Roots Mediate the Effects of Snowpack Decline on Soil Bacteria, Fungi, and Nitrogen Cycling in a Northern Hardwood Forest

Sorensen, Patrick O.; Bhatnagar, Jennifer M.; Christenson, Lynn; Duran, Jorge; Fahey, Timothy; Fisk, Melany C.; Finzi, Adrien C.; Groffman, Peter M.; Morse, Jennifer L.; Templer, Pamela H.

doi:10.3389/fmicb.2019.00926

Title: Roots Mediate the Effects of Snowpack Decline on Soil Bacteria, Fungi, and Nitrogen Cycling in a Northern Hardwood Forest

Journal Article · 30 April 2019 · Frontiers in Microbiology

DOI: https://doi.org/10.3389/fmicb.2019.00926 · OSTI ID:1509922

Sorensen, Patrick O. ^[1]; Bhatnagar, Jennifer M. ^[2]; Christenson, Lynn ^[3]; Duran, Jorge ^[4]; Fahey, Timothy ^[5]; Fisk, Melany C. ^[6]; Finzi, Adrien C. ^[2]; Groffman, Peter M. ^[7]; Morse, Jennifer L. ^[8]; Templer, Pamela H. ^[2]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Boston Univ., MA (United States)
Boston Univ., MA (United States)
Vassar College, Poughkeepsie, NY (United States)
Univ. of Coimbra, Coimbra (Portugal)
Cornell Univ., Ithaca, NY (United States)
Miami Univ., Oxford, OH (United States)
City Univ. (CUNY), NY (United States); Cary Inst. of Ecosystem Studies, Millbrook, NY (United States)
Portland State Univ., Portland, OR (United States)

Rising winter air temperature will reduce snow depth and duration over the next century in northern hardwood forests. Reductions in snow depth may affect soil bacteria and fungi directly, but also affect soil microbes indirectly through effects of snowpack loss on plant roots. We incubated root exclusion and root ingrowth cores across a winter climate-elevation gradient in a northern hardwood forest for 29 months to identify direct (i.e., winter snow-mediated) and indirect (i.e., root-mediated) effects of winter snowpack decline on soil bacterial and fungal communities, as well as on potential nitrification and net N mineralization rates. Both winter snowpack decline and root exclusion increased bacterial richness and phylogenetic diversity. Variation in bacterial community composition was best explained by differences in winter snow depth or soil frost across elevation. Root ingrowth had a positive effect on the relative abundance of several bacterial taxonomic orders (e.g., Acidobacterales and Actinomycetales). Nominally saprotrophic (e.g., Saccharomycetales and Mucorales) or mycorrhizal (e.g., Helotiales, Russalales, Thelephorales) fungal taxonomic orders were also affected by both root ingrowth and snow depth variation. However, when grouped together, the relative abundance of saprotrophic fungi, arbuscular mycorrhizal fungi, and ectomycorrhizal fungi were not affected by root ingrowth or snow depth, suggesting that traits in addition to trophic mode will mediate fungal community responses to snowpack decline in northern hardwood forests. Potential soil nitrification rates were positively related to ammonia-oxidizing bacteria and archaea abundance (e.g., Nitrospirales, Nitrosomondales, Nitrosphaerales). Rates of N mineralization were positively and negatively correlated with ectomycorrhizal and saprotrophic fungi, respectively, and these relationships were mediated by root exclusion. The results from this study suggest that a declining winter snowpack and its effect on plant roots each have direct effects on the diversity and abundance of soil bacteria and fungal communities that interact to determine rates of soil N cycling in northern hardwood forests.

