View Item 

Show simple item record

Anthropogenic N deposition alters soil organic matter biochemistry and microbial communities on decaying fine roots
dc.contributor.authorArgiroff, William A.
dc.contributor.authorZak, Donald R.
dc.contributor.authorUpchurch, Rima A.
dc.contributor.authorSalley, Sydney O.
dc.contributor.authorGrandy, A. Stuart
dc.date.accessioned2019-11-12T16:20:51Z
dc.date.availableWITHHELD_14_MONTHS
dc.date.available2019-11-12T16:20:51Z
dc.date.issued2019-12
dc.identifier.citationArgiroff, William A.; Zak, Donald R.; Upchurch, Rima A.; Salley, Sydney O.; Grandy, A. Stuart (2019). "Anthropogenic N deposition alters soil organic matter biochemistry and microbial communities on decaying fine roots." Global Change Biology 25(12): 4369-4382.
dc.identifier.issn1354-1013
dc.identifier.issn1365-2486
dc.identifier.urihttps://hdl.handle.net/2027.42/151954
dc.description.abstractFine root litter is a primary source of soil organic matter (SOM), which is a globally important pool of C that is responsive to climate change. We previously established that ~20 years of experimental nitrogen (N) deposition has slowed fine root decay and increased the storage of soil carbon (C; +18%) across a widespread northern hardwood forest ecosystem. However, the microbial mechanisms that have directly slowed fine root decay are unknown. Here, we show that experimental N deposition has decreased the relative abundance of Agaricales fungi (−31%) and increased that of partially ligninolytic Actinobacteria (+24%) on decaying fine roots. Moreover, experimental N deposition has increased the relative abundance of lignin‐derived compounds residing in SOM (+53%), and this biochemical response is significantly related to shifts in both fungal and bacterial community composition. Specifically, the accumulation of lignin‐derived compounds in SOM is negatively related to the relative abundance of ligninolytic Mycena and Kuehneromyces fungi, and positively related to Microbacteriaceae. Our findings suggest that by altering the composition of microbial communities on decaying fine roots such that their capacity for lignin degradation is reduced, experimental N deposition has slowed fine root litter decay, and increased the contribution of lignin‐derived compounds from fine roots to SOM. The microbial responses we observed may explain widespread findings that anthropogenic N deposition increases soil C storage in terrestrial ecosystems. More broadly, our findings directly link composition to function in soil microbial communities, and implicate compositional shifts in mediating biogeochemical processes of global significance.Experimental nitrogen deposition (ca. 20 years) has slowed fine root decay and increased soil carbon across a widespread northern hardwood forest ecosystem, but the microbial mechanisms underlying this response are unknown. Here, we show that experimental N deposition has reduced the relative abundance of ligninolytic fungi and increased that of bacteria with weaker ligninolytic capacity on decaying fine root litter. These responses are correlated with an accumulation of lignin‐derived compounds in soil organic matter, of which fine root litter is the primary source. Thus, anthropogenic nitrogen deposition may enhance terrestrial carbon storage by altering microbial community composition on decaying fine roots.
dc.publisherElsevier
dc.publisherWiley Periodicals, Inc.
dc.subject.otherbacterial community
dc.subject.othersoil carbon
dc.subject.otherbiogeochemical feedback
dc.subject.otherroot decay
dc.subject.othermicrobial decomposition
dc.subject.otherlignin
dc.subject.otherfungal community
dc.titleAnthropogenic N deposition alters soil organic matter biochemistry and microbial communities on decaying fine roots
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelGeology and Earth Sciences
dc.subject.hlbsecondlevelEcology and Evolutionary Biology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/151954/1/gcb14770.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/151954/2/gcb14770_am.pdf
dc.identifier.doi10.1111/gcb.14770
dc.identifier.sourceGlobal Change Biology
dc.identifier.citedreferenceSchloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., … Weber, C. F. ( 2009 ). Introducing mothur: Open‐source, platform‐independent, community‐supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75 ( 23 ), 7537 – 7541. https://doi.org/10.1128/AEM.01541-09
dc.identifier.citedreferenceSchimel, J. P., & Schaeffer, S. M. ( 2012 ). Microbial control over carbon cycling in soil. Frontiers in Microbiology, 3, 1 – 11. https://doi.org/10.3389/fmicb.2012.00348
dc.identifier.citedreferenceSchlesinger, W. H., & Bernhardt, E. S. ( 2013 ). The carbon cycle of terrestrial ecosystems. In Biogeochemistry: An analysis of global change ( 3rd ed., pp. 135 – 172 ). New York, NY: Academic Press.
