Abstract

Biological soil crusts (biocrusts) release the reactive nitrogen gases (Nr) nitrous acid (HONO) and nitric oxide (NO) into the atmosphere, but the underlying microbial process controls have not yet been resolved. In this study, we analyzed the activity of microbial consortia relevant in Nr emissions during desiccation using transcriptome and proteome profiling and fluorescence in situ hybridization. We observed that < 30 min after wetting, genes encoding for all relevant nitrogen (N) cycling processes were expressed. The most abundant transcriptionally active N-transforming microorganisms in the investigated biocrusts were affiliated with Rhodobacteraceae, Enterobacteriaceae, and Pseudomonadaceae within the Alpha- and Gammaproteobacteria. Upon desiccation, the nitrite (NO2−) content of the biocrusts increased significantly, which was not the case when microbial activity was inhibited. Our results confirm that NO2− is the key precursor for biocrust emissions of HONO and NO. This NO2− accumulation likely involves two processes related to the transition from oxygen-limited to oxic conditions in the course of desiccation: (i) a differential regulation of the expression of denitrification genes; and (ii) a physiological response of ammonia-oxidizing organisms to changing oxygen conditions. Thus, our findings suggest that the activity of N-cycling microorganisms determines the process rates and overall quantity of Nr emissions.

Highlights

  • Soils host one of the most diverse microbiomes on Earth [1] with abundances of prokaryotes reaching 4 – 20 × 109 cm−3 [2]

  • nitrogen gases (Nr) emissions and mineral nitrogen content of biocrusts Over the course of the flux measurements, the highest HONO and nitric oxide (NO) emissions were observed at ~20% water holding capacity (WHC)

  • The maximum HONO and NO values at T2 were significantly lower as compared to T3 (Fig. 2; HONOMax: DF = 4, t value = −4.64, p = 0.01; NOMax: DF = 4, t value = −2.82, p = 0.048; Table S1b), since the measurements were stopped before the maximum emissions were reached

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Summary

Introduction

Soils host one of the most diverse microbiomes on Earth [1] with abundances of prokaryotes (bacteria and archaea) reaching 4 – 20 × 109 cm−3 [2]. Biological soil crusts (biocrusts) represent a special type of soil microbiome, colonizing the uppermost layer of the soil in arid and semi-arid ecosystems worldwide [4]. They are composed of a photoautotrophic upper layer with poikilohydric (desiccation-tolerant) organisms, such as cyanobacteria, algae, lichens, and bryophytes, and a layer below with heterotrophic microorganisms [5,6,7,8]. Biocrusts occur globally in regions with dry microclimatic conditions, such as drylands They cover approximately 12% of the Earth’s terrestrial surface, corresponding to an area of ~18 × 106 km2 [9, 10]. Up to 70% of the soil surface is covered by biocrusts [4]

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