View Journal Article

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); Fundação para Ciência e Tecnologia (FCT)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1509922

Alternate ID(s):: OSTI ID: 1560579

Journal Information:: Frontiers in Microbiology, Vol. 10, Issue APR; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (101)

Intact amino acid uptake by northern hardwood and conifer trees Gallet-Budynek, Anne; Brzostek, Edward; Rodgers, Vikki L. Oecologia, Vol. 160, Issue 1 https://doi.org/10.1007/s00442-009-1284-2	journal	February 2009
Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions Schneider, Thomas; Keiblinger, Katharina M.; Schmid, Emanuel The ISME Journal, Vol. 6, Issue 9 https://doi.org/10.1038/ismej.2012.11	journal	March 2012
FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild Nguyen, Nhu H.; Song, Zewei; Bates, Scott T. Fungal Ecology, Vol. 20 https://doi.org/10.1016/j.funeco.2015.06.006	journal	April 2016
Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness Gotelli, Nicholas J.; Colwell, Robert K. Ecology Letters, Vol. 4, Issue 4 https://doi.org/10.1046/j.1461-0248.2001.00230.x	journal	July 2001
Is bacterial moisture niche a good predictor of shifts in community composition under long-term drought? Evans, Sarah E.; Wallenstein, Matthew D.; Burke, Ingrid C. Ecology, Vol. 95, Issue 1 https://doi.org/10.1890/13-0500.1	journal	January 2014
Vanishing winters in Germany: soil frost dynamics and snow cover trends, and ecological implications Kreyling, J.; Henry, Hal Climate Research, Vol. 46, Issue 3 https://doi.org/10.3354/cr00996	journal	May 2011
Waste Not, Want Not: Why Rarefying Microbiome Data is Inadmissible McMurdie, Paul J.; Holmes, Susan arXiv https://doi.org/10.48550/arxiv.1310.0424	text	January 2013
Network analysis reveals multiscale controls on streamwater chemistry McGuire, K. J.; Torgersen, C. E.; Likens, G. E. Proceedings of the National Academy of Sciences, Vol. 111, Issue 19 https://doi.org/10.1073/pnas.1404820111	journal	April 2014
Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics Hobbie, Erik A.; Högberg, Peter New Phytologist, Vol. 196, Issue 2 https://doi.org/10.1111/j.1469-8137.2012.04300.x	journal	August 2012
Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems Bödeker, Inga T. M.; Clemmensen, Karina E.; de Boer, Wietse New Phytologist, Vol. 203, Issue 1 https://doi.org/10.1111/nph.12791	journal	April 2014
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material Hodge, Angela; Campbell, Colin D.; Fitter, Alastair H. Nature, Vol. 413, Issue 6853 https://doi.org/10.1038/35095041	journal	September 2001
Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates de Graaff, Marie-Anne; Classen, Aimee T.; Castro, Hector F. New Phytologist, Vol. 188, Issue 4 https://doi.org/10.1111/j.1469-8137.2010.03427.x	journal	September 2010
Soil Denitrification Fluxes in a Northern Hardwood Forest: The Importance of Snowmelt and Implications for Ecosystem N Budgets Morse, Jennifer L.; Durán, Jorge; Groffman, Peter M. Ecosystems, Vol. 18, Issue 3 https://doi.org/10.1007/s10021-015-9844-2	journal	January 2015
Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible McMurdie, Paul J.; Holmes, Susan PLoS Computational Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pcbi.1003531	journal	April 2014
Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry: Global patterns of plant root mycorrhizal colonization intensity Soudzilovskaia, Nadejda A.; Douma, Jacob C.; Akhmetzhanova, Asem A. Global Ecology and Biogeography, Vol. 24, Issue 3 https://doi.org/10.1111/geb.12272	journal	January 2015
Seasonal and temporal dynamics of arbuscular mycorrhizal and dark septate endophytic fungi in a tallgrass prairie ecosystem are minimally affected by nitrogen enrichment Mandyam, Keerthi; Jumpponen, Ari Mycorrhiza, Vol. 18, Issue 3 https://doi.org/10.1007/s00572-008-0165-6	journal	February 2008
