Article

Protozoan feeding on natural and cultured bacteria deposited on inert polymeric and mineral membrane filters

Authors:
  • The Scottish Association for Marine Science
To read the full-text of this research, you can request a copy directly from the authors.

Abstract

Early stages of development of marine bacterial biofilms were represented by cultured or freshly‐collected natural bacteria radiolabelled and deposited on 0.2 μm pore size polycarbonate (Nuclepore) or aluminium oxide (Anopore) filters. A proportion of the bacteria gradually resuspended themselves, but few were lost from the mineral filters; larger quantities of bacteria were lost from the surfaces of filters (especially the mineral ones) in the presence of un‐specialised protozoa than in the absence of protozoa. The extent of grazing on deposited bacteria and the assimilation of bacterial biomass was measured separately for the flagellates Paraphysomonas imperforata, Pteridomonas danica and Cafeteria menbergensis and the ciliate Uronema marinum. Deposited bacteria were grazed similarly by all four protozoa to the extent of about 25% from polymeric filters and 7% from mineral filters. The proportion of the consumed biomass of cultured Vibrio natriegens that was assimilated by protozoa ranged between 10 and 20%, while between 25% (Cafeteria) and 65% (Pteridomonas) of the consumed natural bacterial biomass was assimilated.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the authors.

... When NZ particles and planktonic cultures of A. junii were added separately, the grazing pressure from the protozoa was not substantial enough to prevent the bacteria from multiplying actively and forming biofilms on the NZ particles ( Table 1). The protection of immobilized A. junii from ciliate grazing can be compared to a study by Zubkov and Sleigh (1999), where grazing of bacteria from marine biofilms amounted to 25% of the biofilm on polymeric filters and up to 7% of the biofilm on mineral filters. ...
Article
Extreme environmental conditions, such as pH fluctuations, high concentrations of toxicants or grazing of protozoa, can potentially be found in wastewater treatment systems. This study was carried out to provide specific evidence on how 'bioparticles' can resist these conditions. The term 'bioparticle' is used to describe a particle comprising natural zeolitized tuff with a developed biofilm of the phosphate-accumulating bacterial species, Acinetobacter junii, on the surface. The bacteria in the biofilm were protected from the negative influence of extremely low pH, high concentrations of benzalkonium-chloride and grazing by Paramecium caudatum and Euplotes affinis, even under conditions that caused complete eradication of planktonic bacteria. During an incubation of 24 h, the biofilms were maintained and bacteria detached from the bioparticles, thus bioaugmenting the wastewater. The bioparticles provided a safe environment for the survival of bacteria in harsh environmental conditions and could be used for successful bioaugmentation in wastewater treatment plants.
Article
This chapter reviews the corresponding information on protozoa in biofilms, such as their grazing rates, evidence of nutrient remineralization, and their susceptibility to mesoinvertebrate grazing. Protozoan participation in the formation and maintenance of freshwater biofilms has received little attention even though it has been estimated that 99% of microbial activity is associated with surfaces. The behavior of protozoan differs from planktons in the biofilm because of the different protozoan community structure in biofilms. Protozoans exhibit a variety of mechanisms to capture their prey, and this has led to a considerable diversification of protozoan morphologies. However, for simplicity sake they can be divided into amoebae, flagellates, and ciliates. In addition, the close proximity of microbial components could lead to increased levels of cell–cell signaling and increased interaction with pathogenic bacteria. Only a handful of studies have attempted to quantify the grazing impact of these biofilm-associated protozoa but a picture is now starting to develop, though it is far from complete.
Article
The chapter focuses on mycological aspects of the genus Metarhizium. The genus includes several species, varieties within species, and individual isolates with broad ranges of physiological traits—including host range. The interactions of these fungi with their hosts, and the large literature on their use for pest control, largely define the scientific and popular concepts of Metarhizium spp. Fungi of the hyphomycete genus Metarhizium have been isolated from infected insects and soil. Although some isolates of these fungi have rather restricted host ranges, the group is better known for its ability to kill a wide spectrum of insects, including insects in at least seven orders. The common name for Metarhizium-induced disease is “green muscardine,” based on the encrustation of insect cadavers with green conidia. The rapid increase in research on Metarhizium, followed by sustained high scientific output, can be explained by several important worldwide attitude changes and the initiation of several promising Metarhizium-based pest-control and molecular-biology efforts.
