Seasonal variation and potential roles of dark septate fungi in an arid grassland

LITERATURE CITED

• Aanderud ZT, Smart TB, Wu N, Taylor AS, Zhang Y, Belnap J. 2018. Fungal loop transfer of N depends on biocrust constituents and N form. Biogeosciences 15:3831–3840.
   Web of Science ®Google Scholar
• Abed RM, Al-Sadi AM, Al-Shehi M, Al-Hinai S, Robinson MD. 2013. Diversity of free-living and lichenized fungal communities in biological soil crusts of the Sultanate of Oman and their role in improving soil properties. Soil Biology and Biochemistry 57:695–705.
   Web of Science ®Google Scholar
• Alberton O, Kuyper TW, Summerbell RC. 2010. Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant and Soil 328:459–470.
   Web of Science ®Google Scholar
• Aly AH, Debbab A, Kjer J, Proksch P. 2010. Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Diversity 41:1–16.
   Web of Science ®Google Scholar
• Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM. 2004. Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235.
   PubMed Web of Science ®Google Scholar
• Barron-Gafford GA, Angert AL, Venable DL, Tyler AP, Gerst KL, Huxman TE. 2013. Photosynthetic temperature responses of co-occurring desert winter annuals with contrasting resource-use efficiencies and different temporal patterns of resource utilization may allow for species coexistence. Journal of Arid Environments 91:95–103.
   Web of Science ®Google Scholar
• Bates ST, Donna BL, Lauber CL, Walters WA, Knight R, Fierer N. 2012a. A preliminary survey of lichen associated eukaryotes using pyrosequencing. The Lichenologist 44:137–146.
   Web of Science ®Google Scholar
• Bates ST, Garcia‐Pichel F. 2009. A culture‐independent study of free‐living fungi in biological soil crusts of the Colorado Plateau: their diversity and relative contribution to microbial biomass. Environmental Microbiology 11:56–67.
   PubMed Web of Science ®Google Scholar
• Bates ST, Nash TH, Garcia-Pichel F. 2012b. Patterns of diversity for fungal assemblages of biological soil crusts from the southwestern United States. Mycologia 104:353–361.
   PubMed Web of Science ®Google Scholar
• Bates ST, Nash TH, Sweat KG, Garcia-Pichel F. 2010. Fungal communities of lichen-dominated biological soil crusts: diversity, relative microbial biomass, and their relationship to disturbance and crust cover. Journal of Arid Environments 74:1192–1199.
   Web of Science ®Google Scholar
• Bates ST, Reddy GS, Garcia-Pichel F. 2006. Exophiala crusticola anam. nov. (affinity Herpotrichiellaceae), a novel black yeast from biological soil crusts in the Western United States. International Journal of Systematic and Evolutionary Microbiology 56:2697–2702.
   PubMed Web of Science ®Google Scholar
• Becker SR, Byrne PF, Reid SD, Bauerle WL, McKay JK, Haley SD. 2016. Root traits contributing to drought tolerance of synthetic hexaploid wheat in a greenhouse study. Euphytica 207:213–224.
   Web of Science ®Google Scholar
• Belnap J. 2006. The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrological Processes 20:3159–3178.
   Web of Science ®Google Scholar
• Belnap J, Lange OL. 2003. Biological soil crusts: structure, function, and management. Ecological Studies Book 150. Berlin, Germany: Springer-Verlag. 150 p.
   Google Scholar
• Belnap J, Phillips SL, Miller ME. 2004. Response of desert biological soil crusts to alterations in precipitation frequency. Oecologia 141:306–316.
   PubMed Web of Science ®Google Scholar
• Berthelot C, Leyval C, Foulon J, Chalot M, Blaudez D. 2016. Plant growth promotion, metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites. FEMS Microbiology Ecology 92:Fiw144.
   PubMed Web of Science ®Google Scholar
• Bhatnagar A, Bhatnagar M. 2005. Microbial diversity in desert ecosystems. Current Science 89:91–100.
   Google Scholar
• Billingsley Tobias T, Farrer EC, Rosales A, Sinsabaugh RL, Suding K, Porras-Alfaro A. 2016. Seed associated fungi: mutualists and pathogens, and their potential impact on seed recruitment and community composition. Fungal Ecology 30:10–18.
   Web of Science ®Google Scholar
• Brown SP, Rigdon-Huss AR, Jumpponen A. 2014. Analyses of ITS and LSU gene regions provide congruent results on fungal community responses. Fungal Ecology 9:65–68.
   Web of Science ®Google Scholar
• Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7:335–336.
