gliding Bacteria , 1985 .

[42]  E. J. Morris,et al.  Cell surface components of Streptococcus sanguis: relationship to aggregation, adherence, and hydrophobicity , 1985, Journal of bacteriology.

[43]  M. Rosenberg,et al.  Isolation of pigmented and nonpigmented mutants of Serratia marcescens with reduced cell surface hydrophobicity , 1984, Journal of bacteriology.

[44]  H. D. Singh,et al.  Different modes of hydrocarbon uptake by two Pseudomonas species , 1991, Biotechnology and bioengineering.

[45]  M. Okazaki,et al.  Assimilation of liquid hydrocarbon by microorganisms. I. Mechanism of hydrocarbon uptake , 1977, Biotechnology and bioengineering.

[46]  E. Rosenberg,et al.  Bacterial adherence at the hydrocarbon-water interface , 1985 .

[47]  P. M. Foegeding,et al.  Involvement of the spore coat in germination of Bacillus cereus T spores , 1987, Applied and environmental microbiology.

[48]  Oakley Jd,et al.  Trypsin-susceptible cell surface characteristics of Streptococcus sanguis. , 1985 .

[49]  S. Mudd,et al.  THE PENETRATION OF BACTERIA THROUGH CAPILLARY SPACES : IV. A KINETIC MECHANISM IN INTERFACES. , 1924 .

[50]  M. Rosenberg,et al.  Mechanism of enhancement of microbial cell hydrophobicity by cationic polymers , 1990, Journal of bacteriology.

[51]  C. J. van Oss,et al.  Phagocytosis as a surface phenomenon. V. Contact angles and phagocytosis of rough and smooth strains of Salmonella typhimurium, and the influence of specific antiserum. , 1975, Immunological communications.

[52]  O. Leon,et al.  Streptococcus pyogenes clinical isolates and lipoteichoic acid , 1990, Infection and immunity.

[53]  T. McMeekin,et al.  The effect of potassium sorbate on the structural integrity of Alteromonas putrefaciens , 1988 .

[54]  A. G. McLee,et al.  Linear growth of a Torulopsis sp. on n-alkanes. , 1972, Canadian journal of microbiology.

[55]  M. J. Kennedy,et al.  Environmental alteration and phenotypic regulation of Candida albicans adhesion to plastic , 1989, Infection and immunity.

[56]  S. Mudd,et al.  CERTAIN INTERFACIAL TENSION RELATIONS AND THE BEHAVIOR OF BACTERIA IN FILMS , 1924, The Journal of experimental medicine.

[57]  W. Bishop,et al.  Molecular and macroscopic aspects of cavity formation in the hydrophobic effect. , 1987, Biophysical chemistry.

[58]  Forces Between Surfaces in Liquids , 1988, Science.

[59]  S. Craven,et al.  Changes in the hydrophobic characteristics of Clostridium perfringens spores and spore coats by heat. , 1987, Canadian journal of microbiology.

[60]  J. N. Baruah,et al.  A kinetic model for microbial growth on solid hydrocarbons , 1972 .

[61]  M. Koohmaraie,et al.  Cell surface charge characteristics and their relationship to bacterial attachment to meat surfaces , 1989, Applied and environmental microbiology.

[62]  R. Colwell,et al.  Mercury-resistant bacteria and petroleum degradation. , 1974, Applied microbiology.

[63]  H. Verbrugh,et al.  Heterogeneity in opsonic requirements of Staphylococcus epidermidis: relative importance of surface hydrophobicity, capsules and slime. , 1989, Immunology.

[64]  J. Freney,et al.  Cell surface hydrophobicity of 88 clinical strains of Acinetobacter baumannii. , 1990, Research in microbiology.

[65]  S. Klotz,et al.  The contribution of bacterial surface hydrophobicity to the process of adherence of Pseudomonas aeruginosa to hydrophilic contact lenses. , 1989, Current eye research.

[66]  T. Koshikawa,et al.  Surface hydrophobicity of spores of Bacillus spp. , 1989, Journal of general microbiology.

[67]  C. J. Oss,et al.  Phagocytosis as a Surface Phenomenon , 1978 .

[68]  P. Lambert,et al.  Iron depletion alters surface-associated properties of Staphylococcus aureus and its association to human neutrophils in chemiluminescence. , 1989, FEMS microbiology letters.

[69]  P. M. Foegeding,et al.  Hydrophobicity of Bacillus and Clostridium spores , 1990, Applied and environmental microbiology.