Article
An improved method for qualitative and quantitative sampling of bacterial endospores using Fourier transform infrared (FT-IR) microscopy on gold-coated porous alumina membranes is presented. Bacillus subtilis endospores were filtered onto gold-coated alumina membranes serving as substrates. Studies in the mid-infrared (MIR) region revealed the characteristic bacterial absorption spectrum at low surface concentration, while scanning electron microscopy (SEM) images of the same samples provided precise calculation of the surface concentration of the bacterial endospores. Under the conditions of study, the average concentration of endospores was determined to be 1356 +/- 35 spores in a 100 x 100 mum(2) area, with a relative standard deviation of 0.0260. Examination of ten random spots on multiple substrates with FT-IR microscopy apertured to the same area gave an average relative standard deviation of 0.0482 in the signal strength of the amide A band at 3278 cm(-1). An extinction cross-section in reflection of sigma(ext) = (7.8 +/- 0.6) x 10(-9) cm(2)/endospore was calculated for the amide A band at the frequency of its peak absorbance, 3278 cm(-1). The absorption cross-section of the amide A band in reflection is estimated to be sigma(abs) approximately (2.10 +/- 0.12) x 10(-9) cm(2)/endospore.
Article
Full-text available
In contrast to the widely held view that microorganisms respond rapidly to changes in environmental conditions, the microbes in biofilms appear remarkably resilient to substantial changes in the abundance of dissolved organic substrates. Removal of high-molecular-weight dissolved materials from waters supplied to river biofilms generally did not affect bacterial densities or the synthesis of phospholipids and DNA. Even the complete elimination of exogenous materials from the overlying waters allowed heterotrophic activity to continue unaffected. Moreover, that continued activity was not supported by the catabolism of endogenous reserves of C (poly$-hydroxy alkanoate-PHA). The addition of inorganic nutrients to substrate-free waters allowed heterotrophic activity to increase within the biofilm. Since neither exogenous sources of river DOC or endogenous reserves (PHA) served as the source of C, we propose that an alternative, namely the poly-saccharide matrix (and any absorbed or incorporated organic matter), served as the primary carbon reserve for biofilm microorganisms during the imposed organic substrate deprivation.
Article
Full-text available
Benthic foraminifera from temperate tidal flats and shallow Antarctic waters were challenged with bacterial biofilms to assess possible foraminiferal impact on attached bacterial populations. Two tectinous species (Allogromia sp. and A. laticollaris) used pseudopodial networks to rend and ingest biofilm parcels, an activity we term harvesting. The numerical density of bacteria in harvested biofilm areas was maximally depleted by ca 80 % for Allogromia sp. and 50 % for A. laticollaris. In contrast, the calcareous (Cyclogyra antarctica, Elphidium incertum, Glandulina antarctica, Pyrgo williamsoni) and agglutinated (Astrammina rara, Astrorhiza sp., Crithionina-like mudball) foraminifera studied did not exhibit harvesting behavior. Time-lapse microscopy revealed that biofilm parcels were transported extracellularly toward the cell body by pseudopodia, an observation which further defines pseudopodial function in foraminiferal trophic mechanisms. Our observations indicate that allogromiid foraminifera may play a previously unrecognized role in bacterial population dynamics and nutrient cycling, particularly in intertidal environments and certain deep-sea habitats where they may constitute a major meiofaunal component.
Article
Full-text available
Heterotrophic protists, mostly flagellates, encountered in association with marine detritus from various collections in the mid North Atlantic are described. About 40 species have been identified and are reported. Taxa reported here for the first time are: Caecitellus gen. nov. (Protista incertae sedis) and Ministeria marisola gen. nov., sp. nov. (Protista incertae sedis). The flagellates form a subset of the community of heterotrophic marine flagellates encountered in more productive marine sites. Most species are bacterivorous and small. The community extends to the ocean floor but the diversity is reduced in samples taken from greater depths. The decline in species diversity is linked also to a decline in numbers of individuals. We discuss these changes in relation to food supply and pressure effects.
Article
Full-text available
We report a novel in vitro method which, through application of appropriate nutrient limitations, enables growth rate control of adherent bacterial populations. Exponentially growing cells are collected by pressure filtration onto cellulose acetate membranes. Following inversion into the bases of modified fermentors, membranes and bacteria are perfused with fresh medium. Newly formed and loosely attached cells are eluted with spent medium. Steady-state conditions (dependent upon the medium flow rate) at which the adherent bacterial biomass is constant and proportional to the limiting nutrient concentrations are rapidly achieved, and within limits, the growth rate is proportional to the medium flow rate. Scanning electron microscopic studies showed that such populations consist of individual cells embedded within an extracellular polymer matrix.
