© 2002 by The Society for Integrative and Comparative Biology
The Influence of Surface Wettability on the Adhesion Strength of Settled Spores of the Green Alga Enteromorpha and the Diatom Amphora1
1 School of Biosciences, University of Birmingham, Birmingham B15 2TT, UK
2 Department of Chemical and Nuclear Engineering, The University of New Mexico, Albuquerque, New Mexico 87131
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In this paper we report on the effect of surface wettability on surface selection and adhesion properties of settled (adhered) spores of the biofouling marine alga Enteromorpha and cells of the diatom Amphora, through the use of patterned self-assembled monolayers (SAMs). The SAMs were formed from alkanethiols terminated with methyl (CH3) or hydroxyl (OH) groups, or mixtures of the two, creating a discontinuous gradient of wettability as measured by advancing water contact angle. In the case of Enteromorpha, primary adhesion, as measured by the transition from a motile spore to a settled, sessile organism, is strongly promoted by the hydrophobic surfaces. On the other hand, adhesion strength of the settled spores, as measured by resistance to detachment in a turbulent flow cell, is greatest on a hydrophilic surface. In the case of Amphora, there is little influence of surface wettability on the primary adhesion of this organism, but motility is inhibited at contact angles
60° and the cells are more strongly adhered to hydrophobic surfaces. Adhesion strength of Enteromorpha spores is also influenced by group size, spores in groups being more resistant to detachment than single spores. |
INTRODUCTION |
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SYNOPSISINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSReferences |
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Marine organisms that spend their adult life attached to surfaces must find a suitable place to settle and adhere before they can complete their life cycle. This is accomplished through the ability of dispersal stages, be they larvae of invertebrate species, or spores of algae, to; a) select an appropriate surface on which to settle through the detection of surface cues, and b) produce materials with permanent or temporary adhesive capabilities that enable the attached propagule to resist detachment forces. This adhesion process takes place rapidly, often within minutes, under water, to a wide range of substrates, over a wide range of temperatures, salinities and conditions of turbulence. In certain cases the adhesion is effectively permanent, in other cases adhesion needs to be reversible as the organism moves around on a surface to find the most appropriate settlement site.
Enteromorpha is a common, green macroalga found throughout the world in the upper intertidal zone of seashores and as a fouling organism on a variety of man-made structures including ships' hulls (Callow, 1996
). It is tolerant of a wide range of environmental conditions and surface coating types including biocidal antifouling paints (Callow, 1986) and non-toxic foul-release coatings (personal communication J. Lewis). Dispersal is achieved mainly through asexual zoospores; quadriflagellate, pear-shaped cells, 5–7 µm in length (Fig. 1a). Colonisation of substrata involves the transition from a free-swimming spore to an adhered non-motile spore (Callow et al., 1997), adhesion being achieved via the secretion of a glycoprotein adhesive from Golgi-derived vesicles in the anterior region of the spore. The secreted adhesive forms a discrete gel-like pad on the surface (Fig. 1b). Spores may settle singly, or as groups through gregarious settlement behaviour (Fig. 1c). After settlement adhesion strength to the substratum increases as the adhesive rapidly "cures," presumably through some form of cross-linking process (Callow et al., 2000a; Finlay et al., 2002).
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Amphora spp. (Fig. 1d) are the most commonly encountered raphid diatoms in biofilms that develop on antifouling paints (Callow, 1986
, 1996, 2000) and on non-toxic fouling-release coatings (unpublished data). Raphid diatoms produce extracellular polymeric substances (EPS) for the dual purpose of adhesion and locomotion (Edgar and Pickett-Heaps, 1984; Hoagland et al., 1993; Wustman et al., 1997; Wetherbee et al., 1998). A. coffeaeformis is commonly used in experimental fouling studies (Geesey et al., 2000; Schultz et al., 2000).
