Abstract
Global N inputs and atmospheric CO2 concentrations have increased as a result of human activities, and are predicted to increase along with population growth, with potentially negative effects on biodiversity. Using taxonomic and phylogenetic measures, we examined the response of arbuscular mycorrhizal fungi (AMF) to experimental manipulations of N and CO2 at the Jasper Ridge Global Change Experiment. No significant interactions between N and CO2 were observed, but individual effects of N and CO2 were found. Elevated CO2 resulted in changes in phylogenetic similarity, and a shift to phylogenetic clustering of AMF communities. N addition resulted in higher phylogenetic diversity and evenness, with no shifts in community composition and no significant signal for phylogenetic clustering. N addition resulted in an increase in both available N and the N:P ratio in N-amended plots, which suggests that changing patterns of nutrient limitation could have lead to altered species interactions. These findings suggest that elevated levels of N and CO2 altered patterns of AMF community assembly, with potential effects on ecosystem function.
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References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Bever JD, Richardson SC, Lawrence BM et al (2009) Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol Lett 12:13–21. doi:10.1111/j.1461-0248.2008.01254.x
Bryant JA, Lamanna C, Morlon HLN et al (2008) Colloquium paper: microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci USA 105(Suppl 1):11505–11511. doi:10.1073/pnas.0801920105
Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715. doi:10.1111/j.1461-0248.2009.01314.x
Davison J, Fierer N, Opik M et al (2012) Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS One 7:e41938. doi:10.1371/journal.pone.0041938.s005
Dumbrell AJ, Nelson M, Helgason T et al (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345. doi:10.1038/ismej.2009.122
Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:113. doi:10.1186/1471-2105-5-113
Egerton-Warburton LM, Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol Appl 10:484–496
Egerton-Warburton LM, Graham RCR, Allen EBE, Allen MFM (2001) Reconstruction of the historical changes in mycorrhizal fungal communities under anthropogenic nitrogen deposition. Proc R Soc B Biol Sci 268:2479–2484. doi:10.1098/rspb.2001.1844
Egerton-Warburton LM, Johnson NC, Allen EB (2007) Mycorrhizal community dynamics following nitrogen fertilization: a cross-site test in five grasslands. Ecol Monogr 77:527–544
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. doi:10.1016/0006-3207(92)91201-3
Fellbaum CR, Gachomo EW, Beesetty Y et al (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 109:2666–2671. doi:10.1073/pnas.1118650109
Garcia MO, Garcia MO, Ovasapyan T et al (2008) Mycorrhizal dynamics under elevated CO2 and nitrogen fertilization in a warm temperate forest. Plant Soil 303:301–310. doi:10.1007/s11104-007-9509-9
Gutknecht JLM, Field CB, Balser TC (2012) Microbial communities and their responses to simulated global change fluctuate greatly over multiple years. Glob Change Biol 18:2256–2269. doi:10.1111/j.1365-2486.2012.02686.x
Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344
Hart MM, Reader RJ, Klironomos JN (2003) Plant coexistence mediated by arbuscular mycorrhizal fungi. Trends Ecol Evol 18:418–423
Helmus MR, Bland TJ, Williams CK, Ives AR (2007) Phylogenetic measures of biodiversity. Am Nat 169:E68–E83. doi:10.1086/511334
Hooper DU, Chapin FS III, Ewel JJ et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35
Horn S, Caruso T, Verbruggen E et al (2014) Arbuscular mycorrhizal fungal communities are phylogenetically clustered at small scales. ISME J 8:2231–2242. doi:10.1038/ismej.2014.72
Horner-Devine MC, Bohannan BJM (2006) Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87:S100–S108. doi:10.1890/0012-9658(2006)87[100:PCAOIB]2.0.CO;2
Hughes JB, Hellmann JJ (2005) The application of rarefaction techniques to molecular inventories of microbial diversity. Meth Enzymol 397:292–308. doi:10.1016/S0076-6879(05)97017-1
Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789. doi:10.1111/j.1469-8137.2007.02294.x
Johnson NC (2009) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647. doi:10.1111/j.1469-8137.2009.03110.x
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–585. doi:10.1046/j.1469-8137.1997.00729.x
Johnson NC, Rowland D, Corkidi L et al (2003) Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84:1895–1908
Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. doi:10.1093/bioinformatics/btq166
Kim Y-C, Gao C, Zheng Y et al (2014) Arbuscular mycorrhizal fungal community response to warming and nitrogen addition in a semiarid steppe ecosystem. Mycorrhiza. doi:10.1007/s00572-014-0608-1
Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303. doi:10.1016/j.soilbio.2011.07.012
Klironomos JN, Ursic M, Rillig M (1998) Interspecific differences in the response of arbuscular mycorrhizal fungi to Artemisia tridentata grown under elevated atmospheric CO5. New Phytol 138:599–605
Koch AM, Croll D, Sanders IR (2006) Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecol Lett 9:103–110. doi:10.1111/j.1461-0248.2005.00853.x
Krüger M, Krüger C, Walker C et al (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984. doi:10.1111/j.1469-8137.2011.03962.x
Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349. doi:10.1111/j.1574-6941.2008.00531.x
Liu Y, Mao L, Li J et al (2014) Resource availability differentially drives community assemblages of plants and their root-associated arbuscular mycorrhizal fungi. Plant Soil 386:341–355. doi:10.1007/s11104-014-2261-z
Loreau M, Naeem S, Inchausti P et al (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808. doi:10.1126/science.1064088
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. doi:10.1128/AEM.71.12.8228-8235.2005
Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748. doi:10.1126/science.1143082
Maherali H, Klironomos JN (2012) Phylogenetic and trait-based assembly of arbuscular mycorrhizal fungal communities. PLoS One 7:e36695. doi:10.1371/journal.pone.0036695.g004
McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. doi:10.1371/journal.pone.0061217
Menge DNL, Field CB (2007) Simulated global changes alter phosphorus demand in annual grassland. Glob Change Biol 13:2582–2591. doi:10.1111/j.1365-2486.2007.01456.x
Moora M, Davison J, Opik M et al (2014) Anthropogenic land use shapes the composition and phylogenetic structure of soil arbuscular mycorrhizal fungal communities. FEMS Microbiol Ecol. doi:10.1111/1574-6941.12420
Munkvold L, Kjøller R, Vestberg M et al (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364. doi:10.1111/j.1469-8137.2004.01169.x
Oksanen J, Blanchet FG, Kindt R et al (2013) vegan: community ecology package. Community ecology
Pennings SC, Clark CM, Cleland EE et al (2005) Do individual plant species show predictable responses to nitrogen addition across multiple experiments? Oikos 110:547–555
Phoenix GK, Emmett BA, Britton AJ et al (2011) Impacts of atmospheric nitrogen deposition: responses of multiple plant and soil parameters across contrasting ecosystems in long-term field experiments. Glob Change Biol 18:1197–1215. doi:10.1111/j.1365-2486.2011.02590.x
Porras-Alfaro A, Herrera J, Natvig DO, Sinsabaugh RL (2007) Effect of long-term nitrogen fertilization on mycorrhizal fungi associated with a dominant grass in a semiarid grassland. Plant Soil 296:65–75. doi:10.1007/s11104-007-9290-9
Poulin R (1998) Comparison of three estimators of species richness in parasite component communities. J Parasitol 84:485–490
Powell JR, Parrent JL, Hart MM et al (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc R Soc B Biol Sci 276:4237–4245. doi:10.1098/rspb.2009.1015
Redecker D, Morton JB, Bruns TD (2000) Ancestral lineages of arbuscular mycorrhizal fungi (Glomales). Mol Phylogenet Evol 14:276–284. doi:10.1006/mpev.1999.0713
Rillig MC, Hernandez GY, Newton P (2000) Arbuscular mycorrhizae respond to elevated atmospheric CO2 after long-term exposure: evidence from a CO2 spring in New Zealand supports the resource balance model. Ecol Lett 3:475–478
Ronquist F, Teslenko M, van der Mark P et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029
