Bacterial Biofilms and Biofouling: Translational Research in Marine Biotechnology

Marc W. Mittelman

Biological fouling (“biofouling”) of engineered materials has been a significant problem for military and civilian oceangoing vessels. Materials deterioration, losses in heat-transfer efficiency, and mechanical blockages of fluid transport systems can result from biological fouling activities. These problems can also influence fuel consumption; for example, it has been estimated that 10% or more of fuel consumed by large naval vessels is required to overcome the viscous drag imposed by fouling organisms on ship hulls. In addition to the direct economic problems created by the activities of micro- and macrofouling organisms, the operational readiness of military vessels is influenced by the frequency of repairs and preventive maintenance activities that result from biological fouling.

The Office of Naval Research (ONR) has been the primary government-funding agency for biofouling research worldwide. Both basic and applied research have been supported under various ONR programs. Research to date has focused on the biology, ecology, detection, and treatment of putative fouling organisms. In addition, significant work has been funded in the fields of environmental toxicology and materials sciences.

Mechanisms associated with marine biofouling activities are, in most cases, identical to those seen in industrial fluid handling operations. Biological fouling is a major problem that results in significant environmen-

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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP Bacterial Biofilms and Biofouling: Translational Research in Marine Biotechnology Marc W. Mittelman Biological fouling (“biofouling”) of engineered materials has been a significant problem for military and civilian oceangoing vessels. Materials deterioration, losses in heat-transfer efficiency, and mechanical blockages of fluid transport systems can result from biological fouling activities. These problems can also influence fuel consumption; for example, it has been estimated that 10% or more of fuel consumed by large naval vessels is required to overcome the viscous drag imposed by fouling organisms on ship hulls. In addition to the direct economic problems created by the activities of micro- and macrofouling organisms, the operational readiness of military vessels is influenced by the frequency of repairs and preventive maintenance activities that result from biological fouling. The Office of Naval Research (ONR) has been the primary government-funding agency for biofouling research worldwide. Both basic and applied research have been supported under various ONR programs. Research to date has focused on the biology, ecology, detection, and treatment of putative fouling organisms. In addition, significant work has been funded in the fields of environmental toxicology and materials sciences. Mechanisms associated with marine biofouling activities are, in most cases, identical to those seen in industrial fluid handling operations. Biological fouling is a major problem that results in significant environmen- Altran Corporation, Boston, MA

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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP tal impacts, both directly and indirectly through the misuse and misapplication of biocides. The biocide business in the United States is a multibillion dollar business, and there are a number of Fortune 500 companies with products and services designed to control biofouling in industrial systems. Bacterial biofilms (Figure 1) are the root cause of biofouling in most industrial systems. A biofilm is an agglomeration of bacteria on a surface that is surrounded or held together by extracellular polymeric substances. Bacteria produce extracellular polymeric substances, in part, to help them attach to surfaces and bind to one another. However, polymers also have a number of ancillary benefits, such as metal binding, which afford labile cellular components (e.g., sulfhydryl groups) some protection from otherwise toxic effects of heavy metals. Due to their size and net negative charge, bacteria in solution act as colloidal particles. Their physicochemical behavior is much like that of clay particles, albeit clay particles with purposive behavior. A significant amount of ONR-sponsored research has focused on exploring the sort of intimate associations that exist between bacteria and various surfaces, particularly in marine environments. Understanding factors that promote the transition of bacteria (and other fouling organisms) from a planktonic to a sessile state is essential to the development of effective biofouling monitoring and treatment programs. Biofouling involves the deleterious effects of microorganisms and some macroorganisms on engineered materials. These effects include FIGURE 1. Bacterial biofilm on 316 stainless steel

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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP mechanical blockages, significant losses in heat transfer, microbially influenced corrosion, product contamination, and threats to public health. Problems range from plugging of fire protection systems to microbially influenced corrosion of ferrous and nonferrous metals. In addition to fouling problems in industrial systems, bacterial biofilms are responsible for significant problems in medicine, particularly with implanted medical devices. The limiting factor in the more widespread application of such critical devices is infection—rather than materials engineering considerations or surgical techniques. For example, devices such as the total artificial heart have a 90-day useful life span. The vast majority of patients chronically catheterized with indwelling devices develop urinary tract infections, usually within about 10 days after catheterization. Urinary catheter-related biofilms are the single greatest cause of nosocomial infections in hospitals, accounting for significant mortality and morbidity among hospitalized patients. Marine research programs funded, for example, by ONR and the National Science Foundation have sponsored research into novel on-line detection mechanisms, physical treatments, development of antifouling compounds, adhesion-resistant surfaces, and antimicrobial coatings that might be useful for both industrial and medical applications. On-line detection techniques developed through research in the marine biotechnology arena have included evanescent wave technologies, fluorometry, acoustical monitoring, and electrochemical techniques. Evanescent wave technologies such as Fourier transform infrared and Raman spectroscopy have been applied to the detection of marine fouling organisms. A quartz crystal microbalance technology evolved from primarily Navy- and some Electric Power Research Institute-sponsored research as a way of evaluating on-line the development of organisms on surfaces. The US Navy has been very interested in developing on-line detection techniques that indicate both when the fouling problems are occurring and when to treat fouled surfaces. The development of novel biofouling control measures had its origins in marine biotechnology research programs. Some of these programs have included antifouling treatments for ship hulls, pipelines, and marine structures. For example, the Navy has sponsored research into acoustical wave treatments involving high-frequency pressure transducers. A significant amount of work has also been devoted to so-called “natural products.” Gorgonian coral is one source of animal-produced novel antifouling compounds; eelgrass is another example. Various extracts from marine animals and plants can be incorporated into antifouling paints and coatings, providing “natural” antifouling protection. These “natural product” antifoulants were discovered by marine biologists who observed that certain species of coral and marine plants were never colonized by

