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Continuous Nondestructive Monitoring of Microbial Biofilms: a Review of Analytical Techniques DE Nivens 1,2, RJ Palmer Jr 2 and DC White Z3,4

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Continuous Nondestructive Monitoring of Microbial Biofilms: a Review of Analytical Techniques DE Nivens 1,2, RJ Palmer Jr 2 and DC White Z3,4 Journal of Indusb'ial Microbiology (1995) 15, 263-276 1995 Society for Industrial Microbiology0169-4146/95/$12.00 Continuous nondestructive monitoring of microbial biofilms: a review of analytical techniques DE Nivens 1,2, RJ Palmer Jr 2 and DC White z3,4 I Microbial Insights Inc, Knoxville, TN; 2Center for Environmental Biotechnology; 3Department of Microbiology, University of Tennessee, Knoxville, TN; 4Environmental Science Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA A fundamental requirement for the understanding and control of biofilms is the continuous nondestructive monitor- Downloaded from https://academic.oup.com/jimb/article/15/4/263/5988582 by guest on 28 September 2021 ing of biofilm processes. This paper reviews research analytical techniques that monitor biofilm processes in a continuous nondestructive manner and that could also be modified for industrial applications. To be considered 'continuous' and 'nondestructive' for the purpose of this review a technique must: (a) function in an aqueous sys- tem; (b)not require sample removal; (c) minimize signal from organisms or contaminants in the bulk phase; and (d) provide real-time data. Various microscopic, spectrochemical, electrochemical, and piezoelectrical analysis methods fulfill these criteria. These techniques monitor the formation of biofilms, the physiology of the microorgan- isms withiin biofilms, and/or the interaction of the biofilms with their environment. It is hoped that this review will stimulate development and use of biofilm monitoring techniques in industrial and environmental settings. Keywords: biofilm; on-line monitoring; nondestructive monitoring; microscopy; Fourier-transform infrared spectrometry; bio- luminescence; microelectrode; quartz crystal microbalanee Introduction within municipal water delivery systems (1 x l01 to 2.2 x 106 colony forming units per cm 2) [79] to the centi- A biofilm has been defined as ' ... cells immobilized meters-thick sludge blankets in sewage treatment sys- at a substratum and frequently embedded in an organic tems. A biofilm in a biotechnological treatment process polymer matrix of microbial origin ... which is not may be a bacterial monoculture, while natural biofilms necessarily uniform in time or space.., composed of a such as the periphyton covering streambed surfaces tend significant fraction of inorganic or abiotic substances to be made up of many species. The composition of a held together by the biotic matrix' [24]. Microbial com- biofilm typically includes (besides the organisms munities at gas-solid, gas-liquid, and liquid-liquid inter- themselves) trace organics which concentrate at surfaces, faces also exist [94], but are not considered here. Bac- extracellular polysaccharides elaborated by the bacteria, teria and microeukaryotes (fungi, algae, and protozoans) and particulate matter trapped in the polysaccharide readily attach to surfaces to form biofilms, and in nature matrix. The complexity and variability of biofilms can most microorganisms are attached rather than free in the significantly increase the difficulty of analysis. bulk-liquid phase. The importance of microbial biofilms Application of classical bacteriological techniques to the has been established in, for example, aquatic, soil, indus- study of industrial process problems such as biofouling and trial, and clinical environments [1,26,45,73]. Advantages corrosion has demonstrated that microorganisms can play for microorganisms within biofilms include increased a significant role in the corrosion of metals [89], the availability of nutrients concentrated on substrata, fix- deterioration of concrete [40], and the clogging of pipelines ation in a flowing system increasing the availability of and filters [116,132]. Heterogeneous distribution of dissolved nutrients, and the creation of 'microniches' microbes and/or their metabolic activity can promote such as anaerobic sites within an aerobic environment. microbiologically influenced corrosion. This multibillion Attachment can prevent transfer to a hostile environment dollar problem [106] is not well understood even after dec- such as, for oral microorganisms, from the hospitable ades of research. Microbial biofouling is ordinarily the pri- conditions of the mouth to the acidic anaerobic gut. The mary step in macrofouling (eg barnacle attachment) and disadvantages of life within a biofilm can include compe- results in a substantial decrease in the hydrodynamic tition for nutrients and the availability to predators of a efficiency of ship hulls [11]. Biofilms can seriously concentrated, sessile