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namic parameters. Merkel et al. now showthat these AFM measurements representonly a single point in a continuous ‘dynam-ic’ spectrum of the force-driven activation-barrier landscape. In a striking proof withthe high-affinity streptavidin–biotin pair,which has a dissociation half-life on theorder of days in solution, they show thatindividual interactions can survive for as lit-tle as 0.001 seconds, with a strength of only5 pN at slow loading rates. The interactionstrengths increase to around 170 pN athigh loading rates, consistent with valuesmeasured in previous AFM experiments.

Can we relate this force-driven energylandscape to the molecular coordinates ofthe streptavidin–biotin dissociation path-way? Fortunately, three different lines ofinvestigation have converged which, takentogether, indicate this might be possible.First are the force-microscopy studies.Second, molecular dynamics simulationsof the unbinding mechanism under forcehave been done with both streptavidin8 andavidin9. The unbinding activation landscapeobtained by experiment can be qualitativelymapped onto these simulations, and Merkelet al. suggest that the outer activation barrierin their work could correspond to the open-ing of the flexible binding loop in the protein,

which seems to act as a swinging door forligand entry and exit. Finally, transition-state mapping of the streptavidin–biotin dis-sociation pathway has also addressed theenergetics and structures along the free(non-force-driven) activation pathway10.These studies indicate that there is a relative-ly well-defined exit pathway which looksremarkably like that derived from the forceexperiments and simulations. This is, per-haps, not surprising given that biotin mayexit ‘tail’ first in a similar way to the force-driven pathway, which is dictated by the teth-er point between biotin’s tail and the surfaceof the probe (Fig. 1).

We now seem to have an unprecedentedopportunity to detail the molecular struc-ture and energetic relationships governingthe streptavidin–biotin reaction coordinateby a combination of computational andexperimental techniques. But we do stillneed to know how much of the strepta-vidin–biotin model is truly ‘model’, and todocument how nature and bioengineers canuse this analogue-like receptor–ligand bio-

physics. As John Locke noted, “That which isstatic … is boring. That which is dynamicand random is confusing. In-between liesart.”Patrick S. Stayton is in the Departmentof Bioengineering, Box 352125, Universityof Washington, Seattle, Washington 98195,USA.e-mail: stayton@bioeng.washington.edu

1. Merkel, R., Nassoy, P., Leung, A., Ritchie, K. & Evans, E. Nature

397, 50–53 (1999).

2. Alon, R., Hammer, D. A. & Springer, T. A. Nature 374, 539–542

(1995).

3. Binnig, G., Quate, C. F. & Gerber, C. H. Phys. Rev. Lett. 56,

930–933 (1986).

4. Drake, B. et al. Science 243, 1586–1589 (1989).

5. Lee, G. U., Kidwell, D. A. & Colton, R. J. Langmuir 10, 354–357

(1994).

6. Moy, V. T., Florin, E.-L. & Gaub, H. E. Science 264, 257–259

(1994).

7. Chilkoti, A., Boland, T., Ratner, B. D. & Stayton, P. S. Biophys. J.

69, 2125–2130 (1995).

8. Grubmüller, H., Heymann, B. & Tavan, P. Science 271, 997–999

(1996).

9. Izrailev, S., Stepaniants, S., Balsera, M., Oono, Y. & Schulten, K.

Biophys. J. 72, 1568–1581 (1997).

10.Chilkoti, A. & Stayton, P. S. J. Am. Chem. Soc. 117,

10622–10628 (1995).

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NATURE | VOL 397 | 7 JANUARY 1999 | www.nature.com 21

Figure 1 The streptavidin–biotinreceptor–ligand pair. Merkel et al.1 attachedstreptavidin to a surface and biotin to a probe.Having allowed the two to interact, the authorsthen measured the forces needed to pull themapart. They found that the interactionstrengths depend on how fast the ligand ispulled away from the protein — they seemweak or strong depending on how quickly orslowly the retracting force is driven.

Getting from one place to another is aproblem for a plant. One of the mostefficient solutions is to wrap seeds in

an attractive, preferably tasty, envelope andso encourage gluttonous animals to trans-port them. Wandering frugivores may thusbecome inadvertent vehicles of plant migra-tion, but they could also find themselves thetarget of higher predators — so what then isthe fate of the fruits? Is this where the storyends for the passively mobile plant? Appar-ently not. Work on fruit-eating lizards fromthe Canary Islands by Nogales, Delgado andMedina1, reported in the Journal of Ecology,shows that viable seeds can be ingested by thepredator with its prey and taken to furtherdestinations, thus adding a new dimensionto dispersal.

