Sunday, July 22, 2018

Self-organization of bacterial populations

Fluorescent bacteria in glass microchannels

In many environments, hundreds, sometimes thousands of different microbial species coexist as mixtures of cells of various sizes and shapes. For example, each human being teems with their very own and unique microbial mixture (trillions of cells), as the human microbiome project unveiled a few years ago. Microbial diversity in soil is equally possibly even moreastounding, with a gram of rich soil capable to host thousands to millions of distinct bacterial and archaeal species, as well as hundreds of fungal and protistan species. A recent study in the magazine Nature highlights the results of the earth microbiome project, which aims at revealing the extent of  microbial diversity on our planet.

Yet, despite this wealth of diversity, microbial communities are not simply soups of species – there is order hiding behind this curtain of complexity. Actually, the more we look, the more we find patterns of microbial organization in the natural world. Some patterns are obvious and have been known for a long time, such as the distinct layers of microorganisms visible with the naked eye in sections of microbial mats. The vast majority of patterns, however, reveal themselves only at the scale of individual microbes, that is, at the microscopic scale. See, for example, the beautiful arrangements revealed in  the lab of Jessica Mark Welch at the University of Chicago. 

Microbial populations are thus often spatially organized at small scale, and in a very defined and refined way. But how does it work? Obviously, microbes don't organize following some kind of blueprint that is imposed on the community!... But what then? Part of the answer seems to reside in so-called
self-organization processes. With such processes, patterns emerge from the individual behavior of cells that can only sense the conditions in their local environment and react accordingly. This in appearance simple process at the individual level can lead to seemingly complex patterns of organization at larger scale. Think of bird murmuration, or of how ants can form bridges with their own bodies! I also discussed spatial patterns of bacterial organization triggered by metabolic cooperation in a previous post.

In a recent paper whose lead author is my colleague Benedict Borer, we examined some of the basic processes that can lead to bacterial spatial self-organization. (In that study we were specifically interested in pore networks that mimic the spatial structure of soil aggregates, but the processes that matter here are valid in other kinds of environments as well.) The idea is as follows. In a given habitat, bacterial populations with distinct metabolic capabilities and food preferences would spontaneously arrange in space in order to optimize their use of the available resources. We thought there must be two necessary conditions for that. First, that the bacterial cells have some level of motility (which could be flagellar motility, such as swimming, or simply movement provide by growth and cell division). Second, that gradients of carbon and nutrients are present in the habitat (i.e. there must be some spatial heterogeneity for the microbes to respond to).  

We chose to work with two bacterial species that differ on their ability to respire: one is a strict aerobe (Pseudomonas putida), which only respires using oxygen as final electron acceptor, while the other (Pseudomonas veronii) is a facultative anaerobe that can respire with oxygen but also with nitrate as final electron acceptor. Both species are motile thanks to flagella that they can use to swim within liquid films. To facilitate observation, the two species were each tagged with a distinct fluorescent protein (green or red). The two bacterial populations were inoculated into micrometric pore networks with various structures,  and which allowed us to create gradients of oxygen (coming from the periphery of the network) and of carbon source (citrate, coming from the center of the network). Although initially well-mixed in the center of the network, after a week of incubation the two bacterial species segregated in the network to form two distinct and coexisting populations (see figure below). One grew preferentially where the oxygen was more abundant (the obligate aerobe), while the other could occupy the anoxic niche at the center of the network, which also contained more carbon.
The two bacterial populations, initially well-mixed, grow and segregate in the pore network as function of their respiration metabolism. From Borer et al., 2018

Interestingly, this spatial organization did not occur when carbon source and oxygen were provided together (i.e., there was no counter-gradients of oxygen and carbon). Another intriguing result was that the coexistence of the two species, as seen in the figure, could not been achieved in well-mixed liquid environments (vials or flasks), because one of the species would always win over and dominate the community (see below). This illustrates how the habitat spatial structure can help limit competition and maintain species coexistence.

Experimental and modeling results show competitive exclusion in homogeneous cultures (a) and coexistence in structured pore networks (b). The percentage corresponds to the connectivity in the network (100% is highest connectivity).
Admittedly, our system is artificial and our community only composed of two species... Yet,  the basic mechanisms that we observed most probably also apply to more complex environments and could participate to the final structure of the community. Bacteria have a remarkable faculty of optimizing their distribution and activity in complex habitats, which we could demonstrate with our simple mathematical and experimental models.


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