dc.identifier.citedreferenceSilver, W. L., & Miya, R. K. ( 2001 ). Global patterns in root decomposition: Comparisons of climate and litter quality effects. Oecologia, 129 ( 3 ), 407 – 419. https://doi.org/10.1007/s004420100740
dc.identifier.citedreferenceSun, T., Dong, L., Wang, Z., Lü, X., & Mao, Z. ( 2016 ). Effects of long‐term nitrogen deposition on fine root decomposition and its extracellular enzyme activities in temperate forests. Soil Biology and Biochemistry, 93, 50 – 59. https://doi.org/10.1016/j.soilbio.2015.10.023
dc.identifier.citedreferenceSun, T., Hobbie, S. E., Berg, B., Zhang, H., Wang, Q., Wang, Z., & Hättenschwiler, S. ( 2018 ). Contrasting dynamics and trait controls in first‐order root compared with leaf litter decomposition. Proceedings of the National Academy of Sciences of the United States of America, 115 ( 41 ), 10392 – 10397. https://doi.org/10.1073/pnas.1716595115
dc.identifier.citedreferenceTalbot, J. M., & Treseder, K. K. ( 2012 ). Interactions between lignin, cellulose, and nitrogen drive litter chemistry–decay relationships. Ecology, 93 ( 2 ), 345 – 354. https://doi.org/10.1890/11-0843.1
dc.identifier.citedreferenceTaylor, C. R., Hardiman, E. M., Ahmad, M., Sainsbury, P. D., Norris, P. R., & Bugg, T. D. H. ( 2012 ). Isolation of bacterial strains able to metabolize lignin from screening of environmental samples. Journal of Applied Microbiology, 113 ( 3 ), 521 – 530. https://doi.org/10.1111/j.1365-2672.2012.05352.x
dc.identifier.citedreferenceTeixeira, M. M., Moreno, L. F., Stielow, B. J., Muszewska, A., Hainaut, M., Gonzaga, L., … de Hoog, G. S. ( 2017 ). Exploring the genomic diversity of black yeasts and relatives (Chaetothyriales, Ascomycota). Studies in Mycology, 86, 1 – 28. https://doi.org/10.1016/j.simyco.2017.01.001
dc.identifier.citedreferenceThomas, D. C., Zak, D. R., & Filley, T. R. ( 2012 ). Chronic N deposition does not apparently alter the biochemical composition of forest floor and soil organic matter. Soil Biology and Biochemistry, 54, 7 – 13. https://doi.org/10.1016/j.soilbio.2012.05.010
dc.identifier.citedreferenceTravers, K. J., Chin, C. S., Rank, D. R., Eid, J. S., & Turner, S. W. ( 2010 ). A flexible and efficient template format for circular consensus sequencing and SNP detection. Nucleic Acids Research, 38 ( 15 ), e159. https://doi.org/10.1093/nar/gkq543
dc.identifier.citedreferenceTreseder, K. K., Balser, T. C., Bradford, M. A., Brodie, E. L., Dubinsky, E. A., Eviner, V. T., … Waldrop, M. P. ( 2012 ). Integrating microbial ecology into ecosystem models: Challenges and priorities. Biogeochemistry, 109 ( 1–3 ), 7 – 18. https://doi.org/10.1007/s10533-011-9636-5
dc.identifier.citedreferencevan den Enden, L., Frey, S. D., Nadelhoffer, K. J., LeMoine, J. M., Lajtha, K., & Simpson, M. J. ( 2018 ). Molecular‐level changes in soil organic matter composition after 10 years of litter, root and nitrogen manipulation in a temperate forest. Biogeochemistry, 141 ( 2 ), 183 – 197. https://doi.org/10.1007/s10533-018-0512-4
dc.identifier.citedreferenceVilgalys, R., & Hester, M. ( 1990 ). Rapid genetic identification and mapping of several Cryptococcus species. Journal of Bacteriology, 172 ( 8 ), 4238 – 4246. https://doi.org/10.1128/JB.172.8.4238-4246.1990
dc.identifier.citedreferenceVoriskova, J., & Baldrian, P. ( 2013 ). Fungal community on decomposing leaf litter undergoes rapid successional changes. ISME Journal, 7 ( 3 ), 477 – 486. https://doi.org/10.1038/ismej.2012.116
dc.identifier.citedreferenceWaldrop, M. P., Zak, D. R. Z., Sinsabaugh, R. L. S., Gallo, M. G. E., & Lauber, C. ( 2004 ). Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecological Applications, 14 ( 4 ), 1172 – 1177. https://doi.org/10.1890/03-5120
dc.identifier.citedreferenceWang, J.‐J., Bowden, R. D., Lajtha, K., Washko, S. E., Wurzbacher, S. J., & Simpson, M. J. ( 2019 ). Long‐term nitrogen addition suppresses microbial degradation, enhances soil carbon storage, and alters the molecular composition of soil organic matter. Biogeochemistry, 4, 299 – 313. https://doi.org/10.1007/s10533-018-00535-4
