Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere

Abstract Background Biological soil crusts (biocrusts) are a key component of arid land ecosystems, where they render critical services such as soil surface stabilization and nutrient fertilization. The bundle-forming, filamentous, non-nitrogen-fixing cyanobacterium Microcoleus vaginatus is a pioneer primary producer, often the dominant member of the biocrust microbiome, and the main source of leaked organic carbon. We hypothesized that, by analogy to the rhizosphere of plant roots, M. vaginatus may shape the microbial populations of heterotrophs around it, forming a specialized cyanosphere. Results By physically isolating bundles of M. vaginatus from biocrusts, we were able to study the composition of the microbial populations attached to it, in comparison to the bulk soil crust microbiome by means of high-throughput 16S rRNA sequencing. We did this in two M. vaginatus-dominated biocrust from distinct desert biomes. We found that a small, selected subset of OTUs was significantly enriched in close proximity to M. vaginatus. Furthermore, we also found that a majority of bacteria (corresponding to some two thirds of the reads) were significantly more abundant away from this cyanobacterium. Phylogenetic placements suggest that all typical members of the cyanosphere were copiotrophs and that many were diazotrophs (Additional file 1: Tables S2 and S3). Nitrogen fixation genes were in fact orders of magnitude more abundant in this cyanosphere than in the bulk biocrust soil as assessed by qPCR. By contrary, competition for light, CO2, and low organic carbon concentrations defined at least a part of the OTUs segregating from the cyanobacterium. Conclusions We showed that M. vaginatus acts as a significant spatial organizer of the biocrust microbiome. On the one hand, it possesses a compositionally differentiated cyanosphere that concentrates the nitrogen-fixing function. We propose that a mutualism based on C for N exchange between M. vaginatus and copiotrophic diazotrophs helps sustains this cyanosphere and that this consortium constitutes the true pioneer community enabling the colonization of nitrogen-poor soils. On the other hand, a large number of biocrust community members segregate away from the vicinity of M. vaginatus, potentially through competition for light or CO2, or because of a preference for oligotrophy.