Article
Full-text available
The speed of recovery of cell suspensions and biofilm populations of the ammonia oxidizer Nitrosomonas europaea, following starvation was determined. Stationary-phase cells, washed and resuspended in ammoniumfree inorganic medium, were starved for periods of up to 42 days, after which the medium was supplemented with ammonium and subsequent growth was monitored by measuring nitrite concentration changes. Cultures exhibited a lag phase prior to exponential nitrite production, which increased from 8.72 h (no starvation) to 153 h after starvation for 42 days. Biofilm populations of N. europaea colonizing sand or soil particles in continuous-flow, fixed column reactors were starved by continuous supply of ammonium-free medium. Following resupply of ammonium, starved biofilms exhibited no lag phase prior to nitrite production, even after starvation for 43.2 days, although there was evidence of cell loss during starvation. Biofilm formation will therefore provide a significant ecological advantage for ammonia oxidizers in natural environments in which the substrate supply is intermittent. Cell density-dependent phenomena in a number of gram-negative bacteria are mediated by N-acyl homoserine lactones (AHL), including N-(3-oxohexanoyl)-L-homoserine lactone (OHHL). Addition of both ammonium and OHHL to cell suspensions starved for 28 days decreased the lag phase in a concentration-dependent manner from 53.4 h to a minimum of 10.8 h. AHL production by N. europaea was detected by using a luxR-luxAB AHL reporter system. The results suggest that rapid recovery of high-density biofilm populations may be due to production and accumulation of OHHL to levels not possible in relatively low-density cell suspensions.
Article
Full-text available
A technique was developed to study microcolony formation by silicone-immobilized bacteria on polycarbonate membrane filters under anaerobic conditions. A sudden shift to anaerobiosis was obtained by submerging the filters in medium which was depleted for oxygen by a pure culture of bacteria. The technique was used to demonstrate that preinduction of nitrate reductase under low-oxygen conditions was necessary for nonfermenting, nitrate-respiring bacteria, e.g., Pseudomonas spp., to cope with a sudden lack of oxygen. In contrast, nitrate-respiring, fermenting bacteria, e.g., Bacillus and Escherichia spp., formed microcolonies under anaerobic conditions with or without the presence of nitrate and irrespective of aerobic or anaerobic preculture conditions.
Article
Full-text available
Model biofilms of Staphylococcus aureus, Staphylococcus epidermidis, Pseudomonas fluorescens, and Pseudomonas aeruginosa were made on steel and polypropylene substrata. Plaque-resembling biofilms of Streptococcus mutans, Actinomyces viscosus, and Fusobacterium nucleatum were made on saliva-coated hydroxyapatite. The activity of enzymes against bacterial cells in biofilm was measured by fluorescence microscopy and an indirect conductance test in which evolution of carbon dioxide was measured. Glucose oxidase combined with lactoperoxidase was bactericidal against biofilm bacteria but did not remove the biofilm from the substrata. A complex mixture of polysaccharide-hydrolyzing enzymes was able to remove bacterial biofilm from steel and polypropylene substrata but did not have a significant bactericidal activity. Combining oxidoreductases with polysaccharide-hydrolyzing enzymes resulted in bactericidal activity as well as removal of the biofilm.
Article
Full-text available
Predation of attached Pseudomonas putida mt2 by the small ciliate Tetrahymena sp. was investigated with a percolated column system. Grazing rates were examined under static and dynamic conditions and were compared to grazing rates in batch systems containing suspended prey. The prey densities were 2 x 10(8) bacteria per ml of pore space and 2 x 10(8) bacteria per ml of suspension, respectively. Postingestion in situ hybridization of bacteria with fluorescent oligonucleotide probes was used to quantify ingestion. During 30 min, a grazing rate of 1,382 +/- 1,029 bacteria individual-1 h-1 was obtained with suspended prey; this was twice the grazing rate observed with attached bacteria under static conditions. Continuous percolation at a flow rate of 73 cm h-1 further decreased the grazing rate to about 25% of the grazing rate observed with suspended prey. A considerable proportion of the protozoans fed on neither suspended bacteria nor attached bacteria. The transport of ciliates through the columns was monitored at the same time that predation was monitored. Less than 20% of the protozoans passed through the columns without being retained. Most of these organisms ingested no bacteria, whereas the retained protozoans grazed more efficiently. Retardation of ciliate transport was greater in columns containing attached bacteria than in bacterium-free columns. We propose that the correlation between grazing activity and retardation of transport is a consequence of the interaction between active predators and attached bacteria.