Nitrate and dissolved organic carbon mobilization in response to soil freezing variability Fuss, Colin B.; Driscoll, Charles T.; Groffman, Peter M. Biogeochemistry, Vol. 131, Issue 1-2 https://doi.org/10.1007/s10533-016-0262-0	journal	October 2016
Calcium and aluminum impacts on sugar maple physiology in a northern hardwood forest Halman, J. M.; Schaberg, P. G.; Hawley, G. J. Tree Physiology, Vol. 33, Issue 11 https://doi.org/10.1093/treephys/tpt099	journal	November 2013
PyNAST: a flexible tool for aligning sequences to a template alignment Caporaso, J. G.; Bittinger, K.; Bushman, F. D. Bioinformatics, Vol. 26, Issue 2 https://doi.org/10.1093/bioinformatics/btp636	journal	November 2009
The Performance of a Frost-Tube for the Determination of soil Freezing and Thawing Depths Rickard, Warren; Brown, Jerry Soil Science, Vol. 113, Issue 2 https://doi.org/10.1097/00010694-197202000-00011	journal	January 1972
Effects of selected root exudate components on soil bacterial communities: Root exudate components and soil microbial communities Shi, Shengjing; Richardson, Alan E.; O'Callaghan, Maureen FEMS Microbiology Ecology, Vol. 77, Issue 3 https://doi.org/10.1111/j.1574-6941.2011.01150.x	journal	July 2011
Microbial community responses to 17 years of altered precipitation are seasonally dependent and coupled to co-varying effects of water content on vegetation and soil C Sorensen, Patrick O.; Germino, Matthew J.; Feris, Kevin P. Soil Biology and Biochemistry, Vol. 64 https://doi.org/10.1016/j.soilbio.2013.04.014	journal	September 2013
Rhizosphere disturbance influences fungal colonization and community development on dead fine roots Fisk, Melany C.; Fahey, Timothy J.; Sobieraj, James H. Plant and Soil, Vol. 341, Issue 1-2 https://doi.org/10.1007/s11104-010-0643-4	journal	November 2010
Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland Cruz-Martínez, Karelyn; Suttle, K. Blake; Brodie, Eoin L. The ISME Journal, Vol. 3, Issue 6 https://doi.org/10.1038/ismej.2009.16	journal	March 2009
Effects of Winter Weather Conditions on soil Freezing in Southern Michigan Isard, Scott A.; Schaetzl, Randall J. Physical Geography, Vol. 19, Issue 1 https://doi.org/10.1080/02723646.1998.10642641	journal	January 1998
Increased nitrogen leaching following soil freezing is due to decreased root uptake in a northern hardwood forest Campbell, John L.; Socci, Anne M.; Templer, Pamela H. Global Change Biology, Vol. 20, Issue 8 https://doi.org/10.1111/gcb.12532	journal	February 2014
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Rhizosphere disturbance influences fungal colonization and community development on dead fine roots Fisk, Melany C.; Fahey, Timothy J.; Sobieraj, James H. Plant and Soil, Vol. 341, Issue 1-2 https://doi.org/10.1007/s11104-010-0643-4	journal	November 2010
Growing season warming and winter freeze–thaw cycles reduce root nitrogen uptake capacity and increase soil solution nitrogen in a northern forest ecosystem Sanders-DeMott, Rebecca; Sorensen, Patrick O.; Reinmann, Andrew B. Biogeochemistry, Vol. 137, Issue 3 https://doi.org/10.1007/s10533-018-0422-5	journal	January 2018
The Performance of a Frost-Tube for the Determination of soil Freezing and Thawing Depths Rickard, Warren; Brown, Jerry Soil Science, Vol. 113, Issue 2 https://doi.org/10.1097/00010694-197202000-00011	journal	January 1972
Mycorrhiza and Litter Decomposition Gadgil, Ruth L.; Gadgil, P. D. Nature, Vol. 233, Issue 5315 https://doi.org/10.1038/233133a0	journal	September 1971
Climate change at the ecosystem scale: a 50-year record in New Hampshire Hamburg, Steven P.; Vadeboncoeur, Matthew A.; Richardson, Andrew D. Climatic Change, Vol. 116, Issue 3-4 https://doi.org/10.1007/s10584-012-0517-2	journal	July 2012
