BSC: Understanding the Key Players of N2 Fixation in European Biological Soil Crusts

Biological soil crusts (BSCs) are present in habitats where the growth of vascular plants is limited and play an essential role in soil stabilization…
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✉ dagmar.woebken(at)univie.ac.at

“Soils” comprise many different habitats for microorganisms, even at the micro-scale, which is one factor that explains the enormous diversity of soil microbial communities. Soil habitats often represent challenging conditions for the residing microbes and yet, they endure and might even flourish in specific situations. Many questions regarding their adaptation to stressful conditions in soil habitats and the factors that influence their activity remain unanswered.
In my group, we are investigating the genomic and physiological features that allow for the survival and success of soil microorganisms. We aim to elucidate their survival strategies, as well as patterns and processes during resuscitation. Projects cover arid soils (desert biological soil crusts) that experience extended droughts, and temperate soils that are limited in easily available carbon sources. To include the other end of the spectrum, we also work with plant-associated habitats, where soil microorganisms are provided with energy-rich root exudates. Here we are particularly interested in how plant microbiomes are assembled and their potential beneficial effects, like nitrogen fixation or salt-stress mitigation.
For our investigations, we combine molecular techniques (such as metagenomics and metatranscriptomics), stable isotope probing and single-cell approaches (such as NanoSIMS and Raman microspectroscopy) with process-level biogeochemical methods and cultivation-based investigations.
Soil microorganisms are faced with unpredictable conditions due to environmental stressors (such as water, energy or nutrient limitation), and therefore the majority is assumed to be in a state of ‘dormancy’ – a state with low metabolic activity enabling long-term persistence. We are particulalrly interested in microbial communities that inhabit surface soils of arid deserts – so-called biological soil crusts or biocrusts. This environment experiences persistent (high) UV irradiation, heat and osmotic stress in addition to limited water availability, with favorable conditions caused by rain surmounting to only few days during a couple months per year.
A metagenome investigation of crusts in the Negev Desert, Israel, revealed diverse physiological potential and diverse survival strategies within the microbial community. While the potential for sporulation was only found in a small proportion of the community, oxidation of atmospheric hydrogen gas (H2) seemed to be a more common survival mechanism. However, dormancy cannot be sustained indefinitely, and therefore phases of resuscitation must also play an important role for long-term survival of desert soil microorganisms.
By mimicking rain events and combining metagenome-centered metatranscriptomics with heavy-water incubations and NanoSIMS, we revealed that biocrust microbial communities are perfectly adapted to unpredictable and short-lived rain events. This is mediated via rapid and simultaneous resuscitation of the majority of cells and taxonomical and physiological diverse groups. Additionally, these microorganisms are prepared for sudden osmotic changes and thus protected from significant cell loss. Together, these mechanisms enable long-term survival of biocrusts bacteria and explain the observed limited productivity.

The Acidobacteriota are characterized by large phylogenetic diversity and great abundance in soils worldwide. Being particularly successful in these often carbon-limited soils, we focus on this group with the goal to elucidate the physiological features that enable them to survive or even thrive in the often-challenging soil habitats. In a comparative genomic investigation, we identified different physiological capacities that could provide them with an advantage in soil. These features were investigated in detail in a multidisciplinary approach, revealing the unexpected use of low-affinity terminal oxidases to respire nano-molar concentrations of oxygen and the oxidation of H2 during starvation. Our studies uncovered great physiological flexibility of this abundant group of soil bacteria, which, together with H2 scavenging as a survival strategy, might explain the success and thus ubiquity of these bacteria. We have received funding for this project by the FWF, Austrian Science Fund (project No. P 26392-B20).

Plant-associated habitats in soil, such as the rhizosphere, represent more favorable situations for microorganisms, as plant roots excrete carbon compounds that can be readily utilized. In several projects, we investigate how plants influence the microbial community structure and as well as activity in their vicinity and the effect of this association. One focus are bacteria that fix atmospheric N2 in association with plants, as the carbon-rich rhizosphere could be a suitable niche for them considering the high energy demand for this process. We are currently investigating diazotrophs associated with grasses and herbs in an Austrian Alpine grassland, with the goal to decipher the processes influencing the diazotroph community assembly and activity, such as fertilization and vegetation. For our investigations of diazotrophs in soils, we developed a toolbox of stable-isotope labeling techniques along with a bioinformatic pipeline, NifMAP, to analyze nifH amplicons.
Another focus is the plant-ectomycorrhiza-bacteria symbiosis, where we explored the assembly of bacteria and were able to follow the transfer of recent plant photosynthates to ectomycorrhizal hyphae-associated bacteria via nanoSIMS. The Woebken group is also involved in a project led by Veronika Mayer investigating microbial communities in tropical ant-plant associations. In an exciting new project, we are studying the associated microbiome of halophytic plants together with Stefanie Wienkoop with the goal to decipher the beneficial effects of this association.


Biological soil crusts (BSCs) are present in habitats where the growth of vascular plants is limited and play an essential role in soil stabilization…

Soils are considered the last scientific frontiers that harbor one of the most diverse microbial communities on Earth. It is hypothesized that this…

The terrestrial nitrogen (N) cycle is essential for the Earth’s biosphere and intimately linked by microbial activity. Understanding the microorganism…
Imminger S, Meier DV, Schintlmeister A, Legin A, Schnecker J, Richter A et al. Survival and rapid resuscitation permit limited productivity in desert microbial communities. Nature Communications. 2024 Dec;15(1):3056. Epub 2024 Apr 17. doi: 10.1038/s41467-024-46920-6
Trojan D, García-Robledo E, Hausmann B, Revsbech NP, Woebken D, Eichorst SA. A respiro-fermentative strategy to survive nanoxia in Acidobacterium capsulatum. FEMS microbiology ecology. 2024 Nov 18;100(12):fiae152. doi: 10.1093/femsec/fiae152
Dietrich M, Panhölzl C, Angel R, Giguere AT, Randi D, Hausmann B et al. Plant roots affect free-living diazotroph communities in temperate grassland soils despite decades of fertilization. Communications Biology. 2024 Jul 11;7(1):846. doi: 10.1038/s42003-024-06522-w
Barrajon-Santos V, Nepel M, Hausmann B, Voglmayr H, Woebken D, Mayer VE. Dynamics and drivers of fungal communities in a multipartite ant-plant association. BMC Biology. 2024;22(1):112. doi: 10.1186/s12915-024-01897-y
Nepel M, Mayer VE, Barrajon-Santos V, Woebken D. Bacterial diversity in arboreal ant nesting spaces is linked to colony developmental stage. Communications Biology. 2023 Dec;6(1):1217. doi: 10.1038/s42003-023-05577-5
Dagmar Wöbken is part of the FWF-funded Cluster of Excellence (CoE)

