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
) 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
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
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, λi (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 λ (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.