   PubMed Web of Science ®Google Scholar
• Coe KK, Belnap J, Sparks JP. 2012. Precipitation‐driven carbon balance controls survivorship of desert biocrust mosses. Ecology 93:1626–1636.
   PubMed Web of Science ®Google Scholar
• Coe KK, Sparks JP. 2014. Physiological ecology of dryland biocrust mosses. In. Hanson DT, Steven KR, eds. Photosynthesis in bryophytes and early land plants. Dordrecht, Netherlands: Springer. p. 291–308.
   Google Scholar
• Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM. 2014. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Research 41:1–10.
   Google Scholar
• Colesie C, Gommeaux M, Green ATG, Budel B. 2014. Biological soil crusts in continental Antarctica: Garwood Valley, southern Victoria Land, and Diamond Hill, Darwin Mountains region. Antarctic Science 26:115–123.
   Web of Science ®Google Scholar
• Collins SL, Avolio ML, Gries C, Hallett LM, Koerner SE, La Pierre KL, Rypel AL, Sokol ER, Fey SB, Flynn DF, Jones SK. 2018. Temporal heterogeneity increases with spatial heterogeneity in ecological communities. Ecology 99:858–865.
   PubMed Web of Science ®Google Scholar
• Collins SL, Sinsabaugh RL, Crenshaw C, Green L, Porras‐Alfaro A, Stursova M, Zeglin LH. 2008. Pulse dynamics and microbial processes in aridland ecosystems. Journal of Ecology 96:413–420.
   Web of Science ®Google Scholar
• Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461.
   PubMed Web of Science ®Google Scholar
• Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10:996.
   PubMed Web of Science ®Google Scholar
• Flagg CB, Neff JC, Reynolds RL, Belnap J. 2014. Spatial and temporal patterns of dust emissions (2004–2012) in semi-arid landscapes, southeastern Utah, USA. Aeolian Research 15:31–43.
   Web of Science ®Google Scholar
• Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Molecular Ecology 2:113–118.
   PubMed Web of Science ®Google Scholar
• Gazis R, Rehner S, Chaverri P. 2011. Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences. Molecular Ecology 20:3001–3013.
   PubMed Web of Science ®Google Scholar
• Gostinčar C, Grube M, De Hoog S, Zalar P, Gunde-Cimerman N. 2009. Extremotolerance in fungi: evolution on the edge. FEMS Microbiology Ecology 71:2–11.
   Web of Science ®Google Scholar
• Green LE, Porras-Alfaro A, Sinsabaugh RL. 2008. Translocation of nitrogen and carbon integrates biotic crust and grass production in desert grassland. Journal of Ecology 96:1076–1085.
   Web of Science ®Google Scholar
• Gudmundsdottir PL, Andresson OS. 2019. Fungi in liverwort-based biocrust. Icelandic Agricultural Sciences 32:43–60.
   Web of Science ®Google Scholar
• Hamayun M, Khan SA, Khan AL, Rehman G, Kim YH, Iqbal I, Hussain J, Sohn EY, Lee IJ. 2010a. Gibberellin production and plant growth promotion from pure cultures of Cladosporium sp. MH-6 isolated from cucumber (Cucumis sativus L.). Mycologia 102:989–995.
   PubMed Web of Science ®Google Scholar
• Hamayun M, Khan SA, Khan AL, Tang DS, Hussain J, Ahmad B, Anwar Y, Lee IJ. 2010b. Growth promotion of cucumber by pure cultures of gibberellin-producing Phoma sp. GAH7. World Journal of Microbiology and Biotechnology 26:889–894.
   Web of Science ®Google Scholar
• Hawkes CV, Kivlin SN, Rocca JD, Huguet V, Thomsen MA, Suttle KB. 2011. Fungal community responses to precipitation. Global Change Biology 17:1637–1645.
   Web of Science ®Google Scholar
• Herrera J, Poudel R, Nebel KA, Collins SL. 2011. Precipitation increases the abundance of some groups of root‐associated fungal endophytes in a semiarid grassland. Ecosphere 2:50.
   Web of Science ®Google Scholar
• Herrera JH, Khidir HH, Eudy MD, Porras-Alfaro A, Natvig DO, Sinsabaugh RL. 2010. Shifting fungal endophyte communities colonize Bouteloua gracilis: effect of host tissue and geographical distribution. Mycologia 102:1012–1026.
   PubMed Web of Science ®Google Scholar
• Hesse CN, Mueller RC, Vuyisich M, Gallegos-Graves LV, Gleasner CD, Zak DR, Kuske C. 2015. Forest floor community metatranscriptomes identify fungal and bacterial responses to N deposition in two maple forests. Frontiers in Microbiology 6:337.