dc.identifier.citedreferenceWang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. ( 2007 ). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73 ( 16 ), 5261 – 5267. https://doi.org/10.1128/AEM.00062-07
dc.identifier.citedreferenceWhalen, E. D., Smith, R. G., Grandy, A. S., & Frey, S. D. ( 2018 ). Manganese limitation as a mechanism for reduced decomposition in soils under atmospheric nitrogen deposition. Soil Biology and Biochemistry, 127, 252 – 263. https://doi.org/10.1016/J.SOILBIO.2018.09.025
dc.identifier.citedreferenceWickham, H. ( 2017 ). tidyverse: Easily install and load the “Tidyverse”. R package version 1.2.1. https://CRAN.R-project.org/package=tidyverse
dc.identifier.citedreferenceWickings, K., Grandy, A. S., Reed, S., & Cleveland, C. ( 2011 ). Management intensity alters decomposition via biological pathways. Biogeochemistry, 104 ( 1–3 ), 365 – 379. https://doi.org/10.1007/s10533-010-9510-x
dc.identifier.citedreferenceWilhelm, R. C., Singh, R., Eltis, L. D., & Mohn, W. W. ( 2018 ). Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing. ISME Journal, 13 ( 2 ), 413 – 429. https://doi.org/10.1038/s41396-018-0279-6
dc.identifier.citedreferenceXia, M., Guo, D., & Pregitzer, K. S. ( 2010 ). Ephemeral root modules in Fraxinus mandshurica. New Phytologist, 188 ( 4 ), 1065 – 1074. https://doi.org/10.1111/j.1469-8137.2010.03423.x
dc.identifier.citedreferenceXia, M., Talhelm, A. F., & Pregitzer, K. S. ( 2015 ). Fine roots are the dominant source of recalcitrant plant litter in sugar maple‐dominated northern hardwood forests. New Phytologist, 208 ( 3 ), 715 – 726. https://doi.org/10.1111/nph.13494
dc.identifier.citedreferenceXia, M., Talhelm, A. F., & Pregitzer, K. S. ( 2017 ). Chronic nitrogen deposition influences the chemical dynamics of leaf litter and fine roots during decomposition. Soil Biology and Biochemistry, 112, 24 – 34. https://doi.org/10.1016/j.soilbio.2017.04.011
dc.identifier.citedreferenceXia, M., Talhelm, A. F., & Pregitzer, K. S. ( 2018 ). Long‐term simulated atmospheric nitrogen deposition alters leaf and fine root decomposition. Ecosystems, 21 ( 1 ), 1 – 14. https://doi.org/10.1007/s10021-017-0130-3
dc.identifier.citedreferenceZak, D. R., Argiroff, W. A., Freedman, Z. B., Upchurch, R. A., Entwistle, E. M., & Romanowicz, K. J. ( 2019 ). Anthropogenic N deposition, fungal gene expression, and an increasing soil carbon sink in the Northern Hemisphere. Ecology, e02804. https://doi.org/10.1002/ecy.2804
dc.identifier.citedreferenceZak, D. R., Freedman, Z. B., Upchurch, R. A., Steffens, M., & Kögel‐Knabner, I. ( 2017 ). Anthropogenic N deposition increases soil organic matter accumulation without altering its biochemical composition. Global Change Biology, 23 ( 2 ), 933 – 944. https://doi.org/10.1111/gcb.13480
dc.identifier.citedreferenceZak, D. R., Holmes, W. E., Burton, A. J., Pregitzer, K. S., & Talhelm, A. F. ( 2008 ). Simulated atmospheric NO 3 − deposition increases organic matter by slowing decomposition. Ecological Applications, 18 ( 8 ), 2016 – 2027. https://doi.org/10.1890/07-1743.1
dc.identifier.citedreferenceAhmad, M., Taylor, C. R., Pink, D., Burton, K., Eastwood, D., Bending, G. D., & Bugg, T. D. H. ( 2010 ). Development of novel assays for lignin degradation: Comparative analysis of bacterial and fungal lignin degraders. Molecular BioSystems, 6 ( 5 ), 815 – 821. https://doi.org/10.1039/b908966g
dc.identifier.citedreferenceAllison, S. D. ( 2012 ). A trait‐based approach for modelling microbial litter decomposition. Ecology Letters, 15 ( 9 ), 1058 – 1070. https://doi.org/10.1111/j.1461-0248.2012.01807.x
dc.identifier.citedreferenceAnderson, M. J. ( 2001 ). A new method for non‐parametric multivariate analysis of variance. Austral Ecology, 26, 32 – 46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
dc.identifier.citedreferenceAnderson, M. J. ( 2004 ). PERMDISP: A FORTRAN computer program for permutational analysis of multivariate dispersions (for any two‐factor ANOVA design) using permutation tests.
