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Non-cyanobacterial diazotrophs mediate dinitrogen fixation in biological soil crusts during early crust formation.

ABSTRACT: Biological soil crusts (BSCs) are key components of ecosystem productivity in arid lands and they cover a substantial fraction of the terrestrial surface. In particular, BSC N2-fixation contributes significantly to the nitrogen (N) budget of arid land ecosystems. In mature crusts, N2-fixation is largely attributed to heterocystous cyanobacteria; however, early successional crusts possess few N2-fixing cyanobacteria and this suggests that microorganisms other than cyanobacteria mediate N2-fixation during the critical early stages of BSC development. DNA stable isotope probing with (15)N2 revealed that Clostridiaceae and Proteobacteria are the most common microorganisms that assimilate (15)N2 in early successional crusts. The Clostridiaceae identified are divergent from previously characterized isolates, though N2-fixation has previously been observed in this family. The Proteobacteria identified share >98.5% small subunit rRNA gene sequence identity with isolates from genera known to possess diazotrophs (for example, Pseudomonas, Klebsiella, Shigella and Ideonella). The low abundance of these heterotrophic diazotrophs in BSCs may explain why they have not been characterized previously. Diazotrophs have a critical role in BSC formation and characterization of these organisms represents a crucial step towards understanding how anthropogenic change will affect the formation and ecological function of BSCs in arid ecosystems.

SUBMITTER: Pepe-Ranney C

PROVIDER: S-EPMC4737922 | biostudies-literature | 2016 Feb

REPOSITORIES: biostudies-literature

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Non-cyanobacterial diazotrophs mediate dinitrogen fixation in biological soil crusts during early crust formation.

Pepe-Ranney Charles C Koechli Chantal C Potrafka Ruth R Andam Cheryl C Eggleston Erin E Garcia-Pichel Ferran F Buckley Daniel H DH

The ISME journal 20150626 2

Biological soil crusts (BSCs) are key components of ecosystem productivity in arid lands and they cover a substantial fraction of the terrestrial surface. In particular, BSC N2-fixation contributes significantly to the nitrogen (N) budget of arid land ecosystems. In mature crusts, N2-fixation is largely attributed to heterocystous cyanobacteria; however, early successional crusts possess few N2-fixing cyanobacteria and this suggests that microorganisms other than cyanobacteria mediate N2-fixatio ...[more]

PMID: 26114889

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Project description:Here we report details of the European research initiative "Soil Crust International" (SCIN) focusing on the biodiversity of biological soil crusts (BSC, composed of bacteria, algae, lichens, and bryophytes) and on functional aspects in their specific environment. Known as the so-called "colored soil lichen community" (Bunte Erdflechtengesellschaft), these BSCs occur all over Europe, extending into subtropical and arid regions. Our goal is to study the uniqueness of these BSCs on the regional scale and investigate how this community can cope with large macroclimatic differences. One of the major aims of this project is to develop biodiversity conservation and sustainable management strategies for European BSCs. To achieve this, we established a latitudinal transect from the Great Alvar of Öland, Sweden in the north over Gössenheim, Central Germany and Hochtor in the Hohe Tauern National Park, Austria down to the badlands of Tabernas, Spain in the south. The transect stretches over 20° latitude and 2,300 m in altitude, including natural (Hochtor, Tabernas) and semi-natural sites that require maintenance such as by grazing activities (Öland, Gössenheim). At all four sites BSC coverage exceeded 30 % of the referring landscape, with the alpine site (Hochtor) reaching the highest cyanobacterial cover and the two semi-natural sites (Öland, Gössenheim) the highest bryophyte cover. Although BSCs of the four European sites share a common set of bacteria, algae (including cyanobacteria) lichens and bryophytes, first results indicate not only climate specific additions of species, but also genetic/phenotypic uniqueness of species between the four sites. While macroclimatic conditions are rather different, microclimatic conditions and partly soil properties seem fairly homogeneous between the four sites, with the exception of water availability. Continuous activity monitoring of photosystem II revealed the BSCs of the Spanish site as the least active in terms of photosynthetic active periods.

Project description:As the critical ecological engineers, biological soil crusts (biocrusts) are considered to play essential roles in improving substrate conditions during ecological rehabilitation processes. Physical disturbance, however, often leads to the degradation of biocrusts, and it remains unclear how the physical disturbance affects biocrust microorganisms and their related metabolism. In this study, the photosynthetic biomass (indicated by chlorophyll a), nutrients, enzyme activities, and bacterial communities of biocrusts were investigated in a gold mine tailing of Central China to evaluate the impact of physical disturbance on biocrusts during the rehabilitation process of gold mine tailings. The results show that physical disturbance significantly reduced the photosynthetic biomass, nutrient contents (organic carbon, ammonium nitrogen, nitrate nitrogen, and total phosphorus), and enzyme activities (β-glucosidase, sucrase, nitrogenase, neutral phosphatase, and urease) of biocrusts in the mine tailings. Furthermore, 16S rDNA sequencing showed that physical disturbance strongly changed the composition, structure, and interactions of the bacterial community, leading to a shift from a cyanobacteria dominated community to a heterotrophic bacteria (proteobacteria, actinobacteria, and acidobacteria) dominated community and a more complex bacterial network (higher complexity, nodes, and edges). Altogether, our results show that the biocrusts dominated by cyanobacteria could also develop in the tailings of humid region, and the dominants (e.g., Microcoleus) were the same as those from dryland biocrusts; nevertheless, physical disturbance significantly reduced cyanobacterial relative abundance in biocrusts. Based on our findings, we propose the future work on cyanobacterial inoculation (e.g., Microcoleus), which is expected to promote substrate metabolism and accumulation, ultimately accelerating the development of biocrusts and the subsequent ecological restoration of tailings.

Dataset Information

Non-cyanobacterial diazotrophs mediate dinitrogen fixation in biological soil crusts during early crust formation.

Publications

Non-cyanobacterial diazotrophs mediate dinitrogen fixation in biological soil crusts during early crust formation.

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