   PubMed Web of Science ®Google Scholar
• Hocking AD, Pitt JI. 1980. Dichloran-glycerol medium for enumeration of xerophilic fungi from low-moisture foods. Applied and Environmental Microbiology 39:488–492.
   PubMed Web of Science ®Google Scholar
• Hulsen T, De Vlieg J, Alkema W. 2008. BioVenn-a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9:488.
   PubMed Web of Science ®Google Scholar
• Johnson SL, Kuske CR, Carney TD, Housman DC, Gallegos‐Graves LV, Belnap J. 2012. Increased temperature and altered summer precipitation have differential effects on biological soil crusts in a dryland ecosystem. Global Change Biology 18:2583–2593.
   Web of Science ®Google Scholar
• Jumpponen A, Jones KL. 2010. Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytologist 186:496–513.
   Google Scholar
• Jumpponen A, Trappe JM. 1998. Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytologist 140:295–310.
   PubMed Web of Science ®Google Scholar
• Khan AR, Ullah I, Waqas M, Shahzad R, Hong SJ, Park GS, Jung BK, Lee IJ, Shin JH. 2015. Plant growth-promoting potential of endophytic fungi isolated from Solanum nigrum leaves. World Journal of Microbiology and Biotechnology 31:1461–1466.
   PubMed Web of Science ®Google Scholar
• Khidir HH, Eudy DM, Porras-Alfaro A, Herrera J, Natvig DO, Sinsabaugh RL. 2010. A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland. Journal of Arid Environments 74:35–42.
   Web of Science ®Google Scholar
• Kivlin SN, Emery SM, Rudgers JA. 2013. Fungal symbionts alter plant responses to global change. American Journal of Botany 100:1–13.
   PubMed Web of Science ®Google Scholar
• Knapp DG, Kovács GM, Zajta E, Groenewald JZ, Crous PW. 2015. Dark septate endophytic Pleosporalean genera from semiarid areas. Persoonia 35:87–100.
   PubMed Web of Science ®Google Scholar
• Knapp DG, Pintye A, Kovács GM. 2012. The dark side is not fastidious–dark septate endophytic fungi of native and invasive plants of semiarid sandy areas. PLoS ONE 7: e32570.LangeOL, Belnap J, Reichenberger H, Meyer A. 1997. Photosynthesis of green algal soil crust lichens from arid lands in southern Utah, USA: role of water content on light and temperature responses of CO₂ exchange. Flora 192:1–15.
   Google Scholar
• Li X, He X, Hou L, Ren Y, Wang S, Su F. 2018. Dark septate endophytes isolated from a xerophyte plant promote the growth of Ammopiptanthus mongolicus under drought condition. Scientific Reports 8:7896.
   PubMed Web of Science ®Google Scholar
• Magan N. 2007. Fungi in extreme environments. The Mycota 4:85–103.
   Google Scholar
• Maier S, Muggia L, Kuske CR, Grube M. 2016. Fungi and bacteria in biological soil crusts. In: Weber B, Burkhard B, Belnap J, eds. Biological Soil crusts: an organizing principle in drylands. Ecological Studies Book 226. Berlin Germany: Springer-Verlag. p. 81–100.
   Google Scholar
• Mandyam, K, Jumpponen A. 2005. Seeking the elusive function of the root-colonising dark septate endophytic fungi. Studies in Mycology 53:173–189.
   Google Scholar
• Mandyam K, Jumpponen A. 2008. Seasonal and temporal dynamics of arbuscular mycorrhizal and dark septate endophytic fungi in a tallgrass prairie ecosystem are minimally affected by nitrogen enrichment. Mycorrhiza 18:145–155.
   PubMed Web of Science ®Google Scholar
• Mannaa M, Kim KD. 2017. Influence of temperature and water activity on deleterious fungi and mycotoxin production during grain storage. Mycobiology 45:240–254.
   PubMed Web of Science ®Google Scholar
• Mayerhofer MS, Kernaghan G, Harper KA. 2013. The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza 23:119–128.
   PubMed Web of Science ®Google Scholar
• Menkis A, Allmer J, Vasiliauskas R, Lygis V, Stenlid J, Finlay R. 2004. Ecology and molecular characterization of dark septate fungi from roots, living stems, coarse and fine woody debris. Mycological Research 108:965–973.
   PubMed Web of Science ®Google Scholar
• Morgan JAW, Bending GD, White PJ. 2005. Biological costs and benefits to plant–microbe interactions in the rhizosphere. Journal of Experimental Botany 56:1729–1739.