Saks Ü, Davison J, Opik M et al (2013) Root-colonizing and soil-borne communities of arbuscular mycorrhizal fungi in a temperate forest understorey. Botany 92:277–285. doi:10.1139/cjb-2013-0058
Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM.01541-09
Smith R (2008) Arbuscular mycorrhizas. In: Smith SE, Read DJ (eds) Mycorrhizal Symbiosis. Academic Press, Cambridge, UK
Staddon PL, Fitter AH (1998) Does elevated atmospheric carbon dioxide affect arbuscular mycorrhizas? Trends Ecol Evol 13:455–458. doi:10.1016/S0169-5347(98)01493-1
Tedersoo L, Nilsson RH, Abarenkov K et al (2010) 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol 188:291–301
Thonar C, Schnepf A, Frossard E et al (2010) Traits related to differences in function among three arbuscular mycorrhizal fungi. Plant Soil 339:231–245. doi:10.1007/s11104-010-0571-3
Treseder KK (2004) A meta-analysis of mycorrhizal responses to N, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355. doi:10.1111/j.1469-8137.2004.01159.x
Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120. doi:10.1111/j.1461-0248.2008.01230.x
Treseder KK, Allen MF (2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol 147:189–200
Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:946–954
Treseder KK, Egerton-Warburton LM, Allen MF et al (2003) Alteration of soil carbon pools and communities of mycorrhizal fungi in chaparral exposed to elevated carbon dioxide. Ecosystems 6:786–796. doi:10.1007/s10021-003-0182-4
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363. doi:10.1111/j.1461-0248.2008.01250.x
van der Heijden MGA, Scheublin TR (2007) Functional traits in mycorrhizal ecology: their use for predicting the impact of arbuscular mycorrhizal fungal communities on plant growth and ecosystem functioning. New Phytol 174:244–250. doi:10.1111/j.1469-8137.2007.02041.x
van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091. doi:10.1890/0012-9658(1998)079[2082:DAMFSA]2.0.CO;2
van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. doi:10.1111/j.1461-0248.2007.01139.x
van Diepen LTA, Lilleskov EA, Pregitzer KS, Miller RM (2010) Simulated nitrogen deposition causes a decline of intra- and extraradical abundance of arbuscular mycorrhizal fungi and changes in microbial community structure in northern hardwood forests. Ecosystems 13:683–695. doi:10.1007/s10021-010-9347-0
van Diepen LTA, Lilleskov EA, Pregitzer KS (2011) Simulated nitrogen deposition affects community structure of arbuscular mycorrhizal fungi in northern hardwood forests. Mol Ecol 20:799–811. doi:10.1111/j.1365-294X.2010.04969.x
van Diepen LTA, Entwistle EM, Zak DR (2013) Chronic nitrogen deposition and the composition of active arbuscular mycorrhizal fungi. Applied Soil Ecol 72:62–68. doi:10.1016/j.apsoil.2013.05.012
Waldrop MP, Zak DR, Blackwood CB et al (2006) Resource availability controls fungal diversity across a plant diversity gradient. Ecol Lett 9:1127–1135. doi:10.1111/j.1461-0248.2006.00965.x
Webb CO (2000) Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat 156:145–155. doi:10.1086/303378
Zavaleta ES (2003) Additive effects of simulated climate changes, elevated CO2, and nitrogen deposition on grassland diversity. Proc Natl Acad Sci 100:7650–7654. doi:10.1073/pnas.0932734100
Acknowledgments
We thank Nona Chiariello and Chris Field for coordinating field sampling, Kathryn Docherty and Evan Jones for laboratory support, Will Truce for help in field collections and Jessica Gutknecht for sharing PLFA data. This work was funded by a Doctoral Dissertation Improvement grant (National Science Foundation DEB-0910374). The funding agency had no role in the design or execution of this research.
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Communicated by Maria J. Pozo.
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Mueller, R.C., Bohannan, B.J.M. Shifts in the phylogenetic structure of arbuscular mycorrhizal fungi in response to experimental nitrogen and carbon dioxide additions. Oecologia 179, 175–185 (2015). https://doi.org/10.1007/s00442-015-3337-z
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DOI: https://doi.org/10.1007/s00442-015-3337-z