The range of marine surfaces available for colonisation by diatoms and Enteromorpha spores is vast and most seem to be utilised. The different characteristics of these surfaces will affect the physical and chemical interactions with the adhesive that will likely be reflected in bonding strength. By examining the strength of attachment to surfaces of known chemistry, greater insight into the mechanics of adhesion can be gained. Traditionally, since the work of Baier (1973), settlement and adhesion of fouling organisms has been associated with low surface free energy of the substrate. Surface free energy is a measure of the capacity of a surface to interact spontaneously with other materials by forming new bonds (the related parameter, critical surface tension is a measure of surface wettability). More recent models of adhesion performance for hard, macro-fouling organisms on elastomeric surfaces have incorporated considerations of fracture mechanics (Singer et al., 2000), but there is no suggestion that mechanical factors are likely to play a role in controlling adhesion of microscopic, compliant, soft-fouling unicells, and for such organisms the generalized relationship between adhesion and low surface energy is likely to pertain. The effect of surface energy on adhesion is often studied by employing widely different materials, ranging from urethanes and epoxies (high energy), to silicones and fluorinated materials (low energy). However, such diverse materials have substantially different chemistries and physical properties such as modulus, and more recently those interested in fundamental adsorption and adhesion phenomena have used surfaces formed from self-assembled monolayers (SAMs) on gold-coated glass or some other common substrate (Sigal et al., 1998; Callow et al., 2000b; Ostuni et al., 2001). SAM surfaces are more fully characterized and uniform with respect to surface topography and modulus, and can be made with a variety of functional groups (Bain et al., 1989). The use of mixed alkane thiolate SAMs of different wettability, and patterned on the same slide, is particularly revealing since a wide range of surface properties is simultaneously presented to attaching organisms, allowing "choice" experiments to be conducted. In a previous paper (Callow et al., 2000b) we examined the settlement of Enteromorpha zoospores on mixed patterned SAMs. In the present paper we extend these observations to include the diatom Amphora, and an evaluation of the influence of surface wettability on the tenacity of adhesion of both organisms.
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MATERIALS AND METHODS |
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Enteromorpha settlement and adhesion assays
Fertile plants of Enteromorpha linza were collected from Wembury beach, UK (50°18'N; 4°02'W). Zoospores were released and prepared for adhesion experiments as described previously (Callow et al., 1997
). Zoospores were settled in individual compartments of "quadriperm" dishes (Fisher) each containing an acid-washed glass microscope slide. Ten ml of zoospore suspension (typically 1–2 x 106 spores ml–1) were added to each dish and incubated in the dark at 
20°C for 1 hr. The slides were then gently washed in filter-sterilized artificial seawater (ASW, Instant Ocean) to remove zoospores that had not properly attached. For static settlement assays, slides were fixed in 2% (v/v) glutaraldehyde in seawater for 10 min, followed by washing as described previously (Callow et al., 1997). Adhered zoospores were counted using a Zeiss Kontron 3000 image capture analysis system attached to a Zeiss epifluorescence microscope (Callow et al., 2002). Counts were made for 10 fields of view on each of 3 replicate slides. Precise experimental conditions are given in individual figure legends.
For detachment studies, after the initial settlement period, washed, unfixed slides were exposed to 56 Pa wall shear stress in a fully turbulent flow apparatus (Schultz et al., 2000). The number of spores still attached to slides after exposure to flow was counted and compared to unexposed samples.
Amphora settlement and adhesion assays
Cells of Amphora coffeaeformis var. purpusilla were cultured in F/2 medium (Guillard and Ryther, 1962) at 20°C on an illuminated orbital incubator. After 3 days the cells were in log phase growth. Cells were settled under gravity, then washed twice in ASW to prevent carry over of nutrients, thereby preventing cell division during the course of the experiment, before dilution with sea water to give a suspension of cells with a chlorophyll a content of approximately 0.3 µg ml–1. Filtering through a nylon mesh of pore size 35 µm produced a final suspension consisting largely of single cells. Ten ml of the cell suspension were added to individual compartments of "quadriperm" dishes (Fisher) each containing an acid-washed glass microscope slide. After 2.5 hr settlement in the light, the slides were gently washed in ASW to remove cells that had not properly attached. For static settlement assays, the slides were fixed and counted as described for Enteromorpha. For detachment studies, slides were incubated for a further 2.5 hr before exposure to shear stresses in the flow apparatus. Percentage removal was calculated by comparing the number of cells attached after flow with the number of cells before flow as described for Enteromorpha.
