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Article Is Available Online At Biogeosciences, 15, 3831–3840, 2018 https://doi.org/10.5194/bg-15-3831-2018 © Author(s) 2018. This work is distributed under the Creative Commons Attribution 4.0 License. Fungal loop transfer of nitrogen depends on biocrust constituents and nitrogen form Zachary T. Aanderud1, Trevor B. Smart1, Nan Wu2, Alexander S. Taylor1, Yuanming Zhang2, and Jayne Belnap3 1Department of Plant and Wildlife Sciences, Brigham Young University, Provo, UT 84602, USA 2Xinjiang Institute of Ecology and Geography, Key Laboratory of Biogeography and Bioresource in Arid Land, Chinese Academy of Sciences, Urumqi 830011, China 3US Geological Survey, Southwest Biological Science Center, 2290 SW Resource Blvd., Moab, UT 84532, USA Correspondence: Zachary T. Aanderud ([email protected]) Received: 15 October 2017 – Discussion started: 20 November 2017 Revised: 17 May 2018 – Accepted: 26 May 2018 – Published: 22 June 2018 Abstract. Besides performing multiple ecosystem services cant enrichment of δ15N in A. hymenoides leaves but only in individually and collectively, biocrust constituents may also cyanobacteria biocrusts translocating 15N, offering evidence create biological networks connecting spatially and tempo- of links between biocrust constituents and higher plants. Our rally distinct processes. In the fungal loop hypothesis rain- results suggest that minor rainfall events may initiate fun- fall variability allows fungi to act as conduits and reser- gal loops potentially allowing constituents, like dark septate C − voirs, translocating resources between soils and host plants. Pleosporales, to rapidly translocate N from NH4 over NO3 To evaluate the extent to which biocrust species composi- through biocrust networks. tion and nitrogen (N) form influence loops, we created a mi- 15 C 15 − nor, localized rainfall event containing NH4 and NO3 . We then measured the resulting δ15N in the surrounding dry cyanobacteria- and lichen-dominated crusts and grass, 1 Introduction Achnatherum hymenoides, after 24 h. We also estimated the biomass of fungal constituents using quantitative PCR Fungi may act as conduits for biological networks, connect- and characterized fungal communities by sequencing the ing belowground ecosystem processes to plants. Soil fungi 18S rRNA gene. We found evidence for the initiation of fun- contribute to all aspects of litter decomposition via the fol- gal loops in cyanobacteria-dominated crusts where 15N, from lowing: the generation of a myriad of extracellular enzymes 15 C −1 15 (Osono, 2007; Schneider et al., 2012); altered trophic dy- NH4 , moved 40 mm h in biocrust soils with the δ N of crusts decreasing as the radial distance from the water addi- namics, decomposer species diversity, and nutrient turnover tion increased (linear mixed effects model (LMEM)): R2 D rates (Hattenschwiler et al., 2005); and by forming multiple 15 0:67, F2;12 D 11, P D 0:002). In cyanobacteria crusts, δ N, types of endophyte-plant symbioses (Johnson et al., 1997; 15 C Saikkonen et al., 2004). Endophytic fungi, in particular, form from NH4 , was diluted as Ascomycota biomass increased 2 (LMEM: R D 0:63, F2;8 D 6:8, P D 0:02), Ascomycota ac- hubs connecting spatially and temporally distinct microbial- counted for 82 % (±2.8) of all fungal sequences, and one mediated soil processes and plants. For example, the per- order, Pleosporales, comprised 66 % (±6.9) of Ascomycota. vasive distribution of mycorrhizae in mesic systems allows The seeming lack of loops in moss-dominated crusts may common mycorrhizal networks to deliver essential resources. stem from the relatively large moss biomass effectively ab- Therefore, mycorrhizae promote or hinder seedling growth sorbing and holding N from our minor wet deposition event. depending on the network species composition (van der Hei- 15 C jden and Horton, 2009), and facilitate the one-way transfer The substantial movement of NH4 may indicate a fungal preference for the reduced N form during amino acid trans- of multiple forms of nitrogen (N) and phosphorus (P) be- formation and translocation. We found a marginally signifi- tween two plant species linked by arbuscular mycorrhizae and ectomycorrhizae (He et al., 2003; Walder et al., 2012). In Published by Copernicus Publications on behalf of the European Geosciences Union. 