[70]  R. Doyle,et al.  Hydrophobic interactions and the adherence of Streptococcus sanguis to hydroxylapatite , 1982, Infection and immunity.

[71]  R. Ellen,et al.  Adhesion of Actinomyces viscosus to Porphyromonas (Bacteroides) gingivalis-coated hexadecane droplets , 1991, Journal of bacteriology.

[72]  Norbert Muller,et al.  Search for a realistic view of hydrophobic effects , 1990 .

[73]  P. Lambert,et al.  Penetration of immunoglobulins through the Klebsiella capsule and their effect on cell-surface hydrophobicity. , 1988, Journal of medical microbiology.

[74]  E. Rosenberg,et al.  Properties of hydrocarbon‐in‐water emulsions stabilized by Acinetobacter RAG‐1 emulsan , 1982, Biotechnology and bioengineering.

[75]  A. E. Toranzo,et al.  Influence of the growth conditions on the hydrophobicity of Renibacterium salmoninarum evaluated by different methods. , 1989, FEMS microbiology letters.

[76]  Paul Rouxhet,et al.  Methods for Measuring Hydrophobicity of Microorganisms , 1987 .

[77]  M. A. Martin,et al.  Use of cellular hydrophobicity, slime production, and species identification markers for the clinical significance of coagulase-negative staphylococcal isolates. , 1989, American journal of infection control.

[78]  M. Rosenberg,et al.  Putative role of a 70 kDa outer-surface protein in promoting cell-surface hydrophobicity of Serratia marcescens RZ. , 1989, Journal of general microbiology.

[79]  T. Kato,et al.  Neuraminidase-enhanced attachment of Bacteroides intermedius to human erythrocytes and buccal epithelial cells , 1989, Infection and Immunity.

[80]  D. Harty,et al.  Expression of the surface properties of the fibrillar Streptococcus salivarius HB and its adhesion deficient mutants grown in continuous culture under glucose limitation. , 1989, Journal of general microbiology.

[81]  Y. Iimura,et al.  Cell Surface Hydrophobicity as a Pellicle Formation Factor in Film Strain of Saccharomyces , 1980 .

[82]  J. Remon,et al.  Kinetics of Pseudomonas aeruginosa adhesion to 304 and 316-L stainless steel: role of cell surface hydrophobicity , 1990, Applied and environmental microbiology.

[83]  S. Hjertén,et al.  A new test based on ‘salting out’ to measure relative hydrophobicity of bacterial cells , 1981 .

[84]  Van Oss Cj,et al.  Phagocytosis as a surface phenomenon. Contact angles and phagocytosis of non-opsonized bacteria. , 1972 .

[85]  K. R. Gurijala,et al.  Effect of growth rate and hydrophobicity on bacteria surviving protozoan grazing , 1990, Applied and environmental microbiology.

[86]  D. Sharon,et al.  Measurement of the kinetics of bacterial adherence to hexadecane in polystyrene cuvettes , 1986 .

[87]  M. Rosenberg,et al.  Cell surface hydrophobicity of dental plaque microorganisms in situ , 1983, Infection and immunity.

[88]  R. Gibbons,et al.  Interbacterial aggregation of plaque bacteria. , 1970, Archives of oral biology.

[89]  S. Hjertén,et al.  Differences in hydrophobic surface characteristics of porcine enteropathogenic Escherichia coli with or without K88 antigen as revealed by hydrophobic interaction chromatography , 1978, Infection and immunity.

[90]  J. Zajic,et al.  Cell Surface Measurements in Hydrocarbon and Carbohydrate Fermentations , 1980, Applied and environmental microbiology.

[91]  D I Wang,et al.  Measurements on the interfacial areas of hydrocarbon in yeast fermentations and relationships to specific growth rates , 1972, Biotechnology and bioengineering.

[92]  E. Bayer,et al.  Role of Thin Fimbriae in Adherence and Growth of Acinetobacter calcoaceticus RAG-1 on Hexadecane , 1982, Applied and environmental microbiology.

[93]  K. Kristinsson Adherence of staphylococci to intravascular catheters. , 1989, Journal of medical microbiology.

[94]  A. Fiechter,et al.  The mode of interaction between the substrate and cell surface of the hydrocarbon‐utilizing yeast Candida tropicalis , 1976, Biotechnology and bioengineering.

[95]  H. Busscher,et al.  Adhesion of Streptococcus sanguis CH3 to polymers with different surface free energies , 1985, Applied and environmental microbiology.