Ecological Perspectives on Microbes Involved in N-Cycling Isobe, Kazuo; Ohte, Nobuhito Microbes and Environments, Vol. 29, Issue 1 https://doi.org/10.1264/jsme2.me13159	journal	January 2014
Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry Talbot, Jennifer M.; Martin, Francis; Kohler, Annegret Soil Biology and Biochemistry, Vol. 88 https://doi.org/10.1016/j.soilbio.2015.05.006	journal	September 2015
Winter climate change affects growing-season soil microbial biomass and activity in northern hardwood forests Durán, Jorge; Morse, Jennifer L.; Groffman, Peter M. Global Change Biology, Vol. 20, Issue 11 https://doi.org/10.1111/gcb.12624	journal	May 2014
Nitrate and dissolved organic carbon mobilization in response to soil freezing variability Fuss, Colin B.; Driscoll, Charles T.; Groffman, Peter M. Biogeochemistry, Vol. 131, Issue 1-2 https://doi.org/10.1007/s10533-016-0262-0	journal	October 2016
Differential sensitivity to climate change of C and N cycling processes across soil horizons in a northern hardwood forest Durán, Jorge; Morse, Jennifer L.; Rodríguez, Alexandra Soil Biology and Biochemistry, Vol. 107 https://doi.org/10.1016/j.soilbio.2016.12.028	journal	April 2017
Past and future changes in climate and hydrological indicators in the US Northeast Hayhoe, Katharine; Wake, Cameron P.; Huntington, Thomas G. Climate Dynamics, Vol. 28, Issue 4 https://doi.org/10.1007/s00382-006-0187-8	journal	November 2006
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Differential abundance analysis for microbial marker-gene surveys Paulson, Joseph N.; Stine, O. Colin; Bravo, Héctor Corrada Nature Methods, Vol. 10, Issue 12 https://doi.org/10.1038/nmeth.2658	journal	September 2013
Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? Read, D. J.; Perez-Moreno, J. New Phytologist, Vol. 157, Issue 3 https://doi.org/10.1046/j.1469-8137.2003.00704.x	journal	March 2003
Soil Microbial Community Responses to Multiple Experimental Climate Change Drivers Castro, H. F.; Classen, A. T.; Austin, E. E. Applied and Environmental Microbiology, Vol. 76, Issue 4 https://doi.org/10.1128/AEM.02874-09	journal	December 2009
Two decades of warming increases diversity of a potentially lignolytic bacterial community Pold, Grace; Melillo, Jerry M.; DeAngelis, Kristen M. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00480	journal	May 2015
Sequence Depth, Not PCR Replication, Improves Ecological Inference from Next Generation DNA Sequencing Smith, Dylan P.; Peay, Kabir G. PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0090234	journal	February 2014
Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics Hobbie, Erik A.; Högberg, Peter New Phytologist, Vol. 196, Issue 2 https://doi.org/10.1111/j.1469-8137.2012.04300.x	journal	August 2012
Increased soil respiration in response to experimentally reduced snow cover and increased soil freezing in a temperate deciduous forest Reinmann, Andrew B.; Templer, Pamela H. Biogeochemistry, Vol. 140, Issue 3 https://doi.org/10.1007/s10533-018-0497-z	journal	September 2018
UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi: Methods Kõljalg, Urmas; Larsson, Karl-Henrik; Abarenkov, Kessy New Phytologist, Vol. 166, Issue 3 https://doi.org/10.1111/j.1469-8137.2005.01376.x	journal	March 2005
A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries Fisher, Sheila; Barry, Andrew; Abreu, Justin Genome Biology, Vol. 12, Issue 1 https://doi.org/10.1186/gb-2011-12-1-r1	journal	January 2011
Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: What lies ahead? Classen, Aimée T.; Sundqvist, Maja K.; Henning, Jeremiah A. Ecosphere, Vol. 6, Issue 8 https://doi.org/10.1890/ES15-00217.1	journal	August 2015
Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness Gotelli, Nicholas J.; Colwell, Robert K. Ecology Letters, Vol. 4, Issue 4 https://doi.org/10.1046/j.1461-0248.2001.00230.x	journal	July 2001
FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild Nguyen, Nhu H.; Song, Zewei; Bates, Scott T. Fungal Ecology, Vol. 20 https://doi.org/10.1016/j.funeco.2015.06.006	journal	April 2016
Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions Schneider, Thomas; Keiblinger, Katharina M.; Schmid, Emanuel The ISME Journal, Vol. 6, Issue 9 https://doi.org/10.1038/ismej.2012.11	journal	March 2012
Climate Variation and Soil Carbon and Nitrogen Cycling Processes in a Northern Hardwood Forest Groffman, Peter M.; Hardy, Janet P.; Fisk, Melany C. Ecosystems, Vol. 12, Issue 6 https://doi.org/10.1007/s10021-009-9268-y	journal	September 2009
Is bacterial moisture niche a good predictor of shifts in community composition under long-term drought? Evans, Sarah E.; Wallenstein, Matthew D.; Burke, Ingrid C. Ecology, Vol. 95, Issue 1 https://doi.org/10.1890/13-0500.1	journal	January 2014
Reduced snow cover alters root-microbe interactions and decreases nitrification rates in a northern hardwood forest Sorensen, Patrick O.; Templer, Pamela H.; Christenson, Lynn Ecology, Vol. 97, Issue 12 https://doi.org/10.1002/ecy.1599	journal	December 2016
Climate change and soil freezing dynamics: historical trends and projected changes Henry, Hugh A. L. Climatic Change, Vol. 87, Issue 3-4 https://doi.org/10.1007/s10584-007-9322-8	journal	September 2007
Mycorrhizal fungi affect orchid distribution and population dynamics McCormick, Melissa K.; Whigham, Dennis F.; Canchani-Viruet, Armando New Phytologist, Vol. 219, Issue 4 https://doi.org/10.1111/nph.15223	journal	May 2018
PyNAST: a flexible tool for aligning sequences to a template alignment Caporaso, J. G.; Bittinger, K.; Bushman, F. D. Bioinformatics, Vol. 26, Issue 2 https://doi.org/10.1093/bioinformatics/btp636	journal	November 2009
Network analysis reveals multiscale controls on streamwater chemistry McGuire, K. J.; Torgersen, C. E.; Likens, G. E. Proceedings of the National Academy of Sciences, Vol. 111, Issue 19 https://doi.org/10.1073/pnas.1404820111	journal	April 2014
Phenology of a northern hardwood forest canopy Richardson, Andrew D.; Bailey, Amey Schenck; Denny, Ellen G. Global Change Biology, Vol. 12, Issue 7 https://doi.org/10.1111/j.1365-2486.2006.01164.x	journal	July 2006
Seasonality and partitioning of root allocation to rhizosphere soils in a midlatitude forest Abramoff, Rose Z.; Finzi, Adrien C. Ecosphere, Vol. 7, Issue 11 https://doi.org/10.1002/ecs2.1547	journal	November 2016
Seasonal and temporal dynamics of arbuscular mycorrhizal and dark septate endophytic fungi in a tallgrass prairie ecosystem are minimally affected by nitrogen enrichment Mandyam, Keerthi; Jumpponen, Ari Mycorrhiza, Vol. 18, Issue 3 https://doi.org/10.1007/s00572-008-0165-6	journal	February 2008
R$^{2}$s for Correlated Data: Phylogenetic Models, LMMs, and GLMMs Ives, Anthony R. Systematic Biology, Vol. 68, Issue 2 https://doi.org/10.1093/sysbio/syy060	journal	September 2018
A paradox of cooling winter soil surface temperatures in a warming northeastern United States Brown, Paula J.; DeGaetano, Arthur T. Agricultural and Forest Meteorology, Vol. 151, Issue 7 https://doi.org/10.1016/j.agrformet.2011.02.014	journal	July 2011
Trends in wintertime climate in the northeastern United States: 1965–2005 Burakowski, Elizabeth A.; Wake, Cameron P.; Braswell, Bobby Journal of Geophysical Research, Vol. 113, Issue D20 https://doi.org/10.1029/2008JD009870	journal	January 2008
Calcium and aluminum impacts on sugar maple physiology in a northern hardwood forest Halman, J. M.; Schaberg, P. G.; Hawley, G. J. Tree Physiology, Vol. 33, Issue 11 https://doi.org/10.1093/treephys/tpt099	journal	November 2013
Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry Talbot, Jennifer M.; Martin, Francis; Kohler, Annegret Soil Biology and Biochemistry, Vol. 88 https://doi.org/10.1016/j.soilbio.2015.05.006	journal	September 2015