The effectiveness of seed dispersal bypassing through animal guts (endozoo-chory) is widely recognized, and illustra-tions abound. Telegraph poles and wiresover open grassy plains can be the first stagein colonization by trees, as their avian seedvectors find somewhere to perch2. Migratorybirds may carry plants considerable dis-tances, as in the case of snow buntings (Plec-trophenaz nivalis) collected on the island ofSurtsey off Iceland. The gizzards of thesebirds contained many seeds, including thoseof the bog rosemary (Andromeda polifolia),which must have been consumed in Britain3.So, defecation or death of seed-eating migra-tory birds can result in colonization andspread of plants to new regions, depending

on how long the seeds have been in the gut,their final germination potential, and thespeed and direction of bird movement.

Even flightless birds can be valuable vec-tors — the Australian cycad genus Macroza-mia, for example, is dispersed by emus2. Butflight offers rapid and distant transport thatmay be particularly important for colonizingislands. For instance, redevelopment of veg-etation on the Krakatau Islands between Javaand Sumatra after the destructive volcaniceruption of 1883 may have been largely dueto the movements of fruit-eating birds andbats4. More than 20 species of fig (Ficus spp.)must have arrived by air in the guts of flyingvertebrates.

Frugivory is less common among reptilesthan in birds. However, it is found in manyisland lizard species including Gallotiaatlantica, an endemic species of the CanaryIslands. This is the only lizard on the smallisland of Alegranza (10.5 km2), 17 km northof Lanzarote, and it is the focus of the studyby Nogales and colleagues1. There is only onefleshy-fruited plant on the island, Lyciumintricatum (Solanaceae), a thorny shrub upto 2 m in height that bears bright red berriesin winter. The lizard eats many of theseberries, and the authors found that about30% of lizard droppings contained the seeds.The lizard, in turn, falls prey to the great greyshrike (Lanius excubitor). Seeds within thelizard’s alimentary system are consumed byshrikes, but they are then often regurgitatedin pellets. The fact that the seeds in the pellets

Ecology

A shrike for mobilityPeter D. Moore

© 1999 Macmillan Magazines Ltd

are ingested with lizards — rather thandirectly from the plant — is supported byobservation and by a strong correlationbetween lizard remains and Lycium seeds inthe pellets. The seeds in the shrike pellets hada higher germination rate (64%) than thosefrom lizard droppings (50%) or directlyfrom the plant (54%), showing that theirexperience in passing through two vectorshad increased their potential for immediategermination.

Lizards are an effective dispersal systemfor Lycium on Alegranza, but movementof the plant between islands using the lizardas a vector is likely to be rare (although notimpossible5). Movement of the seeds fromlizard to bird, however, presents a range ofopportunities for island-dwelling plants, giv-ing them a far greater chance of moving tonew islands. Because the seeds are retained inthe shrike’s gizzard for less than an hour, feed-ing and flight must follow in rapid successionif dispersal by this means is to be effective.Like so many other events in island biology,given enough time it will probably happen.

The significance of predators as sec-ondary dispersers of fruits and seeds is likelyto be limited to specific situations. In Britain,

the sparrowhawk (Accipiter nisus) is knownto exploit situations where flocks of fruit-eating birds are feeding6. So, again, thepredator could easily ingest seeds with theprey. But the transfer of seeds from one birdto another in this way is unlikely to havemuch of an effect on seed dispersal. On Ale-granza, Lycium seeds have also been found inkestrel (Falco tinunculus) pellets, but thesemay have been derived from fruit-eatingbirds rather than lizards. Only where seedtransfer involves increased mobility andrange (as in the plant–lizard–bird sequence)will new dimensions of dispersal be opened.Predation can then assume a biogeographi-cally significant role.Peter D. Moore is in the Division of Life Sciences,King’s College, Campden Hill Road, LondonW8 7AH, UK.e-mail: peter.moore@kcl.ac.uk1. Nogales, M., Delgado, J. D. & Medina, F. M. J. Ecol. 86, 866–871

(1998).

2. van der Pijl, L. Principles of Dispersal in Higher Plants (Springer,

Berlin, 1982).

3. Fridriksson, S. Surtsey (Wiley, New York, 1975).

4. Whittaker, R. J. & Jones, S. H. J. Biogeogr. 21, 245–258

(1994).