   PubMed Web of Science ®Google Scholar
• Mueller RC, Belnap J, Kuske CR. 2015. Soil bacterial and fungal community responses to nitrogen addition across soil depth and microhabitat in an arid shrubland. Frontiers in Microbiology 6:891.
   Web of Science ®Google Scholar
• Mueller RC, Gallegos-Graves LV, Kuske CR. 2016. A new fungal large subunit ribosomal RNA primer for high-throughput sequencing surveys. FEMS Microbiology Ecology 92: fiv153.
   Google Scholar
• Nair DN, Padmavathy S. 2014. Impact of endophytic microorganisms on plants, environment, and humans. The Scientific World Journal 2014:250693.
   Google Scholar
• Naznin HA, Kimura M, Miyazawa M, Hyakumachi M. 2013. Analysis of volatile organic compounds emitted by plant growth-promoting fungus Phoma sp. GS8-3 for growth promotion effects on tobacco. Microbes and Environments 28:42–49.
   Google Scholar
• Nelsen MP, Chavez N, Sackett-Hermann E, Thell A, Randlane T, Divakar P, Lumbsch HT. 2011. The cetrarioid core group revisited (Lecanorales: Parmeliaceae). The Lichenologist 43:537–551.
   Web of Science ®Google Scholar
• Newsham KK. 2011. A meta-analysis of plant responses to dark septate root endophytes. New Phytologist 190:783–793.
   PubMed Web of Science ®Google Scholar
• Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. 2020. Vegan: community ecology package. [cited 2021 Feb 16]. Available from https://cran.r-project.org/web/packages/vegan/index.html
   Google Scholar
• Panno L, Bruno M, Voyron S, Anastasi A, Gnavi G, Miserere L, Varese GC. 2013. Diversity, ecological role and potential biotechnological applications of marine fungi associated to the seagrass Posidonia oceanica. New Biotechnology 30:685–694.
   PubMed Web of Science ®Google Scholar
• Paul D, Park K. 2013. Identification of volatiles produced by Cladosporium cladosporioides CL-1, a fungal biocontrol agent that promotes plant growth. Sensors 13:13969–13977
   PubMed Web of Science ®Google Scholar
• Perry RS, Gorbushina A, Engel MH, Kolb VM, Krumbein WE, Staley JT. 2004. Accumulation and deposition of inorganic and organic compounds by microcolonial fungi. In: Harris RA and Ouwehand L, eds. Proceedings of the Third European Workshop on Exo-Astrobiology, Madrid, Spain, 2003 Nov 18–20. Noordwijk, Netherlands: ESA Publications Division. p. 55–58.
   Google Scholar
• Petrovič U, Gunde-Cimerman N, Zalar P. 2000. Xerotolerant mycobiota from high altitude Anapurna soil, Nepal. FEMS Microbiology Letters 182:339–342.
   PubMed Web of Science ®Google Scholar
• Pointing SB, Belnap J. 2012. Microbial colonization and controls in dryland systems. Nature Reviews Microbiology 10:551–562.
   PubMed Web of Science ®Google Scholar
• Porras-Alfaro A, Bayman P. 2011. Hidden fungi, emergent properties: endophytes and microbiomes. Annual Review of Phytopathology 49:291–315.
   PubMed Web of Science ®Google Scholar
• Porras-Alfaro A, Herrera J, Natvig DO, Lipinski K, Sinsabaugh RL. 2011. Diversity and distribution of soil fungal communities in a semiarid grassland. Mycologia 103:10–21.
   PubMed Web of Science ®Google Scholar
• Porras-Alfaro A, Herrera J, Sinsabaugh RL, Odenbach KJ, Lowrey T, Natvig DO. 2008. Novel root fungal consortium associated with a dominant desert grass. Applied and Environmental Microbiology 74: 2805–2813.Porras-Alfaro A, Liu KL, Kuske CR, Xie G. 2014. From genus to phylum: large-subunit and internal transcribed spacer rRNA operon regions show similar classification accuracies influenced by database composition. Applied and Environmental Microbiology 80:829–840.