Motility was assessed on cells after 5 hr settlement. Slides immersed in ASW were illuminated for 5 min on an illuminated microscope stage before counting. Counts were made of at least 50 single cells on each surface using a long working distance lens. Each cell was assessed for movement. "Shunting" behaviour (small-scale movements back and forth) was not recorded as movement. From these data the proportion of motile cells was determined.
Flow cell apparatus
Slides settled with spores or diatoms were exposed to shear in a specially designed flow cell apparatus (Schultz et al., 2000), modified by fitting a higher capacity pump (1.12 kW (1.5 hp) 3-phase Baldor thermoplastic centrifugal pump (McMaster-Carr, Chicago, IL, USA) generating flows of sea water (Instant Ocean) up to 4.9 m sec–1 (wall shear stresses up to 56 Pa). Exposure of slides to flow was standardised at 5 min. Control experiments conducted on uncoated slides established that there was no difference in the removal of cells in the flow cell due to the slight streamwise position of the SAM patterns (see next section).
Surfaces
Glass microscope slides were successively washed in a 50% methanol/50% concentrated hydrochloric acid mixture, followed by 100% concentrated hydrochloric acid (2 hr in each). After thorough washing in distilled water the static water contact angles were ca. 10–15°.
Self-assembled monolayers (SAMs) of 
-substituted alkane thiolates on gold were used to examine the effect of surface wettability on settlement and the strength of attachment of Enteromorpha spores and diatom cells (for general background on the preparation and characterisation of alkanethiolate SAMs on gold the reader is referred to Bain et al. [1989]). SAM technology provides surfaces that are chemically defined and uniformly smooth (this depends mainly on the roughness of the underlying gold and ellipsometric thicknesses typical show errors of ±2 Å [Bain, 1989]). The SAMs used in this study were prepared and characterized by advancing water contact angle and XPS (X-ray photoelectron spectroscopy) at the University of New Mexico, as described previously (Callow et al., 2000b). Hydrophobic methyl-terminated SAMs (CH3-SAM) for gregarious settlement studies, were formed on gold-coated standard microscope slides and typically had an advancing water contact angle (
AW) between 105 and 115°.
In all other studies patterned SAMs were formed from mixtures of dodecane thiol (referred to as CH3-thiol) and mercaptoundecanol (referred to as OH-thiol) by serial electrochemical desorption and reformation on a standard microscope slide coated with a pure CH3-SAM, as described previously (Callow et al., 2000b). The pattern consisted of a square (16 x 16 mm) divided into four sectors, each 8 x 8 mm. The four sectors bore mixed component SAMs formed from solutions that produced contact angles (AW) of approximately 20°, 40°, 60° and 80°. The mean measured AW values are used in the data plots. Adjacent SAMs were separated by approximately 15 µm of bare glass. The AW of the hydrophobic background CH3-SAM varied between 93° and 103° indicating that some slight degradation or contamination had occurred, most probably the result of repeated exposure to air during the laser etching, or during repeated exposure to ethanolic KOH during subsequent processing.
