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Abstract Microbial communities are typically characterized by some degree of self-organization. In biological soil crust (biocrust) communities, vertical organization of resident populations at the mm scale is driven by organismal adaptations to physicochemical microniches. However, the extent of horizontal organization and its driving processes are unknown. Using a combination of observational and genetic mapping, we provide evidence for a highly defined, horizontal self-organization (patchiness) at the mm to cm scale in a successionally early biocrust community dominated by the pioneer cyanobacteria, Microcoleus vaginatus (Microcoleaceae) and Parifilum sp. (Coleofasciculaceae). Experiments with representative isolates of each species demonstrate that the phenomenon is driven by active spatial segregation based on cross-species sensing through the exometabolome acted upon with motility responses. Further, we show that both species share the ability to enrich for specialized cyanospheres of heterotrophic bacteria at smaller scales, and that these cyanospheres are characterized by compositional host-specificity, thus expanding the reach of spatial patchiness beyond primary producers. Our results highlight the importance of specific microbial interactions in the emergence of microbiome compositional architecture and the enhancement of microbial diversity.