Spatial self-segregation of pioneer cyanobacterial species drives microbiome organization in biocrusts

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.

Niche formation and metabolic interactions result in stable diversity in a spatially structured cyanobacterial community

“…Where analysed, these communities are found to be distinct from the microbial composition of the surrounding environment (10, 14). These observations align with the suggestion that there exists a cyanosphere, where specific microbes associate closely with cyanobacteria as they form granule and aggregate structures (14–18).…”

“…Where analysed, these communities are found to be distinct from the microbial composition of the surrounding environment (10,14). These observations align with the suggestion that there exists a cyanosphere, where specific microbes associate closely with cyanobacteria as they form granule and aggregate structures (14)(15)(16)(17)(18). One of the better studied natural cyanobacterial aggregates are those formed by the filamentous Trichodesmium species, found commonly in the ocean and coastal waters.…”

Environmental conditions play a key role in controlling the composition and diversity of Colombian biocrust microbiomes

“…Tables were merged based on the primers set used for Illumina sequencing in each of the studies included in the meta-analysis. Accordingly, feature tables from USA ( Couradeau et al, 2016 ; Fernandes et al, 2018 ; Giraldo-Silva et al, 2019 ; Nelson et al, 2022 ), Mexico ( Becerra-Absalón et al, 2019 ) and Colombia (this study) were merged into a single table (Primer set: general bacterial 515F; 806R) and the two studies from Brazil ( Machado-de-Lima et al, 2019 ; Machado de Lima et al, 2021 ) were merged in a separate table (Primer set: cyanobacterial specific CYA359 and 781a/d). We then curated the cyanobacterial taxonomy of each of the newly merged tables (merged by countries based on primer sets) by means of phylogenetic placements using Cydrasil 3 ( Roush et al, 2021 ).…”

Spatial organization of a soil cyanobacterium and its cyanosphere through GABA/Glu signaling to optimize mutualistic nitrogen fixation

“…One of its defining traits is the ability to aggregate into bundles of trichomes held within a common sheath through dynamic motility responses [7] that help it attain macroscopic size and initially stabilize unconsolidated soils [7,8]. While M. vaginatus cannot fix nitrogen, it does colonize N-limited bare soils due to its ability to spatially arrange other soil bacteria around it, repelling or avoiding competing cyanobacteria by reacting to their exudates [9] and attracting a mutualistic "cyanosphere microbiome" that trades newly fixed nitrogen in exchange for its photosynthates [10][11][12][13][14]. Further, bundling seems to be an integral part of the mechanism for mutualistic interaction [11], as it is enhanced in culture by N limitation and by the presence of specific cyanosphere mutualists.…”