   Google Scholar
• Porras-Alfaro A, Nninga-Muniania C, Hamm PS, Torres-Cruz TJ, Kuske CL. 2017. Fungal Diversity and Function in Desert Ecosystems. In: Steven B, ed. The biology of arid soils. Berlin, Germany: De Gruyter. p. 97–115
   Google Scholar
• Powell AJ, Parchert KJ, Bustamante JM, Ricken JB, Hutchinson MI, Natvig DO. 2012. Thermophilic fungi in an aridland ecosystem. Mycologia 104:813–825
   PubMed Web of Science ®Google Scholar
• R Core Team. 2015. R: a language and environment for statistical computing. [cited 2021 Feb 16]. Available from:  https://www.R-project.org
   Google Scholar
• Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM. 2002. Thermotolerance generated by plant/fungal symbiosis. Science 298:1581.
   PubMed Web of Science ®Google Scholar
• Rehner SA, Samuels GJ. 1994. Taxonomy and phylogeny of Gliocladium analysed from nuclear large subunit ribosomal DNA sequences. Mycological Research 98:625–634.
   Web of Science ®Google Scholar
• Ruibal C, Platas G, Bills GF. 2005. Isolation and characterization of melanized fungi from limestone formations in Mallorca. Mycological Progress 4:23–38.
   Google Scholar
• Schade JD, Hobbie SE. 2005. Spatial and temporal variation in islands of fertility in the Sonoran Desert. Biogeochemistry 73:541–553.
   Web of Science ®Google Scholar
• Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Bolchacova E, Voigt K, Crous PW, Miller AN. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences of the United States of America 109:6241–6246.
   Google Scholar
• Seifert KA. 2009. Progress towards DNA barcoding of fungi. Molecular Ecology Resources 9:83–89.
   PubMed Web of Science ®Google Scholar
• States JS, Christensen M. 2001. Fungi associated with biological soil crusts in desert grasslands of Utah and Wyoming. Mycologia 93:432–439.
   Web of Science ®Google Scholar
• Sterflinger K, Tesei D, Zakharova K. 2012. Fungi in hot and cold deserts with particular reference to microcolonial fungi. Fungal Ecology 5:453–462.
   Web of Science ®Google Scholar
• Steven B, Gallegos-Graves LV, Belnap J, Kuske CR. 2013. Dryland soil microbial communities display spatial biogeographic patterns associated with soil depth and soil parent material. FEMS Microbiology Ecology 86:101–113.
   PubMed Web of Science ®Google Scholar
• Steven B, Gallegos-Graves LV, Yeager C, Belnap J, Kuske CR. 2014. Common and distinguishing features of the bacterial and fungal communities in biological soil crusts and shrub root zone soils. Soil Biology and Biochemistry 69:302–312.
   Web of Science ®Google Scholar
• Steven B, Hesse C, Gallegos-Graves LV, Belnap J, Kuske CR. 2015. Fungal diversity in biological soil crusts of the Colorado Plateau. In: Ralston BE, ed. Proceedings of the 12th Biennial Conference of Research on the Colorado Plateau, Flagstaff, Arizona, 2013 Sep 16–19. Boulder, Colorado: US Geological Survey. p. 2015–5180.
   Google Scholar
• Vargas-Gastélum L, Romero-Olivares AL, Escalante AE, Rocha-Olivares A, Brizuela C, Riquelme M. 2015. Impact of seasonal changes on fungal diversity of a semi-arid ecosystem revealed by 454 pyrosequencing. FEMS Microbiology Ecology 91:44–56.
   Web of Science ®Google Scholar
• Vilgalys R, Hester M. 1990. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172:4238–4246.
   PubMed Web of Science ®Google Scholar
• Weber B, Büdel B, Belnap J. 2016. Biological soil crusts: an organizing principle in drylands. Ecological Studies Book 226. Cham, Switzerland: Springer. 549 p.
   Google Scholar
• Wehner J, Powell JR, Muller LA, Caruso T Veresoglou SD, Hempel SRillig 2014. Determinants of root‐associated fungal communities within Asteraceae in a semi‐arid grassland. Journal of Ecology 102:425–436.
   Google Scholar
• White TJ, Bruns TD, Lee SB, Taylor JW. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Inns AM, Gelfand DH, Sninsky JJ, White TJ. PCR protocols: a guide to methods and applications. New York: Academic Press. p. 315–324.
   Google Scholar
• Zhang T, Wei XL, Zhang YQ, Liu HY, Yu LY. 2014. Diversity and distribution of lichen-associated fungi in the Ny-Ålesund Region (Svalbard, High Arctic) as revealed by 454 pyrosequencing. Scientific Reports 5:14850–14859.
   Web of Science ®Google Scholar
• Zhuang W, Downing A, Zhang Y. 2015. The influence of biological soil crusts on 15N translocation in soil and vascular plant in a temperate desert of Northwestern China. Journal of Plant Ecology 8:420–428.
   Web of Science ®Google Scholar