Article
Full-text available
The role of electrostatic and hydrophobic interactions and solid and liquid surface tensions in the adhesion of four bacterial species (Pseudomonas fluorescens, Enterobacter cloacae, Chromobacterium sp., and Flexibacter sp.) to hydrophobic polystyrene petri dishes and to more hydrophilic polystyrene tissue culture dishes was investigated. The effect of electrostatic interactions was investigated by determining the effects of different electrolyte solutions on attachment to and of different electrolyte and pH solutions on detachment from the polystyrene substrate. The significance of solid and liquid surface tensions and hydrophobic interactions was investigated by measuring the effects of different surfactants (including a concentration series of dimethyl sulfoxide) on adhesion and detachment. Adhesion varied with bacterial species, substratum, and electrolyte type and concentration, with no apparent correlation between adhesion and electrolyte valence or concentration. The influence of different pH and detergent solutions on bacterial detachment also varied with species, substratum, pH, and detergent type; however, the greatest degree of detachment of all strains from the surfaces was produced by detergent treatment. The results suggest that adhesion cannot be attributed to any one type of adhesive interaction. There was some evidence for both electrostatic and hydrophobic interactions, but neither interaction could wholly account for the data.
Article
Full-text available
[H]thymidine incorporation, the rate of reduction of iodonitrotetrazolium violet (INT) to INT formazan normalized to DNA, and the ratio of ATP to DNA were adapted to measure the activity of attached and unattached microbial assemblages of Bayboro Harbor, Fla. Activity measurements by [H]thymidine incorporation were made of cells attached to polystyrene culture dishes, in unfiltered water samples, and in the <1-mum-filtered fraction. In most cases, the activity of attached cells was greater than that of unattached cells either in unfiltered water samples or in the <1-mum fraction. The calculated thymidine incorporation rates for cells in the >1-mum fraction were higher than those for cells either in unfiltered water or in the <1-mum-filtered fraction. By the rate of reduction of INT to INT formazan normalized to DNA and by ATP-to-DNA ratios, attached cells were also more active than cells in unfiltered water samples. These results indicate that the microenvironment afforded by attachment is a more beneficial habitat for microbial growth. Reasons for greater activity by natural populations of attached bacteria are discussed.
Article
Full-text available
A microbial community was cultivated in flow cells with 2,4,6-trichlorobenzoic acid (2,4,6-TCB) as sole carbon and energy source and was examined with scanning confocal laser microscopy and fluorescent molecular probes. The biofilm community which developed under these conditions exhibited a characteristic architecture, including a basal cell layer and conspicuous mounds of bacterial cells and polymer (approximately 20 to 30 (mu)m high and 25 to 40 (mu)m in diameter) occurring at 20- to 200-(mu)m intervals. When biofilms grown on 2,4,6-TCB were shifted to a labile, nonchlorinated carbon source (Trypticase soy broth), the biofilms underwent an architectural change which included the loss of mound structures and the formation of a more homogeneous biofilm. Neutrally charged fluorescent dextrans, which upon hydration become cationic, were observed to bind to mounds, as well as to the basal cell layer, in 14-day biofilms. In contrast, polyanionic dextrans bound only to the basal cell layer, indicating that this material incorporated sites with both positive and negative charge. The results from this study indicate that nutrient composition has a significant impact on both the architecture and the physicochemistry of degradative biofilm communities.
Chapter
It has been realized for some time that solid surfaces, such as clay particles or glass beads, added to a bacterial suspension may produce an increase in bacterial activity and that bacterial attachment to these surfaces may be involved. As early as 1917, Douglas et al. reported that the addition of “inert” materials, such as glass, asbestos, charcoal, or chalk, allowed the growth of anaerobic bacilli in broth culture. In the 1930s and 1940s, a much more extensive study of the effects of surfaces on marine bacterial activity was conducted by ZoBell and co-workers (ZoBell and Anderson, 1936; ZoBell, 1943; ZoBell and Grant, 1943). However, it was not until recently that workers refocused attention on the effects of solid surfaces on bacterial physiological processes and renewed attempts to determine the underlying mechanisms for this surface effect.
