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 N 2 -fixation contributes significantly to the nitrogen (N) budget of arid land ecosystems. In mature crusts, N 2 -fixation is largely attributed to heterocystous cyanobacteria; however, early successional crusts possess few N 2 -fixing cyanobacteria and this suggests that microorganisms other than cyanobacteria mediate N 2 -fixation during the critical early stages of BSC development. DNA stable isotope probing with 15 N 2 revealed that Clostridiaceae and Proteobacteria are the most common microorganisms that assimilate 15 N 2 in early successional crusts. The Clostridiaceae identified are divergent from previously characterized isolates, though N 2 -fixation has previously been observed in this family. The Proteobacteria identified share 498.5% 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.

Chronic Physical Disturbance Substantially Alters the Response of Biological Soil Crusts to a Wetting Pulse, as Characterized by Metatranscriptomic Sequencing

“…A lack of diazotrophic cyanobacteria in early and disturbed crusts is supported by reductions of nitrogen fixation potential as measured by acetylene reduction by up to 250% (Evans R. D. and Belnap J., 1999; Zhou et al, 2016). However, the presence of non-cyanobacterial diazotrophs, predominantly within the phyla Firmicutes and Proteobacteria in early successional stage crusts has been presented as evidence that the nitrogen fixation potential of early successional biocrust may be under-estimated (Pepe-Ranney et al, 2016) The metatranscriptome data presented here suggest that nitrogen fixation potential is significantly reduced in trampled soils as assessed by the abundance of nitrogen fixation transcripts in the trampled soils (Fig. 6).…”

Patterns and Controls on Nitrogen Cycling of Biological Soil Crusts

“…Light cyanobacterial biocrusts (dominated by low biomass Microcoleus spp., which are typically less mature) showed the lowest areal rates (~0.6 nmols C 2 H 4 cm À2 h À1 ). Recent evidence suggests that N fixation in these light cyanobacterial biocrusts is associated with heterotrophic diazotrophic bacteria in the Clostridiaceae and Proteobacteria groups (Pepe-Ranney et al 2015). Moss biocrusts and dark cyanobacterial biocrusts, dominated by a mix of Nostoc spp., Tolypothrix spp., Scytonema spp., as well as Microcoleus spp., showed an average of~3-4 times higher rates than light biocrusts, whereas the cyanolichen Collema spp.…”

Hydration status and diurnal trophic interactions shape microbial community function in desert biocrusts

“…These data generally delineate the interplay between multilevel trophic interactions Nunes da Rocha et al, 2015;Pepe-Ranney et al, 2016) and surrounding environmental conditions (Caruso et al, 2011). Biocrusts host a complex community of diverse autotrophs and heterotrophs (hundreds of species including about 20 generic or subgeneric taxa of Cyanobacteria) (Bowker et al, 2010a, b;Garcia-Pichel et al, 2013).…”