PHYSICAL SCIENCES / BIOLOGICAL SCIENCES / ENVIRONMENTAL SCIENCES / EVOLUTION
Bacterial metapopulations in nanofabricated landscapes
Juan E. Keymer , Peter Galajda , Cecilia Muldoon , Sungsu Park , and Robert H. Austin
Department of Physics, Princeton University, Princeton, NJ 08544-1014
Contributed by Robert H. Austin, September 17, 2006
We have constructed a linear array of coupled, microscale patches of habitat. When bacteria are inoculated into this habitat landscape, a metapopulation emerges. Local bacterial populations in each patch coexist and weakly couple with neighbor populations in nearby patches. These spatially distributed bacterial populations interact through local extinction and colonization processes. We have further built heterogeneous habitat landscapes to study the adaptive dynamics of the bacterial metapopulations. By patterning habitat differences across the landscape, our device physically implements an adaptive landscape. In landscapes with higher niche diversity, we observe rapid adaptation to large-scale, low-quality (high-stress) areas. Our results illustrate the potential lying at the interface between nanoscale biophysics and landscape evolutionary ecology.
biophysics | microbiology | landscape ecology | metapopulation biology
PNAS | November 14, 2006 | vol. 103 | no. 46 | 17290-17295. Open Access Article.
In nature, habitats are patchy, aggregating at several scales generating a discrete habitat landscape (1). The landscape ecology of such environments provides communities with a distribution of characteristic scales (temporal and spatial) that can be used to partition such habitat landscapes (2, 3) allowing for species coexistence. In general, a metapopulation (4) or "population of populations" develops over such habitat landscape and is characterized by local population extinctions and colonizations. It is known that the topological properties of the ensemble and the quality of the individual patches have deep implications for fitness (4, 5).
The environments in which single-celled organisms exist is no different. However, natural habitat landscapes populated with "big" organisms are difficult to approach experimentally. On the contrary, bacteria are great experimental systems, and the environments they populate are amenable to experimental manipulation. Bacteria, like other life forms, self-organize into sophisticated dynamic assemblages. Escherichia coli individuals are known to exhibit complex patterns of motility (6). Individual bacteria are known to associate even further into very complex communities (biofilms) that resemble a human metropolis (7) in which microbes communicate with each other (8) and work together toward common goals (9), exploiting what is called niche complementarity (10).
Sewall Wright (11) realized that a collection of interacting and interbreeding populations of organisms moving across patchy landscapes implemented a spatially distributed network, facilitating the flow of alleles across a fitness landscape. In Wright's view, spatially distributed populations adapted to different local environments but weakly coupled through population dispersal is the key to the dynamics of the evolution of coadapted complexes of genes. Wright's adaptive landscape (Fig. 1A) is a heuristic one. It changes with space and time, and is a function of many degrees of freedom, including the collective response of a population of interacting organisms as well as its intricate relationships with its habitat. The phenotype of an organism's genome consists of both individual aspects, such as cell growth and reproduction rates, and collective ones, such as the way the cells interact in mutually beneficial (or destructive) ways.
Because the landscape ecology of the habitat distribution provides a proxy for fitness, micro- and nanofabrication techniques open up the possibilities of making spatially complex habitat landscapes that probe how microorganisms can adapt to both temporally and spatially varying challenges to fitness (adaptive landscape). Fig. 1B shows our solution to this problem: microhabitat patches (MHPs) that allow distinct local populations to fill a given habitat patch of quality parameters determined by nanoslits linking each MHP to external feeding channels. Individual MHPs have coupling corridors. Thus, a species can move from one patch to another, allowing the bacterial metapopulation to adapt to the different regions of our designed landscapes.
The chemostat was conceived by Novick and Szilárd (12) to provide us with an homogeneous ecology. Because chemostats lack spatial structure, they do not allow organisms to search out different niches in a spatially heterogeneous habitat. But, natural habitats are indeed heterogeneous. The nanofabricated habitat landscapes we can construct afford a variability in habitat structure, allowing us to experimentally explore Wright's adaptive landscape. There have been microchemostat systems created recently (13, 14), but the technology discussed here differs in a fundamental way. Microfabricated chemostats described so far (just as the macroscopic ones) do not allow for the emergence of a metapopulation [a spatially distributed network, of parallel populations adapted to different local conditions but weakly coupled with one another by dispersal (4)]. Moreover, in a "strict" chemostat, biomass is constantly removed and resources are added to reach a steady-state, yielding cells in exponential growth, rather than in other phases of growth (15). By adding spatial structure to the system, we can create heterogeneity in habitat structure and study how cells adapt to different regions of the landscape (ecotopes).
We constructed a one-dimensional (1D) array of coupled MHPs; the running index i here is used to denote the ith MHP. The corridors "coupling" MHPs are designed to be narrow enough so that each MHP can be viewed as a local niche in a much larger adaptive landscape generated by the heterogeneous array of habitat patches. There are three fundamental parameters that characterize the habitat in this array of coupled MHPs: (i) the local carrying capacity, Ki (patch size), of bacteria in the ith MHP; (ii) the coupling strength, Ji,i+1 (corridor structure), between adjacent MHPs; and (iii) the coupling strength, i (number of nanoslits), between the MHP and feeding channels that allow food to diffuse into, and waste out of, a given MHP.
In general, vectors K, J, and (landscape parameters) can be made a strong function of the index i, so that nanoscale patchy environments can be designed to test the fitness of organisms to different ecotopes of the landscape. We address the question of how bacterial metapopulations behave when allowed to populate such landscapes.