Adaptation to the Sessile State

Are certain prokaryotes uniquely adapted to a sessile form of life? The answer to this question is not simple because of the very wide range of bacteria that can be found on various surfaces. Several examples of different modes of sessile behavior will be considered in order to illustrate the complexity that may be encountered in natural habitats.

Although many bacteria are capable of adhering to a wide variety of surfaces (nonspecific adhesion), the extent of adhesion on the various surfaces varies considerably. Some bacteria adhere best to hydrophobic surfaces (Fletcher and Loeb, 1979), some adhere best to hydro-philic surfaces (Dexter et al., 1975), whereas others adhere best to surfaces of more intermediate surface-free-energy values (Pringle and Fletcher, 1983). The conditions under which the bacteria are grown also modify the adhesive ability of various bacteria on a range of different surfaces (McEldowney and Fletcher, 1986).

Many bacteria that require relatively high nutrient concentrations (copiotrophic bacteria) exist planktonically in oligotrophic waters in a state of starvation. These starvation-survival forms are characterized by a significant reduction in size and by lower endogenous respiration and heat output, and are often more adhesive than actively growing cells (Morita, 1982; Dawson et al., 1981; Humphrey and Marshall, 1984). Adhesion to surfaces by these starvation-survival forms provides access to nutrients accumulated at the surfaces. The starved bacteria are able to scavenge these nutrients and metabolize them (Kefford et al. 1982; Kjelleberg et al., 1983), thereby leading to cellular growth and reproduction (Kjelleberg et al., 1982; Power and Marshall, 1988; Szewzyk and Schink, 1988). In

Sessile Planktonic

Sessile Planktonic

Fig. 4. Four mechanisms for alternating between the planktonic and sessile states: (a) a perpendicularly attached mother cell releases a motile daughter cell, as in Vibrio sp. DWI; (b) division of a cell adhering in a face-to-face manner, and release of a cell on utilization of a bound hydrophobic substrate, as in Pseudomonas sp. JD8; (c) detachment of a fimbrial-attached organism following the production of a hydrophilic capsule, as in Acinetobacter calcoaceticus; and (d) growth of a reversibly adhering organism at a surface and completion of the division phase following drift of the cell from the surface, as in Vibrio sp. MH3.

Fig. 4. Four mechanisms for alternating between the planktonic and sessile states: (a) a perpendicularly attached mother cell releases a motile daughter cell, as in Vibrio sp. DWI; (b) division of a cell adhering in a face-to-face manner, and release of a cell on utilization of a bound hydrophobic substrate, as in Pseudomonas sp. JD8; (c) detachment of a fimbrial-attached organism following the production of a hydrophilic capsule, as in Acinetobacter calcoaceticus; and (d) growth of a reversibly adhering organism at a surface and completion of the division phase following drift of the cell from the surface, as in Vibrio sp. MH3.

many marine environments, it appears that such small, starved bacteria are the primary colonizers of freshly immersed surfaces (Marshall et al., 1971b).

Some copiotrophic bacteria seem unable to adhere firmly to surfaces, yet, under oligotrophic conditions, any starvation-survival forms approaching a surface are able to metabolize surface-bound substrates (Hermansson and Marshall, 1985) and exhibit both cellular growth and reproduction (Power and Marshall, 1988). Thus, nonadhesive bacteria do exist in the planktonic state but it is still possible for such organisms to benefit from association with surfaces.

A particularly effective adaptation to the sessile state is the ability of many bacteria in nature to adhere in an orientation perpendicular to the surface (Fig. 4a; see also Fig. 1). Such prokaryotes appear to have either a specialized holdfast (Caulobacter) or a particularly adhesive portion at one pole of the cell (Hyphomicrobium, Flexibacter, and Leucothrix). Such an orientation allows a very efficient contact both with the solid and the aqueous phases, as well as providing an effective means of releasing daughter cells into the planktonic state. An examination of this mode of orientation at solid surfaces revealed that both Hyphomicrobium and Flexibacter exhibited the same perpendicular orientation at air-water and oil-water interfaces (Marshall and Cruickshank, 1973). It was postulated that the pole of the cell approaching the interface was hydrophobic while the bulk of the cell was hydrophilic, and the hydrophobic pole was rejected from the water phase and aligned at the nonaqueous phase, regardless of whether it was solid, air, or oil (Marshall and Cruickshank, 1973).

Some bacteria are adapted to growth at surfaces, yet possess various mechanisms to ensure that some cells return to the planktonic state. For instance, cells of the marine species Vibrio DW1 adhered to a surface in a perpendicular manner (Fig. 4a) and, following cellular growth of the starved cells to normal size, motile daughter cells were released at regular intervals (approximately 57 min) from the attached mother cells (Kjelleberg et al., 1982). Cells of the marine Pseudomonas sp. JD8 adhered in a face-to-face manner (Fig. 4b) and, following cellular growth and one division cycle the daughter cells slowly (about 0.15 mg/min) began to migrate away from each other while still adhering to the surface. After subsequent division cycles, similar migration patterns were observed but, eventually, some of the daughter cells detached from the surface (Power and Marshall, 1988). This slow migration was explained in terms of the cells being initially irreversibly attached to the hydro-phobic stearic-acid-covered surface but, upon utilization of the fatty acid in the microenvironment around the cell, the cells became reversibly attached to the underlying hydrophilic substratum (Busscher et al., 1986) and were capable of some form of movement. As soon as the cells moved a short distance, however, they encountered more hydrophobic stearic acid and adhered irreversibly again until that substrate was utilized, and the cycle was repeated. When the bound substrate was essentially exhausted, cells detached from the underlying hydrophilic surface (Power and Marshall, 1988). Even the nonadhesive Vibrio MH3 (Fig. 4d) was able to grow from the small starvation-survival form to normal size and then begin the division cycle when exposed to surface-bound stearic acid (Power and Marshall, 1988). The dividing cells drifted away from the surface and completed the division cycle in the planktonic state.

An interesting adaptation ensuring reversibility of the sessile state has been described in Acinetobacter calcoaceticus, which adheres reversibly to epithelial cells and oil by means of thin fimbriae (Fig. 4c). The adhesion of this bacterium is reversed as a result of the production of an excessive amount of extracellular emulsan that surrounds and thus masks the adhesive properties of the fimbriae (Rosenberg et al., 1983). Another example of reversible adhesion has been described in the cyanobacterium Phor-midium, which in its sessile state possesses a hydrophobic surface but under certain conditions produces a hydrophilic capsule, thus allowing the organism to revert to the planktonic state (Fattom and Shilo, 1984).

These studies emphasize the ability of some prokaryotes to take advantage of substrates adsorbed to surfaces, as well as revealing a variety of strategies for releasing daughter cells from the sessile to the planktonic state. As pointed out by Pedros-Alio and Brock (1983), a simple division into sessile and planktonic forms is overly simplistic. Different bacteria have a variety of mechanisms to attach at surfaces but they also possess a range of mechanisms for detachment in order to return to a planktonic existence.

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