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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP bacteria, fungi, or higher organisms. In marine ecosystems, colonization space is a significant limiting factor for the development of many life forms. Therefore, the absence of colonizing marine organisms on these species of coral and marine plants was surprising. Further investigations revealed that gorgonian coral and eelgrass—among many others—produced complex organic compounds, which when extracted and applied to paints, similarly prevented colonization by fouling organisms. A number of investigators have conducted research into fouling release compounds. Very often these are nontoxic compounds, such as silicones that are released from surfaces with exposure to fluid shear stresses. These types of ablative coatings are gradually sloughed under flowing conditions, taking with them attached fouling organisms. The association of fouling release compounds research with medical devices could be in the development of so-called biomimetic surfaces—mimicking natural tissue surface moieties. Surfaces exhibiting, for example, heparin-like moieties might retard microbial attachment and subsequent adhesion. This brief discussion summarizes some of the key issues in this area of marine biotechnology research (Table 1). There is a wealth of information in the marine biotechnology arena, and the translation of much of this research into industrial and other environmental applications has yet to be realized. TABLE 1. Key Issues in the Translation of Marine Biotechnology Research into Industrial, Environmental, and Medical Arenas Issue Challenge Translation of marine research to industrial, medical, and environmental applications Paucity of research into the microbial ecology of fouling biofilms On-line monitoring for biofilms and biofouling Sensitivity and selectivity of analytical tools Novel antifouling compounds Toxicity and materials compatibility Commercialization of applicable marine biotechnology inventions Intellectual property considerations; economics

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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP REFERENCES Bremer PJ, Geesey GG. 1991 An evaluation of biofilm development utilizing non-destructive attenuated total reflectance Fourier transform infrared spectroscopy. Biofouling 3:89-100. Characklis WG 1990 Microbial biofouling control. In: Characklis WG, Marshall KC, eds. Biofilms. New York: John Wiley. p 585-633. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. 1995 Microbial biofilms. Ann Rev Microbiol 49:711-745. Davidson D, Beheshti B, Mittelman MW. 1996 Effects of Arthrobacter sp., Acidovorax delafieldii, and Bacillus megaterium colonisation on copper solvency in a laboratory reactor. Biofouling 9:279-292. Franklin MJ, Nivens DE, Vass AA, Mittelman MW, Jack RF, Dowling NJE, White DC. 1990 Effect of chlorine and chlorine/bromine biocide treatments on the number and activity of biofilm bacteria and on carbon steel corrosion Corrosion 47:128-134. Gu JD, Roman M, Esselman T, Mitchell R. 1998 The role of microbial biofilms in deterioration of space station candidate materials. Int Biodeter Biodegrad 41:25-33. Hirota H, Okino T, Yoshimura E, Fusetani N. 1998 Five new antifouling sesquiterpenes from two marine sponges of the genus Axinyssa and the nudibranch Phyllidia pustulosa.Tetrahedron 54:13971-13980. Maki JS, Patel G, Mitchell R. 1998 Experimental pathogenicity of Aeromonas spp. for the zebra mussel, Dreissenapolymorpha .Curr Microbiol 36:19-23. Marshall KC, Stout R, Mitchell R. 1971 Mechanisms of the initial events in the sorption of marine bacteria to surfaces. J Gen Microbiol 68:337-348. McCoy WF. 1998 Imitating natural fouling control. Mat Perform 37:45-48. Mittelman MW. 1994 Emerging techniques for the evaluation of bacterial biofilm formation and metabolic activity in marine and freshwater environments In: Morse D, ed. Recent Developments in the Control of Biodeterioration. London: Oxford University Press. p 49-56. Mittelman MW. 1997 Adhesion to biomaterials. In: Fletcher M, ed. The Molecular and Ecological Diversity of Bacterial Adhesion. New York: Wiley. p 89-127. Mittelman MW. 1997 Structure-function characteristics of bacterial biofilms in fluid processing operations. Guelph, Ontario: American Dairy Science Association. Vrolijk NH, Targett NM, Baier RE, Meyer AE. 1990 Surface characterization of two gorgonian coral species: Implications for a natural antifouling defense. Biofouling 2:39-54.