dc.identifier.citedreferenceAssavanig, A., Amornikitticharoen, B., Ekpaisal, N., Meevootisom, V., & Flegel, T. W. ( 1992 ). Isolation, characterization and function of laccase from Trichoderma. Applied Microbiology and Biotechnology, 38 ( 2 ), 198 – 202. https://doi.org/10.1007/BF00174468
dc.identifier.citedreferenceAverill, C., & Waring, B. ( 2018 ). Nitrogen limitation of decomposition and decay: How can it occur? Global Change Biology, 24 ( 4 ), 1417 – 1427. https://doi.org/10.1111/gcb.13980
dc.identifier.citedreferenceBaldrian, P. ( 2008 ). Enzymes of saprotrophic basidiomycetes. In L. Boddy, J. Frankland, & P. Van West (Eds.), Ecology of saprotrophic basidiomycetes. British Mycological Symposia Series (Vol. 28, pp. 19 – 41 ). New York, NY: Elsevier. https://doi.org/10.1016/S0275-0287(08)80004-5
dc.identifier.citedreferenceBarnes, B. V., Zak, D. R., Denton, S. R., & Spurr, S. H. ( 1998 ). Nutrient cycling. In E. Schatz, S. Russell, & E. Starr (Eds.), Forest ecology ( 4th ed., pp. 524 – 576 ). New York, NY: John Wiley & Sons Inc.
dc.identifier.citedreferenceBatjes, N. H. ( 1996 ). Total carbon and nitrogen in the soils of the world. European Journal of Soil Science, 47 ( 2 ), 151 – 163. https://doi.org/10.1111/ejss.12114_2
dc.identifier.citedreferenceBerg, B. ( 2014 ). Decomposition patterns for foliar litter – A theory for influencing factors. Soil Biology and Biochemistry, 78, 222 – 232. https://doi.org/10.1016/j.soilbio.2014.08.005
dc.identifier.citedreferenceBugg, T. D. H., Ahmad, M., Hardiman, E. M., & Singh, R. ( 2011 ). The emerging role for bacteria in lignin degradation and bio‐product formation. Current Opinion in Biotechnology, 22 ( 3 ), 394 – 400. https://doi.org/10.1016/j.copbio.2010.10.009
dc.identifier.citedreferenceBurton, A. J., Pregitzer, K. S., Crawford, J. N., Zogg, G. P., & Zak, D. R. ( 2004 ). Simulated chronic NO 3 − deposition reduces soil respiration in northern hardwood forests. Global Change Biology, 10 ( 7 ), 1080 – 1091. https://doi.org/10.1111/j.1365-2486.2004.00737.x
dc.identifier.citedreferenceBurton, A. J., Ramm, C. W., Pregitzer, K. S., & Reed, D. D. ( 1991 ). Use of multivariate methods in forest research site selection. Canadian Journal of Forest Research, 21, 1573 – 1580. https://doi.org/10.1139/x91-219
dc.identifier.citedreferenceChen, J., Luo, Y., Jan van Groenigen, K., Hungate, B. A., Cao, J., Zhou, X., & Wang, R. ( 2018 ). A keystone microbial enzyme for nitrogen control of soil carbon storage. Science Advances, 4 ( 8 ), 2 – 8. https://doi.org/10.1126/sciadv.aaq1689
dc.identifier.citedreferenceCole, J. R., Wang, Q., Fish, J. A., Chai, B., McGarrell, D. M., Sun, Y., … Tiedje, J. M. ( 2014 ). Ribosomal database project: Data and tools for high throughput rRNA analysis. Nucleic Acids Research, 42 ( D1 ), 633 – 642. https://doi.org/10.1093/nar/gkt1244
dc.identifier.citedreferenceCotrufo, M. F., Soong, J. L., Horton, A. J., Campbell, E. E., Haddix, M. L., Wall, D. H., & Parton, W. J. ( 2015 ). Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nature Geoscience, 8 ( 10 ), 776 – 779. https://doi.org/10.1038/ngeo2520
dc.identifier.citedreferencede Mendiburu, F. ( 2017 ). Agricolae: Statistical procedures for agricultural research. R package version 1.3-1. https://CRAN.R-project.org/package=agricolae
dc.identifier.citedreferenceDeForest, J. L., Zak, D. R., Pregitzer, K. S., & Burton, A. J. ( 2004 ). Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Science Society of America Journal, 68 ( 1 ), 132. https://doi.org/10.2136/sssaj2004.1320
dc.identifier.citedreferenceEdgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. ( 2011 ). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27 ( 16 ), 2194 – 2200. https://doi.org/10.1093/bioinformatics/btr381
dc.identifier.citedreferenceEisenlord, S. D., Freedman, Z., Zak, D. R., Xue, K., He, Z., & Zhou, J. ( 2013 ). Microbial mechanisms mediating increased soil C storage under elevated atmospheric N deposition. Applied and Environmental Microbiology, 79 ( 4 ), 1191 – 1199. https://doi.org/10.1128/AEM.03156-12