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RESULTS AND DISCUSSION |
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The influence of surface wettability on adhesion strength
The settlement of Enteromorpha zoospores was examined on mixed alkane thiolate SAMs (OH/CH3) of different wettability. Results were consistent with those obtained previously (Callow et al., 2000b
): spores showed a strong preference for settlement on hydrophobic surfaces (Fig. 2a): after 1 hr incubation there was approximately 10 times more spores attached to the pure CH3-SAM compared with the pure OH-SAM. The implication of this result in terms of thermodynamic models in which the free energy of adhesion is minimized by the low surface energy, hydrophobic surface, was extensively discussed by Callow et al. (2000b). More mechanistic interpretations include the possibility that hydrophobic interactions may be important during this initial phase of adhesion and that the wetting of the surface, i.e., the removal of water molecules from the interface, is also facilitated by a hydrophobic surface.
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However, when the tenacity of adhesion of settled spores was examined on patterned SAMs, a quite different relationship was obtained, adhesion strength being greatest on hydrophilic (OH-rich) surfaces and weakest on hydrophobic (CH3-rich) surfaces (Fig. 2b).
SAMs are used extensively in biophysical studies on adsorption of single proteins and the general relationship is that hydrophobic surfaces tend to adsorb proteins from solution while hydrophilic surfaces are more resistant although there is some dependence on protein size; small proteins such as ribonuclease and lysozyme adsorbing only on the least wettable surface while larger proteins (pyruvate kinase, fibrinogen, 
-globulin) adsorbed to some extent on all surfaces (Sigal et al., 1998). The present results and those obtained by others for bacterial and mammalian cells (Ostuni et al., 2001) demonstrate that cell adhesion is a much more complex affair than can be described by protein adsorption and the Enteromorpha adhesion strength results are consistent with a generalised relationship for fouling organisms, between low adhesion strength and low surface free energy (Baier, 1973). This relationship forms the basis of the search for low surface energy, "fouling release" marine coatings.
However, caution in generalization should be exercised since it is known that some bacteria attach more strongly to hydrophobic surfaces (van Loosdrecht et al., 1987; Otto et al., 1999) and when adhesion experiments were conducted with Amphora cells a different relationship with wettability was observed compared with Enteromorpha. The level of initial settlement of Amphora cells on the patterned SAMs was very similar at all wettabilities (data not shown) since cells drop down onto the surface by gravity and initial weak attachment is probably through EPS covering the cells. However, at low to moderate levels of shear stress, cells were more easily removed from the hydrophilic than the hydrophobic surfaces (Fig. 3). Although similar experiments should be conducted on a wider range of diatoms to see how widely this relationship applies, this result is consistent with the observation that low surface energy, antifouling coatings frequently fail to diatoms slime communities, of which Amphora is a common member.
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Unlike Enteromorpha spores, adhered cells of most raphid diatoms retain the capacity for motility on a surface. In observations of Amphora motility on the SAMs surfaces, approximately 60% of cells were seen to be moving on glass or hydrophilic SAMs with a
AW of 40° or less, after 5 hr contact time on the surface (Fig. 4). By contrast, no movement was seen by cells on SAMs with a AW of 60° or greater. The inability of Amphora to move on silanised gradients with AW > 40% was noted by Wigglesworth-Cooksey et al. (1999). In diatoms, adhesion and motility are strongly interlinked, the latter being based on an actin/myosin motility system (Poulsen et al., 1999). Polymers, secreted in the raphe, which connect the cell to the surface, are themselves linked to internal actin bundles by transmembrane proteins. Interaction of actin bundles with myosin generates movement. The implication of our data showing stronger adhesion but lower motility of Amphora on hydrophobic SAMs, is that the cells are able to orient themselves and secrete exopolymers to adhere but cannot break free to glide (Wetherbee et al., 1998). There is some evidence to suggest that surface characteristics affect the chemistry of the EPS that is produced. Becker (1996) demonstrated that the production of more EPS did not increase attachment strength on hydrophobic materials and suggested that Amphora might produce hydrophobic polysaccharides or other molecules to improve strength of attachment to such surfaces. Wigglesworth-Cooksey et al. (1999) comment that a strong interaction between the polymer and surface is required for adhesion and motility. It is also possible that if the adhesion is too strong motility is prevented. If contact with a hydrophobic surface stimulates the production of more hydrophobic polymers (which would associate more strongly to the surface than polar hydrophilic polymers) then these might prevent locomotion. The inability of Amphora to move on hydrophobic surfaces may therefore represent an overproduction of a hydrophobic polymer. At the time of testing, the cells may be in the process of fine-tuning the chemistry and quantities of polymers produced (hence the shunting motion sometimes observed by cells on these surfaces).