Article
Four species of heterotrophic microflagellates were examined for their ability to graze attached and unattached bacteria. The species tested displayed pronounced differences in their ability to graze the bacteriumPseudomonas halodurans attached to chitin particles. Two species of microflagellates (Monas andCryptobia sp.) efficiently grazed unattached bacteria but showed little or no ability to graze attached or aggregated cells. In contrast,Rhynchomonas nasuta andBodo sp. showed marked preferences for attached and aggregated bacteria and a limited ability to graze unattached cells. The density of attached bacteria was reduced by an order of magnitude due to grazing byBodo andR. nasuta, even though the density of unattached bacteria was ∼5-90× the density of attached cells. The maximum densities attained by microflagellates in the cultures were related to the density of unattached bacteria forMonas andCryptobia but not forBodo andR. nasuta. Growth of the latter two species appeared to be related to the density of attached or aggregated bacteria. Based on the results of these experiments, it is concluded that the pelagic existence of microflagellates that graze attached bacteria may be strongly linked to the distribution of suspended particles and their associated bacteria. In addition, the removal of attached bacteria by microflagellates can significantly affect the density of bacteria attached to particles in the plankton. This activity may have important implications for the controversy concerning the relative importance of attached and free-living bacteria in the plankton.
Article
A procedure has been developed for preparing living bacteria, quantitatively labeled with (3)H-thymidine and (14)C-leucine, for short-term grazing experiments. The negligible rate of accumulation in protozoan macromolecules of moieties of bacterial macromolecules labeled with (3)H compared with moieties labeled with (14)C permits estimation of the consumption, digestion, and assimilation of prey biomass in protists without separating them from bacteria. The principles of this method are described, and the results of its application in examples of grazing by the ciliates Euplotes and Uronema and the flagellate Pteridomonas on the bacterium Vibrio are outlined.
Article
The sorption of two marine bacteria to surfaces involved an instantaneous reversible phase, and a time-dependent irreversible phase. Reversible sorption of the non-motile Achromobacter strain R8 decreased to zero as the electrolyte concentration decreased, or as the thickness of the electrical double-layer increased. The electrolyte concentration at which all bacteria were repelled from the glass surface depended on the valency of the cation. The reversible phase is interpreted in terms of the balance between the electrical double-layer repulsion energies at different electrolyte concentrations and the van der Waals attractive energies. Even at the electrolyte concentration of seawater, the bacteria probably are held at a small distance from the glass surface by a repulsion barrier. Reversible sorption often led to rotational motion of the motile Pseudomonas sp. strain R3 at a liquid-glass interface. Pseudomonas R3 produced polymeric fibrils in artificial seawater; these may be concerned in the irreversible sorption of the bacteria to surfaces. Sorption and polymer production were stimulated by 7 mg./l. glucose but higher levels inhibited irreversible sorption. Omission of Ca2+ and Mg2+ from the artificial seawater prevented growth, polymer production, and sorption to surfaces by Pseudomonas R3.
Article
The diversity of heterotrophic nanoflagellates and other protists was examined at various sites around Southampton Water (U.K.) between 1991 and 1994. Observations were made on species occurring in enrichment cultures, in freshly collected material concentrated by gentle centrifugation, and on electron microscope whole mounts. The species described belong to the apusomonads, cercomonads, dinoflagellates, euglenids, stramenopiles and thaumatomonads or else are of uncertain taxonomic affinities (Protista incertae sedis). Choanoflagellate species found during the study are described elsewhere (Tong 1997). Five new species are described: Luffisphaera hamatus n. sp., Ministeria vibrans n. sp., Pendulomonas adriperis n. gen., n. sp., Rigidomastix devoratum n. sp., and Thaumatomastix thomseni n. sp.
Article
Protozoa are the main consumers of heterotrophic bacteria in aquatic habitats. The numbers of these bacteria and protozoa in oligotrophic areas of the open ocean are low, and current methods lack the sensitivity to assess rates of bacterivory in such waters. A new method is proposed for estimating bacterivory on dual radioactively labelled natural bacteria using living ambient prey bacteria and separation of predators from prey by fractionation. This approach is sufficiently sensitive to measure the consumption of less than 1% of the labelled bacteria during a 13-h incubation period. When tested on samples collected from 27 stations in mesotrophic and oligotrophic regions of the North and South Atlantic Oceans, about 17% of metabolically active bacteria were grazed per day and about 60% of consumed prey biomass labelled with 14C-leucine was retained by the predators.