Sequence Depth, Not PCR Replication, Improves Ecological Inference from Next Generation DNA Sequencing Smith, Dylan P.; Peay, Kabir G. PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0090234	journal	February 2014
Solid-phase reversible immobilization for the isolation of PCR products DeAngelis, Margaret M.; Wang, David G.; Hawkins, Trevor L. Nucleic Acids Research, Vol. 23, Issue 22 https://doi.org/10.1093/nar/23.22.4742	journal	January 1995
Winter climate change affects growing-season soil microbial biomass and activity in northern hardwood forests Durán, Jorge; Morse, Jennifer L.; Groffman, Peter M. Global Change Biology, Vol. 20, Issue 11 https://doi.org/10.1111/gcb.12624	journal	May 2014
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Ecological Perspectives on Microbes Involved in N-Cycling Isobe, Kazuo; Ohte, Nobuhito Microbes and Environments, Vol. 29, Issue 1 https://doi.org/10.1264/jsme2.me13159	journal	January 2014
Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? Read, D. J.; Perez-Moreno, J. New Phytologist, Vol. 157, Issue 3 https://doi.org/10.1046/j.1469-8137.2003.00704.x	journal	March 2003
CXCR4 signaling directs Igk recombination and the molecular mechanisms of late B lymphopoiesis Mandal, Malay; Okoreeh, Michael K.; Kennedy, Domenick E. Nature Immunology, Vol. 20, Issue 10 https://doi.org/10.1038/s41590-019-0468-0	journal	September 2019
Growing season warming and winter freeze–thaw cycles reduce root nitrogen uptake capacity and increase soil solution nitrogen in a northern forest ecosystem Sanders-DeMott, Rebecca; Sorensen, Patrick O.; Reinmann, Andrew B. Biogeochemistry, Vol. 137, Issue 3 https://doi.org/10.1007/s10533-018-0422-5	journal	January 2018
Catalytic power of enzymes decreases with temperature: New insights for understanding soil C cycling and microbial ecology under warming Alvarez, Gaël; Shahzad, Tanvir; Andanson, Laurence Global Change Biology, Vol. 24, Issue 9 https://doi.org/10.1111/gcb.14281	journal	May 2018
Predicting forest dieback in Maine, USA: a simple model based on soil frost and drought Auclair, Allan N. D.; Heilman, Warren E.; Brinkman, Blondel Canadian Journal of Forest Research, Vol. 40, Issue 4 https://doi.org/10.1139/x10-023	journal	April 2010
Life stages, demographic rates, and leaf damage for the round-leaved orchids, Platanthera orbiculata (Pursh.) Lindley and P. macrophylla (Goldie) P.M. Brown in a northern hardwood forest in New Hampshire, USA Cleavitt, Natalie L.; Berry, Eric J.; Hautaniemi, Jill Botany, Vol. 95, Issue 1 https://doi.org/10.1139/cjb-2016-0164	journal	January 2017
Life stages, demographic rates, and leaf damage for the round-leaved orchids, Platanthera orbiculata (Pursh.) Lindley and P. macrophylla (Goldie) P.M. Brown in a northern hardwood forest in New Hampshire, USA Cleavitt, Natalie L.; Berry, Eric J.; Hautaniemi, Jill Botany, Vol. 95, Issue 1 https://doi.org/10.1139/cjb-2016-0164	journal	January 2017
Effects of Winter Weather Conditions on soil Freezing in Southern Michigan Isard, Scott A.; Schaetzl, Randall J. Physical Geography, Vol. 19, Issue 1 https://doi.org/10.1080/02723646.1998.10642641	journal	January 1998
Catalytic power of enzymes decreases with temperature: New insights for understanding soil C cycling and microbial ecology under warming Alvarez, Gaël; Shahzad, Tanvir; Andanson, Laurence Global Change Biology, Vol. 24, Issue 9 https://doi.org/10.1111/gcb.14281	journal	May 2018
Predicting forest dieback in Maine, USA: a simple model based on soil frost and drought Auclair, Allan N. D.; Heilman, Warren E.; Brinkman, Blondel Canadian Journal of Forest Research, Vol. 40, Issue 4 https://doi.org/10.1139/x10-023	journal	April 2010
UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi: Methods Kõljalg, Urmas; Larsson, Karl-Henrik; Abarenkov, Kessy New Phytologist, Vol. 166, Issue 3 https://doi.org/10.1111/j.1469-8137.2005.01376.x	journal	March 2005