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However, it is not clear that the inability to move on hydrophobic surfaces is purely a function of wettability since we have also observed that Amphora shows normal movements on some hydrophobic silicone elastomers, but slower and more jerky movements on others (unpublished data). Furthermore, the inability to move on hydrophobic surfaces does not appear to be universal for all diatoms as noted by (Edgar and Pickett-Heaps, 1984
), and Wetherbee (personal communication) has observed no effect or in some cases enhanced motility of some diatom species on hydrophobic, silanised glass surfaces. Clearly the interrelationship between surface properties, adhesion strength and motility is complex. The fact that fouling release coatings in the field become fouled by tenaciously adherent diatom slimes (Terlizzi et al., 2000) and that Amphora spp. have been seen dominating some commercial fouling-release coatings (unpublished data) suggests that further effort to understand the behaviour of diatoms on a range of hydrophobic materials would be worthwhile. Taking the Enteromorpha and Amphora data together, the use of the flow apparatus in conjunction with the patterned SAMs has revealed a striking difference between the two organisms in the relationship between adhesion strength and surface wettability.
The influence of gregarious settlement on adhesion strength in Enteromorpha
Kinetic analysis of spore settlement in Enteromorpha revealed this to be a cooperative process, with both negative and positive cooperative effects, depending on initial spore density (Callow et al., 1997). Positive cooperativity is manifested as gregarious settlement in which spores settle in close proximity to previously settled spores, to form rafts of cells. The communication mechanisms promoting gregarious settlement are not well understood but the adaptive value may lie in the lower energy requirements for spores to attach against each other (Callow et al., 2002) and the greater protection provided to cells in groups against detachment forces in a turbulent environment. To test this hypothesis, spores were settled on CH3-SAMs, the hydrophobic surface promoting formation of groups (Callow et al., 2000b). The distribution of spores in groups of various group size categories (group defined as adjacent spores touching) was measured by image analysis before and after exposure to shear stress in the flow cell at 56 Pa. Analysis of the size of spore groups on the CH3-SAM showed that the proportion of single and double spores decreased and the proportion of larger spore groups, especially those with six or more spores, increased from 15% to 29% in the samples exposed to flow (Fig. 5).
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CONCLUSIONS |
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The two organisms used in the present study represent the two most common forms of algal biofouling in the marine environment. Enteromorpha spores are motile and "select" where to settle whilst diatoms arrive at the surface through passive mechanisms. The use of model surfaces has enabled differences in the mechanisms of adhesion to be explored. Enteromorpha spores show a strong preference for settlement on hydrophobic surfaces but are only weakly attached. By contrast, Amphora cells attach more strongly to hydrophobic surfaces, on which gliding motility is inhibited. The interaction between the secreted adhesive(s) and the surface suggests requires further study. We are using ESEM (Environmental Scanning Electron Microscopy, [Callow et al., 2003
]) to determine whether detachment from hydrophobic and hydrophilic SAMs is primarily due to adhesive failure (no adhesive deposits remaining) or cohesive failure ("footprint" remaining).
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ACKNOWLEDGMENTS |
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The authors acknowledge support from the Office of Naval Research (awards N00014-96-1-0373 and N00014-99-1-0311 to JAC and MEC: award N00014-95-1-0901 to GPL).
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FOOTNOTES |
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1 From the Symposium Biomechanics of Adhesion presented at the Annual Meeting of the Society for integrative and Comparative Biology, 2–6 January 2002, at Anaheim, California.
2 Address for correspondence. E-mail: j.a.callow{at}bham.ac.uk
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References |
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