dc.identifier.citedreferenceEisenlord, S. D., & Zak, D. R. ( 2010 ). Simulated atmospheric nitrogen deposition alters actinobacterial community composition in forest soils. Soil Science Society of America Journal, 74 ( 4 ), 1157. https://doi.org/10.2136/sssaj2009.0240
dc.identifier.citedreferenceEntwistle, E. M., Romanowicz, K. J., Argiroff, W. A., Freedman, Z. B., Morris, J. J., & Zak, D. R. ( 2018 ). Anthropogenic N deposition alters the composition of expressed class II fungal peroxidases. Applied and Environmental Microbiology, 84 ( 9 ), e02816 – 17. https://doi.org/10.1128/AEM.02816-17
dc.identifier.citedreferenceEntwistle, E. M., Zak, D. R., & Argiroff, W. A. ( 2018 ). Anthropogenic N deposition increases soil C storage by reducing the relative abundance of lignolytic fungi. Ecological Monographs, 88 ( 2 ), 225 – 244. https://doi.org/10.1002/ecm.1288
dc.identifier.citedreferenceFichot, E. B., & Norman, R. S. ( 2013 ). Microbial phylogenetic profiling with the Pacific Biosciences sequencing platform. Microbiome, 1 ( 1 ), 2 – 6. https://doi.org/10.1186/2049-2618-1-10
dc.identifier.citedreferenceFloudas, D., Binder, M., Riley, R., Barry, K., Blanchette, R. A., Henrissat, B., … Hibbett, D. S. ( 2012 ). The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science, 336 ( 6089 ), 1715 – 1719. https://doi.org/10.1126/science.1221748
dc.identifier.citedreferenceFreedman, Z. B., Upchurch, R. A., Zak, D. R., & Cline, L. C. ( 2016 ). Anthropogenic N deposition slows decay by favoring bacterial metabolism: Insights from metagenomic analyses. Frontiers in Microbiology, 7, 1 – 11. https://doi.org/10.3389/fmicb.2016.00259
dc.identifier.citedreferenceFreedman, Z. B., & Zak, D. R. ( 2014 ). Atmospheric N deposition increases bacterial laccase‐like multicopper oxidases: Implications for organic matter decay. Applied and Environmental Microbiology, 80 ( 14 ), 4460 – 4468. https://doi.org/10.1128/AEM.01224-14
dc.identifier.citedreferenceFreschet, G. T., Cornwell, W. K., Wardle, D. A., Elumeeva, T. G., Liu, W., Jackson, B. G., … Cornelissen, J. H. C. ( 2013 ). Linking litter decomposition of above‐ and below‐ground organs to plant‐soil feedbacks worldwide. Journal of Ecology, 101 ( 4 ), 943 – 952. https://doi.org/10.1111/1365-2745.12092
dc.identifier.citedreferenceFrey, S. D., Ollinger, S., Nadelhoffer, K., Bowden, R., Brzostek, E., Burton, A., … Wickings, K. ( 2014 ). Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests. Biogeochemistry, 121 ( 2 ), 305 – 316. https://doi.org/10.1007/s10533-014-0004-0
dc.identifier.citedreferenceGalloway, J. N., Dentener, F. J., Capone, D. G., Boyer, E. W., Howarth, R. W., Seitzinger, S. P., … Karl, D. M. ( 2004 ). Nitrogen cycles: Past, present, and future. Biogeochemistry, 70 ( 2 ), 153 – 226. https://doi.org/10.1007/s10533-004-0370-0
dc.identifier.citedreferenceGalloway, J. N., Townsend, A. R., Erisman, J. W., Bekunda, M., Cai, Z., Freney, J. R., … Sutton, M. A. ( 2008 ). Transformation of the nitrogen cycle: Recent trends, questions, and potential solutions. Science, 320 ( 5878 ), 889 – 892. https://doi.org/10.1126/science.1136674
dc.identifier.citedreferenceGhosh, A., Frankland, J. C., Thurston, C. F., & Robinson, C. H. ( 2003 ). Enzyme production by Mycena galopus mycelium in artificial media and in Picea sitchensis F1 horizon needle litter. Mycological Research, 107 ( 8 ), 996 – 1008. https://doi.org/10.1017/S0953756203008177
dc.identifier.citedreferenceGrandy, A. S., Neff, J. C., & Weintraub, M. N. ( 2007 ). Carbon structure and enzyme activities in alpine and forest ecosystems. Soil Biology and Biochemistry, 39 ( 11 ), 2701 – 2711. https://doi.org/10.1016/j.soilbio.2007.05.009
dc.identifier.citedreferenceGrandy, A. S., Sinsabaugh, R. L., Neff, J. C., Stursova, M., & Zak, D. R. ( 2008 ). Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions. Biogeochemistry, 91 ( 1 ), 37 – 49. https://doi.org/10.1007/s10533-008-9257-9