3832 Z. T. Aanderud et al.: Fungal loop transfer of nitrogen depends on biocrust constituents and nitrogen form xeric systems, endophytic fungi are also implicated in mov- are Ascomycota, with the Pleosporales being widespread and ing resources within biological networks in a theory known dominant (Bates et al., 2012; Porras-Alfaro et al., 2011). as the fungal loop hypothesis. The hypothesis states that Pleosporales, along with other Ascomycota fungal orders, fungi, supported by biotrophic carbon (C) from plants and contain dark septate endophytes (Jumpponen and Trappe, terrestrial cyanobacteria, act as intermediate reservoirs trans- 1998). Dark septate endophytes are thermal- and drought- forming and translocating resources between soils and plants tolerant fungi due to melanin-rich cell walls conferring pro- (Collins et al., 2008, 2014). Perhaps the most notable exam- tection from UV and drought stress (Gostincar et al., 2010). ple of a fungal loop, albeit from a limited number of studies, Taken together, the prevalence of dark septate fungi in desert occurred in fungal-dominated cyanobacteria biocrusts from systems, along with their ability to maintain metabolic activ- 15 − a Chihuahuan Desert grassland. Specifically, NO3 applied ity under low water potentials (Barrow, 2003), makes these to a root-free biocrust rapidly moved into the perennial grass, endophytes excellent candidates to translocate resources in Bouteloua sp., up to 1 m away within 24 h (Green et al., loops (Green et al., 2008). 2008). Furthermore, 13C-labeled glutamic acid applied to the Minor rainfall events may allow fungi to act as conduits leaf surfaces of Bouteloua was found in biocrusts. Despite and reservoirs for N. To investigate the potential for biocrust the intriguing evidence, many aspects of this burgeoning hy- constituents and N form to influence the movement of N pothesis remain to be validated (Collins et al., 2014). through the putative fungal loops, we created minor, local- 15 15 C Biocrust composition and soil moisture availability inter- ized rainfall events. We then measured δ N, from N-NH4 15 − actions may dictate the movement of resources in fungal and N-NO3 , within the surrounding dry cyanobacteria- loops. Desert fungal–plant interactions occur across spatially and moss-dominated crusts, and grass, Achnatherum hy- discontinuous patches of vegetation interspersed by patches menoides (Indian ricegrass). In tandem with 15N analyses, of soils colonized by biocrusts (Belnap et al., 2005). Fungi we estimated the biomass of two major divisions of fungi participating in loops are necessarily associated with a mo- (Ascomycota and Basidiomycota) and bacteria, and charac- saic of other biocrust organisms (i.e., cyanobacteria, green terized fungal communities by sequencing the 18S rRNA algae, lichens, mosses, and other bacteria). The metabolic ac- gene to identify potential links between fungal taxa and 15N tivity of biocrust constituents participating in fungal loops, movement. including plants, are moisture-dependent and regulated by the magnitude and seasonality of episodic rainfall events. A pulse–reserve paradigm (Collins et al., 2008) may ex- 2 Materials and methods plain biological activities where minor rainfall pulses stim- 2.1 Site description ulate microorganisms, generating reserves of resources to be exploited during subsequent rainfall events (Huxman et We conducted our study in two cold desert ecosystems of al., 2004; Welter et al., 2005). In such loops, minor rainfall the Colorado Plateau, UT. One site was near Castle Val- events may stimulate N2 fixation by free or lichen-associated ley (40◦05027.4300 N–112◦18018.2400 W) and the other was cyanobacteria (Belnap et al., 2003), N mineralization by bac- adjacent to the US Geological Survey (USGS) Southwest teria and fungi (Cable and Huxman, 2004; Yahdjian and Sala, Biological Science Center Research Station in Moab, UT 2010), and nitrification and possibly denitrification (Wang et ◦ 0 00 ◦ 0 00 C − (40 05 27.43 N–112 18 18.24 W). Rugose crusts consist- al., 2014), potentially altering levels of NH4 or NO3 . Fun- ing of 22 % moss Syntrichia caninervis, 5–7 % cyano- gal species, including fungal endophytes, may compete with lichens Collema tenax , and Collema coccophorum and 55 % mosses, lichen, cyanobacteria, and other bacteria for newly cyanobacteria cover the Castle Valley site (Darrouzet-Nardi released N. Once sequestered, the N may be transformed et al., 2015), while smooth, light algal crusts dominated into amino acids and transported within mycelium (Jin et al., by one cyanobacterium, Microcoleus vaginatus, cover the 2012; Behie and Bidochka, 2014). Larger rainfall events may USGS site. Across both sites, vegetation is dominated by the then activate plants, allowing the host plant to receive N from perennial grass Achnatherum hymenoides (Roem & Schult) the fungi and transfer photosynthate to the fungal endophyte. and the native perennial shrub Atriplex confertifolia (Torr. & If fungal endophytes are poor competitors for newly released Frém). Mean annual temperature and precipitation at Cas- N, preferentially sequester one inorganic N form over an- ◦ C tle Valley are 13 C and 269 mm, respectively, while the other, or more efficiently transform and transport
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