Pattern diversification during microbial spatial self-organization

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The importance of biodiversity for ecosystem functioning is well-known. Biodiversity can promote interactions that enable or modulate ecosystem functions (i.e., facilitation), determine the amount of niche space occupied within an ecosystem (i.e., complementation), and provide resistance and resilience to environmental perturbations and invasions. While the field of biodiversity-ecosystem functioning is well established, we (i.e., the authors) tend to think of biodiversity as the set of distinct genotypes, phenotypes and/or individual-level traits within an ecosystem. We then use this set to quantify biodiversity metrics, which may consider or disregard the abundances of distinct genotypes, phenotypes or individual-level traits. Is this the end of the story? Are genotypes, phenotypes, and individual-level traits the only components of biodiversity that one must consider?

Fig. 1. Spatial self-organization of a synthetic community consisting of four isogenic strains of the bacterium Pseudomonas stutzeri. Credit: Yinyin Ma (ETHZ, Eawag).

To be frank, we accidentally stumbled upon what we believe might be a novel (or at least poorly recognized) component of biodiversity. Briefly, our main interest is in microbial spatial self-organization, where different microbial cell-types distribute themselves non-randomly across space and form (often beautiful) spatial patterns (Fig. 1). These spatial patterns have consequences for ecosystem functioning, as they can determine the functions performed by a community, the rates at which those functions occur, the evolutionary processes acting on communities, and the resistance and resilience of communities to environmental change and invasions. To investigate the causes and consequences of spatial self-organization, we assemble simple binary communities together from pairs of microbial strains and propagate them across surfaces that are initially spatially homogeneous. What does this have to do with biodiversity? Perhaps naively, we expected that a single pair of microbial strains that interact with each other in a precise manner and expand across an initially homogeneous surface should produce a single pattern of spatial self-organization. To our surprise, however, we found that two different patterns emerge at the same length- and time-scales (Fig. 2). How is this possible? Does this represent a form of biodiversity?

Fig. 2. Spatial self-organization of a synthetic community consisting of two isogenic strains of the bacterium Pseudomonas stutzeri. One strain consumes nitrate to nitrite (blue) while the other consumes the released nitrite (green). Two different spatial patterns form as they expand across space (white and green arrows). The patterns differ in the radial distance between the two strains and in the orientation of the branching formed by the green strain. 

After nearly eight years of work, we feel that we can now answer both of these questions. Regarding the ‘how’, we believe the formation of the two patterns has no genetic basis. Instead, it is a consequence of small differences in the initial spatial positionings of individuals. Regarding whether spatial pattern diversity represents a form of biodiversity, we believe so. The two patterns have different traits; namely, they have different expansion speeds. Spatial pattern diversity thus has consequences on ecosystem properties. A grand challenge for the future is to find clever ways to incorporate this form of biodiversity into modern biodiversity-ecosystem functioning theory.

Dave Johnson

Senior Scientist, Eawag