dc.identifier.citedreferenceGrandy, A. S., Strickland, M. S., Lauber, C. L., Bradford, M. A., & Fierer, N. ( 2009 ). The influence of microbial communities, management, and soil texture on soil organic matter chemistry. Geoderma, 150 ( 3–4 ), 278 – 286. https://doi.org/10.1016/j.geoderma.2009.02.007
dc.identifier.citedreferenceGuo, D., Xia, M., Wei, X., Chang, W., Liu, Y., & Wang, Z. ( 2008 ). Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty‐three Chinese temperate tree species. New Phytologist, 180 ( 3 ), 673 – 683. https://doi.org/10.1111/j.1469-8137.2008.02573.x
dc.identifier.citedreferenceHassett, J. E., Zak, D. R., Blackwood, C. B., & Pregitzer, K. S. ( 2009 ). Are basidiomycete laccase gene abundance and composition related to reduced lignolytic activity under elevated atmospheric NO 3 − deposition in a northern hardwood forest? Microbial Ecology, 57 ( 4 ), 728 – 739. https://doi.org/10.1007/s00248-008-9440-5
dc.identifier.citedreferenceHawkes, C. V., & Keitt, T. H. ( 2015 ). Resilience vs. historical contingency in microbial responses to environmental change. Ecology Letters, 18 ( 7 ), 612 – 625. https://doi.org/10.1111/ele.12451
dc.identifier.citedreferenceHibbett, D. S., Bauer, R., Binder, M., Giachini, A. J., Hosaka, K., Justo, A., … Thorn, R. G. ( 2014 ). Agaricomycetes. In D. J. McLaughlin & J. W. Spatafora (Eds.), The Mycota, vol. 7A: Systematics and evolution ( 2 nd ed., pp. 373 – 429 ). Berlin: Springer Verlag.
dc.identifier.citedreferenceHobbie, S. E. ( 2005 ). Contrasting effects of substrate and fertilizer nitrogen on the early stages of litter decomposition. Ecosystems, 8 ( 6 ), 644 – 656. https://doi.org/10.1007/s10021-003-0110-7
dc.identifier.citedreferenceHobbie, S. E., Oleksyn, J., Eissenstat, D. M., & Reich, P. B. ( 2010 ). Fine root decomposition rates do not mirror those of leaf litter among temperate tree species. Oecologia, 162 ( 2 ), 505 – 513. https://doi.org/10.1007/s00442-009-1479-6
dc.identifier.citedreferenceHofrichter, M. ( 2002 ). Review: Lignin conversion by manganese peroxidase (MnP). Enzyme and Microbial Technology, 30 ( 4 ), 454 – 466. https://doi.org/10.1016/S0141-0229(01)00528-2
dc.identifier.citedreferenceHölker, U., Dohse, J., & Höfer, M. ( 2002 ). Extracellular laccases in ascomycetes Trichoderma atroviride and Trichoderma harzianum. Folia Microbiologica, 47 ( 4 ), 423 – 427. https://doi.org/10.1007/BF02818702
dc.identifier.citedreferenceJackson, R. B., Lajtha, K., Crow, S. E., Hugelius, G., Kramer, M. G., & Piñeiro, G. ( 2017 ). The ecology of soil carbon: Pools, vulnerabilities, and biotic and abiotic controls. Annual Review of Ecology, Evolution, and Systematics, 48 ( 1 ), 419 – 445. https://doi.org/10.1146/annurev-ecolsys-112414-054234
dc.identifier.citedreferenceJanssens, I. A., Dieleman, W., Luyssaert, S., Subke, J.‐A., Reichstein, M., Ceulemans, R., … Law, B. E. ( 2010 ). Reduction of forest soil respiration in response to nitrogen deposition. Nature Geoscience, 3 ( 5 ), 315 – 322. https://doi.org/10.1038/ngeo844
dc.identifier.citedreferenceJanusz, G., Pawlik, A., Sulej, J., Świderska‐Burek, U., Jarosz‐Wilkołazka, A., & Paszczyński, A. ( 2017 ). Lignin degradation: Microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiology Reviews, 41 ( 6 ), 941 – 962. https://doi.org/10.1093/femsre/fux049
dc.identifier.citedreferenceKeenan, T. F., Prentice, I. C., Canadell, J. G., Williams, C. A., Wang, H., Raupach, M. R., & Collatz, G. J. ( 2017 ). Recent pause in the growth rate of atmospheric CO 2 due to enhanced terrestrial carbon uptake. Nature Communications, 7 ( 13428 ), 1. https://doi.org/10.1038/ncomms13428
dc.identifier.citedreferenceKellner, H., Luis, P., Pecyna, M. J., Barbi, F., Kapturska, D., Krüger, D., … Hofrichter, M. ( 2014 ). Widespread occurrence of expressed fungal secretory peroxidases in forest soils. PLoS ONE, 9 ( 4 ), e95557. https://doi.org/10.1371/journal.pone.0095557