biomass. The structure, function, decrease the efficiency of heat transfer units [23]. Plank- and physiology of biofilms is beyond the scope of this tonic organisms in ultra-pure water are often a result of work, and ihas been extensively reviewed [23-25,94]. biofilm growth elsewhere in the system [107]. Biofilm for- The characteristics of individual biofilms are extremely variable. The cell density ranges from the mation on medical implants can be life-threatening because the body's natural defenses, even when augmented by extremely sparse communities of oligotrophic bacteria potent antibiotics, are usually ineffective against these infections [26]. Correspondence: DE Nivens, Microbial Insights, 201 Center Park Dr, In other biotechnological or bioremediation processes, it Suite 1140, Knoxville, Tennessee 37922-2105, USA is an advantage to promote biofilm formation and maintain Received 23 January 1995; accepted 8 June 1995 the active biomass. Municipal wastewater treatment is Continuousnondestructive monitoring of biofilms DE Nivenset al 264 largely dependent upon biodegradation of organic waste by digital microscopy have been complemented by rapid microbial biofilms and aggregates [83]. In situ biodegrad- advances in the number and selectivity of dyes used to ation of organic wastes in subsurface aquifers requires the detect biochemical and physiological characteristics of development of sufficiently active subsurface microbial cells. Many of these dyes have a low toxicity and can be biofilms [61]. The stability and productivity of many indus- washed out of the cells (eg fluorescein, certain rhodamines) trial bioprocessing and food fermentation procedures [139] thereby making repetitive staining (temporal is increased by the presence of appropriate microbial measurements) possible (R Palmer and J Almeida, Univ. biofilms. Biofilms are even implicated in the maintenance Tennessee, unpublished). of health in vertebrates--the microbiota attached to the Some of the earliest microscopic observations that could inner lining of the gut produce vitamins and aid in diges- be termed on-line were in situ microscopy of algae and tion [127]. bacteria in a pond [126], and temporal studies of soil bac- Consequently, it is important that biofilm microbial ecol- teria in capillary channels [5,110]. Staley [126] utilized a Downloaded from https://academic.oup.com/jimb/article/15/4/263/5988582 by guest on 28 September 2021 ogy be understood so that biofilm development can be pre- partially immersed microscope to observe the colonization vented or advantageously manipulated. Unfortunately, the of a slide by bacteria and algae. The capillary technique, most commonly applied methods are destructive, requiring which was used to follow the growth of bacteria with dis- either samples of the biofilm-substratum system, or removal tinctive morphologies such as Caulobacter and Pedomicro- of the biofilm from the substratum. This often results in bium, has never been widely used because it requires speci- disruption of the biofilm and usually requires the biofilm alized glassware and because conditions within the to pass through an air-water interface which can damage capillary (Eh, pH, oxygen tension) could not be controlled and/or contaminate the sample. The three-dimensional or monitored. architecture of a biofilm will be lost if analysis procedures The problems of microscopy under field conditions are require fixed and dried samples. Methods for removing difficult, and a more convenient way to examine attached biofilms from the substratum are inefficient and may cause microorganisms is through the use of flowcells. Laminar lysis of the cells. If organisms recovered through biofilm flow conditions can be created in parallel-plate flowcells, removal are regrown ex situ, they are then subject to severe and microscopy of the biofilm that develops on a glass sub- selection by the medium [1,117,135]. However, the greatest stratum can be performed [21]. The flowcells, which are problem with destructive analyses is that the inherent varia- simple, versatile, and inexpensive modifications on a design bility of successive samples may completely mask the originated by Berg and Block [9], can be adapted for development of the biofilm over time. microscopy of biofilms under a wide variety of conditions. The problems outlined above can best be overcome by Movement of Pseudomonas fluorescens within the hydro- use of continuous nondestructive monitoring techniques. dynamic boundary layer was examined photomicroscop- For the purpose of this review, a technique is classified ically [75]. Images were analyzed using the 'turnkey' IBAS as continuous and nondestructive if it allows direct system (Kontron, West Germany). The same techniques measurement of biofilm parameters in an aqueous system were used to examine the effect of laminar flow velocity in real time. Furthermore, the technique should be nonin- on attachment and
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