The spatial ecology of microbes
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Date
2021
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Abstract
Guided by cell biophysics experimentation and equipped with toolsets from theoretical ecology,
the aim of my thesis is to explore the ways in which spatial structure influences the dynamics and
distributions of microbial cells, populations and communities.
In my first project, we highlighted range expansion experiments of a colicin producing-colicin
sensitive E.coli community on solid agar; The process of colony formation is driven by colicin
production, cell lysis and division all driving the dynamical structure and ecological composition of
the colony. Making analogies to percolation theory from statistical physics, we were able to develop
a spatial model to quantify regimes of strain coexistence, competitive exclusion and extinction.
Next we aimed to understand the spatial conditions under which microbial common goods games
could persist. A particular bacterial system motivating this study was Pseudomonas aeruginosa,
which excretes a costly ‘iron-scavenging’ compound (siderophore) in order to bind and transport
iron across the cell membrane. This compound represents a common-pool resource, susceptible to
exploitation by nearby bacteria free from producing this metabolically costly resource. With this
system in mind we asked the following question: what spatial conditions permit these common-pool
resources to be monopolized by a cooperator strategy in competition with an exploiter strategy?
By developing a stochastic spatial model, we quantified the phase transition from monopolized
to exploited and predicted which circumstances to expect coexistence between niche constructing
and exploiter strategies as a result of differences in niche monopolization and colonization rates,
respectively, and when to expect a collapse of the niche and a ‘tragedy of the commons’.
Following this work, I began to apply newly acquired expertise in microfluidics, microfabrication
techniques, microscopy and experimental cell biophysics in order to observe and study the spatial
colonization dynamics of E.coli and P.aeruginosa in structured microfabricated landscapes. We showed how these two bacterial species enact a competition-colonization tradeoff where the faster
colonizing E.coli can be overwhelmed locally by the slower but superior competitor, P.aeruginosa.
This work constituted the first evidence of an abstract ecological theory in a spatial bacterial
community. Furthermore, these results showed the importance of spatial structure in leading to
coexistence as E.coli is able to effectively localize P.aeruginosa populations when competing in a
patchy landscape via priority-effects. Conversely, in well-mixed ‘mean-field’ conditions the superior competitor always wins. In order to address the priority effects observed by E.coli, we made
analogies to the Kronig-Penny model of solid state physics to our patchy landscape. To help understand the role habitat structure plays in the process of ecological colonization via invading wave
populations, we represented our patchy landscapes as a periodic potential. An interesting result of
such interpretation is the opening for the possibility of Anderson localization phenomena to take
place; whereby species modulate each other’s dynamic habitat landscape. In this scenario E. coli
cells modulate the potential seen by P.aeruginosa and introduce randomness to ecological corridors.
In this way E. coli can induce strong localization in the spatial distribution of the P.aeruginosa
metapopulation. This work highlights the importance of invisible corridor interactions and their
potential to determine patterns of patch occupancy.
Building on these results we next made an explicit connection between the topological properties
of spatially structured microbial landscapes and Taylor’s Law, which asserts that the fluctuations
within a metapopulation is a power law function of the mean. This statistical phenomena of populations, while well-documented in both the macro- and microscopic world, has yet to be connected
to processes shaping spatially structured microbial populations and communities. Pursuing this
analogy from solid state physics further we generated different degrees of randomness in the patchconnecting ecological corridor widths within a microfabricated microfluidics landscape, we found
that a critical level of randomness leads to a qualitative transition in the fluctuation scaling of an
Escherichia coli metapopulation. That induced randomness leads to such a result is neither expected experimentally nor completely understood theoretically. Nevertheless, these results bring a
landscape perspective to Taylor’s law and the desire to connect this phenomena to ecological processes. Furthermore, bridging Taylor’s Law with other ecological scaling laws is an ongoing effort
in the field of macroecology and one which we think would benefit from collaborations between
theoreticians and experimental cell biophysics techniques like the one implemented here.
Finally, given the unique perspective of this collaborative effort between cell biophysics and
theoretical ecology, we conclude this thesis with a review of the literature in the field. Primarily, we
focus on the necessary theoretical ecology needed for cell biophysicists to interpret their experimental
results. In particular, we review landmark experimental cell biophysics discoveries from the past 15
years ranging from single-cell, population and community/biofilm studies, as well as following-up
with newer findings all of which we discuss from an ecological viewpoint.
Description
Tesis (Doctoral of Philosophy degree in Biological Sciences : Ecology)--Pontificia Universidad Católica de Chile, 2021