dc.identifier.citedreferenceKirk, T. K., & Farrell, R. L. ( 1987 ). Enzymatic “combustion”: The microbial degradation of lignin. Annual Review of Microbiology, 41, 465 – 505. https://doi.org/10.1146/annurev.mi.41.100187.002341
dc.identifier.citedreferenceKohout, P., Charvátová, M., Martina, Š., Ma, T., Tom, M., & Baldrian, P. ( 2018 ). Clearcutting alters decomposition processes and initiates complex restructuring of fungal communities in soil and tree roots. ISME Journal, 12 ( 3 ), 692 – 703. https://doi.org/10.1038/s41396-017-0027-3
dc.identifier.citedreferenceKou, L., Jiang, L., Fu, X., Dai, X., Wang, H., & Li, S. ( 2018 ). Nitrogen deposition increases root production and turnover but slows root decomposition in Pinus elliottii plantations. New Phytologist, 218 ( 4 ), 1450 – 1461. https://doi.org/10.1111/nph.15066
dc.identifier.citedreferenceLane, D. ( 1991 ). 16s/23s rRNA sequencing. In E. Stackebrandt & M. Goodfellow (Eds.), Nucleic acid techniques in bacterial systematics (pp. 115 – 175 ). West Sussex, UK: John Wiley & Sons Inc.
dc.identifier.citedreferenceLehmann, J., & Kleber, M. ( 2015 ). The contentious nature of soil organic matter. Nature, 528 ( 7580 ), 60 – 68. https://doi.org/10.1038/nature16069
dc.identifier.citedreferenceLi, A., Fahey, T. J., Pawlowska, T. E., Fisk, M. C., & Burtis, J. ( 2015 ). Fine root decomposition, nutrient mobilization and fungal communities in a pine forest ecosystem. Soil Biology and Biochemistry, 83, 76 – 83. https://doi.org/10.1016/j.soilbio.2015.01.019
dc.identifier.citedreferenceLiu, K. L., Porras‐Alfaro, A., Kuske, C. R., Eichorst, S. A., & Xie, G. ( 2012 ). Accurate, rapid taxonomic classification of fungal large‐subunit rRNA genes. Applied and Environmental Microbiology, 78 ( 5 ), 1523 – 1533. https://doi.org/10.1128/AEM.06826-11
dc.identifier.citedreferenceLuo, C., Xie, S., Sun, W., Li, X., & Cupples, A. M. ( 2009 ). Identification of a novel toluene‐degrading bacterium from the candidate phylum TM7, as determined by DNA stable isotope probing. Applied and Environmental Microbiology, 75 ( 13 ), 4644 – 4647. https://doi.org/10.1128/AEM.00283-09
dc.identifier.citedreferenceMaaroufi, N. I., Nordin, A., Hasselquist, N. J., Bach, L. H., Palmqvist, K., & Gundale, M. J. ( 2015 ). Anthropogenic nitrogen deposition enhances carbon sequestration in boreal soils. Global Change Biology, 21 ( 8 ), 3169 – 3180. https://doi.org/10.1111/gcb.12904
dc.identifier.citedreferenceMartinez, D., Berka, R. M., Henrissat, B., Saloheimo, M., Arvas, M., Baker, S. E., … Brettin, T. S. ( 2008 ). Genome sequencing and analysis of the biomass‐degrading fungus Trichoderma reesei (syn. Hypocrea jecorina ). Nature Biotechnology, 26 ( 5 ), 553 – 560. https://doi.org/10.1038/nbt1403
dc.identifier.citedreferenceMcCormack, M. L., Dickie, I. A., Eissenstat, D. M., Fahey, T. J., Fernandez, C. W., Guo, D., … Zadworny, M. ( 2015 ). Redefining fine roots improves understanding of below‐ground contributions to terrestrial biosphere processes. New Phytologist, 207 ( 3 ), 505 – 518. https://doi.org/10.1111/nph.13363
dc.identifier.citedreferenceMcMurdie, P. J., & Holmes, S. ( 2013 ). Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE, 8 ( 4 ), e61217. https://doi.org/10.1371/journal.pone.0061217
dc.identifier.citedreferenceMcMurdie, P. J., & Holmes, S. ( 2014 ). Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS Computational Biology, 10 ( 4 ), e1003531. https://doi.org/10.1371/journal.pcbi.1003531
dc.identifier.citedreferenceMiyamoto, T., Igarashi, T., & Takahashi, K. ( 2000 ). Lignin‐degrading ability of litter‐decomposing basidiomycetes from Picea forests of Hokkaido. Mycoscience, 41 ( 2 ), 105 – 110. https://doi.org/10.1007/BF02464317