5. Cendsky, E. J., Hodge, K. & Dudley, J. Nature 395, 556 (1998).

6. Snow, B. & Snow, D. Birds and Berries (T. & A. D. Poyser,

Calton, 1988).

its oxidation state), was transported signifi-cant distances through a groundwater sys-tem, and they argue that colloidal specieswere responsible.

Colloid-facilitated transport of contami-nants has become a sort of Gordian knot forenvironmental scientists. Field studies haveoften been subject to sampling artefacts,such as colloid mobilization through exces-sive well-pumping rates, and it has beendifficult to reconcile field observations withtheory and model simulations. (In 1988, areviewer of a manuscript4, on which I was anauthor, implicating a colloidal intermediatein the scavenging of metals in marine sys-tems, complained: “The problem develop-ing in the literature with colloids is that theyare blamed or claimed for everything thatcan’t be explained”.) Since then, colloid-facilitated contaminant transport has gainedbroad acceptance. Nonetheless, few studieshave unequivocally demonstrated its signifi-cance in the field.

Figure 2 compares two- and three-phasecontaminant transport models. Figure 2ashows a low-solubility contaminant distrib-uted between an aqueous phase and immo-bile aquifer solids (the macroparticles). Col-loidal materials can increase the apparent sol-ubility of low-solubility contaminants (Fig.2b) if those contaminants strongly associatewith the colloids and the colloids minimallyinteract with the stationary macroparticlephase. Because colloid groundwater concen-trations are typically quite low, the contami-nants most likely to be transported by col-loidal materials are of extremely low solubili-ty and strongly partition to mobile non-aqueous phase materials. In this respect, Pu isan ideal candidate; others include pesticides(for instance, DDT and dieldrin), poly-nuclear aromatic hydrocarbons, other lightactinides (for example, thorium) and manytransition metals (such as cobalt).

Groundwater colloids originate from twosources5: through mobilization of existingcolloid-sized (1 nm to 1 mm) materials inaquifer systems following chemical pertur-

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NATURE | VOL 397 | 7 JANUARY 1999 | www.nature.com 23

Perhaps nowhere have the details ofcontaminant transport in ground-water systems been more contentious

than in the area of nuclear waste disposal.Over the past decade, the discovery of col-loidal forms of actinides, such as plutonium(Pu), has often been at the centre of concernover underground storage of radionuclides.On page 56 of this issue1 Kersting et al. pro-vide an illustration of the striking influencecolloids2 may have on contaminant trans-port. The authors have studied groundwatermigration of Pu from a nuclear detonationsite in Nevada. However, the particular sig-nificance of their report lies in reinforcinga general awareness of colloid-facilitatedcontaminant transport.

As late as the early 1980s, a groundwatercontaminant was generally assumed to occu-py one of two phases: a stationary phase con-sisting of aquifer solids; and a mobile, aque-ous phase that serves as the medium for themovement of dissolved chemical species. Insuch a system, the rate of contaminant trans-port depends on the groundwater transportvelocity, of course, but also on the distribu-tion of the contaminant between the twophases. The greater the extent to which acontaminant partitions into the immobilephase, the slower its average transportvelocity in the ground water (Fig. 1).

The unexpected appearance of low-

solubility contaminants some distance fromknown sources, or sooner than would beexpected from their solubility, led to exami-nation of the possible involvement of non-aqueous, mobile colloids in contaminanttransport3. Invoking colloids to explain suchobservations gave rise to three-phase modelsof contaminant transport (Fig. 2, overleaf).The results of Kersting et al. reinforce theneed for such models. In their work, they useisotopic ‘fingerprinting’ to demonstrate thatPu, an element with extremely low aqueoussolubility (as low as 10117 M, depending on

Geochemistry

Colloidal culprits in contaminationBruce D. Honeyman

Dissolvedcontaminant

(mobile)

Sorbedcontaminant(stationary)

Water Water

a b

Macroparticle Macroparticle

Figure 1 Contaminant transport in a simple two-phase groundwater system. a, High sorption, andtherefore low contaminant solubility; b, low sorption, high contaminant solubility. Macroparticlesare the stationary components of a groundwater aquifer and include clays, metal oxides such asquartz, and particulate organic matter. The extent to which contaminant molecules are sorpted tomacroparticles (by adsorption, surface precipitation or absorption) regulates the rate of contaminanttransfer through groundwater systems for a given water velocity.