A symbiotic nutrient exchange within the cyanosphere microbiome of the biocrust cyanobacterium, Microcoleus vaginatus

Abstract

Microcoleus vaginatus plays a prominent role as both primary producer and pioneer in biocrust communities from dryland soils. And yet, it cannot fix dinitrogen, essential in often nitrogen-limited drylands. But a diazotroph-rich “cyanosphere” has been described in M. vaginatus, hinting that there exists a C for N exchange between the photoautotroph and heterotrophic diazotrophs. We provide evidence for this by establishing such a symbiosis in culture and by showing that it is selective and dependent on nitrogen availability. In natural populations, provision of nitrogen resulted in loss of diazotrophs from the cyanosphere of M. vaginatus compared to controls, but provision of phosphorus did not. Co-culturing of pedigreed cyanosphere diazotroph isolates with axenic M. vaginatus resulted in copious growth in C and N-free medium, but co-culture with non-cyanosphere diazotrophs or other heterotrophs did not. Unexpectedly, bundle formation in M. vaginatus, diacritical to the genus but not seen in axenic culture, was restored in vitro by imposed nitrogen limitation or, even more strongly, by co-culture with diazotrophic partners, implicating this trait in the symbiosis. Our findings provide direct evidence for a symbiotic relationship between M. vaginatus and its cyanosphere and help explain how it can be a global pioneer in spite of its genetic shortcomings.

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Fig. 1: Comparison of bacterial composition and nitrogen-fixation potential of M. vaginatus cyanosphere communities with varying nutrient additions.
Fig. 2: Co-cultures of M. vaginatus PCC9802 with heterotrophic bacteria on solid, carbon-, and nitrogen-free medium after 20 days of incubation (n = 3).
Fig. 3: Trichome content of axenic M. vaginatus bundles incubated under various conditions (n = 3).

Data availability

Raw sequence data have been submitted to NCBI and are publicly available under BioProject PRJNA630480.

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Acknowledgements

We would like to thank Júlia Gomes Farias for her help with photography. This work was supported in part by the Jornada Basin LTER Graduate Research Fellowship Program and Center for Bio-mediated and Bio-inspired Geotechnics.

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CN, AGS, and FGP conceived the research; CN, FGP designed experiments; CN performed experiments; CN analyzed data; CN, AGS, and FGP discussed results; CN, FGP wrote and edited the paper.

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Correspondence to Ferran Garcia-Pichel.

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Nelson, C., Giraldo-Silva, A. & Garcia-Pichel, F. A symbiotic nutrient exchange within the cyanosphere microbiome of the biocrust cyanobacterium, Microcoleus vaginatus. ISME J (2020). https://doi.org/10.1038/s41396-020-00781-1

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