dc.identifier.citedreferenceMorrison, E. W., Frey, S. D., Sadowsky, J. J., van Diepen, L. T. A., Thomas, W. K., & Pringle, A. ( 2016 ). Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest. Fungal Ecology, 23, 48 – 57. https://doi.org/10.1016/j.funeco.2016.05.011
dc.identifier.citedreferenceMorrison, E. W., Pringle, A., van Diepen, L. T. A., & Frey, S. D. ( 2018 ). Simulated nitrogen deposition favors stress‐tolerant fungi with low potential for decomposition. Soil Biology and Biochemistry, 125, 75 – 85. https://doi.org/10.1016/j.soilbio.2018.06.027
dc.identifier.citedreferenceMueller, R. C., Balasch, M. M., & Kuske, C. R. ( 2014 ). Contrasting soil fungal community responses to experimental nitrogen addition using the large subunit rRNA taxonomic marker and cellobiohydrolase I functional marker. Molecular Ecology, 23 ( 17 ), 4406 – 4417. https://doi.org/10.1111/mec.12858
dc.identifier.citedreferenceOksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., … Wagner, H. ( 2018 ). vegan: Community ecology package. Retrieved from https://cran.r-project.org/package=vegan
dc.identifier.citedreferencePan, Y., Birdsey, R. A., Fang, J., Houghton, R., Kauppi, P. E., Kurz, W. A., … Hayes, D. ( 2011 ). A large and persistent carbon sink in the world’s forests. Science, 333 ( 6045 ), 988 – 993. https://doi.org/10.1126/science.1201609
dc.identifier.citedreferencePhilpott, T. J., Barker, J. S., Prescott, C. E., & Grayston, S. J. ( 2018 ). Limited effects of variable‐retention harvesting on fungal communities decomposing fine roots in coastal temperate rainforests. Applied and Environmental Microbiology, 84 ( 3 ), 1 – 16. https://doi.org/10.1128/AEM.02061-17
dc.identifier.citedreferencePold, G., Grandy, A. S., Melillo, J. M., & DeAngelis, K. M. ( 2017 ). Changes in substrate availability drive carbon cycle response to chronic warming. Soil Biology and Biochemistry, 110, 68 – 78. https://doi.org/10.1016/j.soilbio.2017.03.002
dc.identifier.citedreferencePorter, T. M., & Golding, G. B. ( 2012 ). Factors that affect large subunit ribosomal DNA amplicon sequencing studies of fungal communities: Classification method, primer choice, and error. PLoS ONE, 7 ( 4 ), e35749. https://doi.org/10.1371/journal.pone.0035749
dc.identifier.citedreferencePregitzer, K. S., Burton, A. J., Zak, D. R., & Talhelm, A. F. ( 2008 ). Simulated chronic nitrogen deposition increases carbon storage in Northern Temperate forests. Global Change Biology, 14 ( 1 ), 142 – 153. https://doi.org/10.1111/j.1365-2486.2007.01465.x
dc.identifier.citedreferencePregitzer, K. S., Deforest, J. L., Burton, A. J., Allen, M. F., Ruess, R. W., & Hendrick, R. L. ( 2002 ). Fine root architecture of nine North American trees. Ecological Mono, 72 ( 2 ), 293 – 309. https://doi.org/10.1890/0012-9615(2002)072[0293:FRAONN]2.0.CO;2
dc.identifier.citedreferencePregitzer, K. S., Zak, D. R., Burton, A. J., Ashby, J. A., & Macdonald, N. W. ( 2004 ). Chronic nitrate additions dramatically increase the export of carbon and nitrogen from northern hardwood ecosystems. Biogeochemistry, 68 ( 2 ), 179 – 197. https://doi.org/10.1023/B:BIOG.0000025737.29546.fd
dc.identifier.citedreferenceQuast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., … Glöckner, F. O. ( 2013 ). The SILVA ribosomal RNA gene database project: Improved data processing and web‐based tools. Nucleic Acids Research, 41 ( D1 ), 590 – 596. https://doi.org/10.1093/nar/gks1219
dc.identifier.citedreferenceR Core Team. ( 2018 ). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.r-project.org/
dc.identifier.citedreferenceRasse, D. P., Rumpel, C., & Dignac, M. F. ( 2005 ). Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant and Soil, 269 ( 1–2 ), 341 – 356. https://doi.org/10.1007/s11104-004-0907-y
dc.identifier.citedreferenceRStudio Team. ( 2018 ). RStudio: Integrated development for R. Boston, MA: RStudio, Inc.
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
gcb14770.pdf
Size:
1.112MB
Format:
PDF
View/Open
Name:
gcb14770_am.pdf
Size:
374.3KB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.