Article
The effect of structure (i.e. particle size) on protozoan population development was studied using liquid culture, containing known amounts of the bacterium Erwinia cartovora subsp. carotovora or nutrient growth medium PPY, and the ciliate protozoan Tetrahymena pyriformis. Structure was introduced into each system in the form of different size ranges of ballotini (glass beads), or sand. Even with the smallest particle sizes used, all pore pathways were accessible to protozoa. Incorporation of structure into nutrient solution acted to lower significantly (P < 0.05) protozoan activity in the structured pore network, as compared to the nutrient solution without structure. There were no significant differences (at the 5% level) in the final protozoa population in either substrate system. As particle size decreased, the protozoan population also decreased. Structure was shown to introduce distances between protozoa and bacterial cells thus, in comparison with treatments without structure, protozoan populations were significantly reduced. Further, reducing particle size would increase the time taken to explore the available pore volume, and reduce the amount of food available in each pore. The outcome was that decreasing the particle size reduced the feeding rate and so reduced the rate of population increase. Other possible physical mechanisms which may limit protozoan movement, such as surface area, are examined.
Article
This article is in Free Access Publication and may be downloaded using the “Download Full Text PDF” link at right.
Article
The attachment of a marine Pseudomonas sp. to a variety of surfaces was investigated, and the number of bacteria which became attached was related to the surface charge and degree of hydrophobicity of the substratum. Large numbers of bacteria attached to hydrophobic plastics with little or no surface charge [Teflon, polyethylene, polystyrene, poly(ethylene terephthalate)]; moderate numbers attached to hydrophilic metals with a positive (platinum) or neutral (germanium) surface charge; and very few attached to hydrophilic, negatively charged substrata (glass, mica, oxidized plastics). The results suggest that both electrostatic and hydrophobic interactions are involved in bacterial attachment.
Article
The assimilation and respiration of glucose by attached and free-living Pseudomonas fluorescens were compared. The attachment surfaces were polyvinylidene fluoride, polyethylene, and glass. Specific uptake of [C]glucose was determined after bacterial biomass was measured by (i) microscopic counts or (ii) prelabeling of cells by providing [H]leucine as substrate, followed by dual-labeling scintillation counting. The glucose concentration was 1.4, 3.5, 5.5, 7.6, or 9.7 muM. Glucose assimilation by cells which became detached from the surfaces during incubation with glucose was also measured after the detached cells were collected by filtration. The composition of the substratum had no effect on the amount of glucose assimilated by attached cells. Glucose assimilation by attached cells exceeded that by free-living cells by a factor of between 2 and 5 or more, and respiration of glucose by surface-associated cells was greater than that by free-living bacteria. Glucose assimilation by detached cells was greater than that by attached bacteria. Measurements of biomass by microscopic counts gave more consistent results that those obtained with dual-labeling, but in general, results obtained by both methods were corroborative.
Ecology of Protozoa The Biology of Free-living Phagotrophic Protists Effect of solid surfaces on the activity of attached bacteria Bacterial Adhesion: Mechanisms and Physiological Significance
  • Fenchel
Fenchel T (1987) Ecology of Protozoa. The Biology of Free-living Phagotrophic Protists. Springer-Verlag, Berlin Fletcher M (1985) Effect of solid surfaces on the activity of attached bacteria. In: Savage D C, Fletcher M (eds) Bacterial Adhesion: Mechanisms and Physiological Significance. Plenum Publishing Corporation, New York, pp 339-362
Growth of silicone-and counting aquatic microflora
  • O Høberg
  • B Jørgen
  • Sørensen
Høberg O, Jørgen B, Sørensen J (1997) Growth of silicone-and counting aquatic microflora. Limnol Oceanogr 25: 943-948
Handbook of Methods in Aquatic Microbial Ecology
  • P F Kemp
  • B F Sherr
  • E B Sherr
In: Kemp P F, Sherr B F, Sherr E B, Cole J J (eds) Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Florida, pp 213-227
Bacterial biofilms as a trophic resource for certain benthic foraminifera Dynamics of bacterial biofilm formation Microbial Biofilms
  • J M Bernhard
  • S Bowser
  • M G Brading
  • Jass J Lappin-Scott
Bernhard J M, Bowser S S (1992) Bacterial biofilms as a trophic resource for certain benthic foraminifera. Mar Ecol Prog Ser 83: 263-272 Brading M G, Jass J, Lappin-Scott H M (1995) Dynamics of bacterial biofilm formation. In: Lappin-Scott H M, Costerton J W (eds) Microbial Biofilms. Cambridge University Press, Cambridge, pp 46-63
  • ZoBell C E