A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries Fisher, Sheila; Barry, Andrew; Abreu, Justin Genome Biology, Vol. 12, Issue 1 https://doi.org/10.1186/gb-2011-12-1-r1	journal	January 2011
Increased nitrogen leaching following soil freezing is due to decreased root uptake in a northern hardwood forest Campbell, John L.; Socci, Anne M.; Templer, Pamela H. Global Change Biology, Vol. 20, Issue 8 https://doi.org/10.1111/gcb.12532	journal	February 2014
Mycorrhiza and Litter Decomposition Gadgil, Ruth L.; Gadgil, P. D. Nature, Vol. 233, Issue 5315 https://doi.org/10.1038/233133a0	journal	September 1971
Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland Cruz-Martínez, Karelyn; Suttle, K. Blake; Brodie, Eoin L. The ISME Journal, Vol. 3, Issue 6 https://doi.org/10.1038/ismej.2009.16	journal	March 2009
Past and future changes in climate and hydrological indicators in the US Northeast Hayhoe, Katharine; Wake, Cameron P.; Huntington, Thomas G. Climate Dynamics, Vol. 28, Issue 4 https://doi.org/10.1007/s00382-006-0187-8	journal	November 2006
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
The microbial nitrogen-cycling network Kuypers, Marcel M. M.; Marchant, Hannah K.; Kartal, Boran Nature Reviews Microbiology, Vol. 16, Issue 5 https://doi.org/10.1038/nrmicro.2018.9	journal	February 2018
Solid-phase reversible immobilization for the isolation of PCR products DeAngelis, Margaret M.; Wang, David G.; Hawkins, Trevor L. Nucleic Acids Research, Vol. 23, Issue 22 https://doi.org/10.1093/nar/23.22.4742	journal	January 1995
An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material Hodge, Angela; Campbell, Colin D.; Fitter, Alastair H. Nature, Vol. 413, Issue 6853 https://doi.org/10.1038/35095041	journal	September 2001
Influence of experimental snow removal on root and canopy physiology of sugar maple trees in a northern hardwood forest Comerford, Daniel P.; Schaberg, Paul G.; Templer, Pamela H. Oecologia, Vol. 171, Issue 1 https://doi.org/10.1007/s00442-012-2393-x	journal	July 2012
A paradox of cooling winter soil surface temperatures in a warming northeastern United States Brown, Paula J.; DeGaetano, Arthur T. Agricultural and Forest Meteorology, Vol. 151, Issue 7 https://doi.org/10.1016/j.agrformet.2011.02.014	journal	July 2011
Soil Denitrification Fluxes in a Northern Hardwood Forest: The Importance of Snowmelt and Implications for Ecosystem N Budgets Morse, Jennifer L.; Durán, Jorge; Groffman, Peter M. Ecosystems, Vol. 18, Issue 3 https://doi.org/10.1007/s10021-015-9844-2	journal	January 2015
Differential abundance analysis for microbial marker-gene surveys Paulson, Joseph N.; Stine, O. Colin; Bravo, Héctor Corrada Nature Methods, Vol. 10, Issue 12 https://doi.org/10.1038/nmeth.2658	journal	September 2013
Climate change at the ecosystem scale: a 50-year record in New Hampshire Hamburg, Steven P.; Vadeboncoeur, Matthew A.; Richardson, Andrew D. Climatic Change, Vol. 116, Issue 3-4 https://doi.org/10.1007/s10584-012-0517-2	journal	July 2012
Differential sensitivity to climate change of C and N cycling processes across soil horizons in a northern hardwood forest Durán, Jorge; Morse, Jennifer L.; Rodríguez, Alexandra Soil Biology and Biochemistry, Vol. 107 https://doi.org/10.1016/j.soilbio.2016.12.028	journal	April 2017
Phenology of a northern hardwood forest canopy Richardson, Andrew D.; Bailey, Amey Schenck; Denny, Ellen G. Global Change Biology, Vol. 12, Issue 7 https://doi.org/10.1111/j.1365-2486.2006.01164.x	journal	July 2006
Past and projected future changes in snowpack and soil frost at the Hubbard Brook Experimental Forest, New Hampshire, USA Campbell, John L.; Ollinger, Scott V.; Flerchinger, Gerald N. Hydrological Processes https://doi.org/10.1002/hyp.7666	journal	January 2010