Evidence for foliar endophytic nitrogen fixation in a widely distributed subalpine conifer

Moyes, Andrew B.; Kueppers, Lara M.; Pett-Ridge, Jennifer; Carper, Dana L.; Vandehey, Nick; O'Neil, James; Frank, A. Carolin

doi:10.1111/nph.13850

Title: Evidence for foliar endophytic nitrogen fixation in a widely distributed subalpine conifer

Journal Article · Mon Feb 01 00:00:00 EST 2016 · New Phytologist

DOI:https://doi.org/10.1111/nph.13850· OSTI ID:1251058

Moyes, Andrew B. ^[1]; Kueppers, Lara M. ^[1]; Pett-Ridge, Jennifer ^[2]; Carper, Dana L. ^[3]; Vandehey, Nick ^[4]; O'Neil, James ^[4]; Frank, A. Carolin ^[5]

Univ. of California Merced, Merced, CA (United States). Sierra Nevada Research Inst.; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Physical and Life Sciences Directorate
Univ. of California Merced, Merced, CA (United States). School of Natural Sciences and Life and Environmental Sciences
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division
Univ. of California Merced, Merced, CA (United States). Sierra Nevada Research Inst., School of Natural Sciences and Life and Environmental Sciences

Coniferous forest nitrogen (N) budgets indicate unknown sources of N. A consistent association between limber pine (Pinus flexilis) and potential N 2 -fixing acetic acid bacteria (AAB) indicates that native foliar endophytes may supply subalpine forests with N. To assess whether the P. flexilis-AAB association is consistent across years, we re-sampled P. flexilis twigs at Niwot Ridge, CO and characterized needle endophyte communities via 16S rRNA Illumina sequencing. To investigate whether endophytes have access to foliar N 2 , we incubated twigs with 13 N 2 -enriched air and imaged radioisotope distribution in needles, the first experiment of its kind using 13 N. We used the acetylene reduction assay to test for nitrogenase activity within P. flexilis twigs four times from June to September. We found evidence for N 2 fixation in P. flexilis foliage. N 2 diffused readily into needles and nitrogenase activity was positive across sampling dates. We estimate that this association could provide 6.8-13.6 μg N m -2 d -1 to P. flexilis stands. AAB dominated the P. flexilis needle endophyte community. We propose that foliar endophytes represent a low-cost, evolutionarily stable N 2 -fixing strategy for long-lived conifers. This novel source of biological N 2 fixation has fundamental implications for understanding forest N budgets.

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); Univ. of Colorado, Boulder, CO (United States). Mountain Research Station; National Science Foundation (NSF)

Grant/Contract Number:: AC52-07NA27344; IOS-1321807; AC02-05CH11231

OSTI ID:: 1251058

Alternate ID(s):: OSTI ID: 1440924

Report Number(s):: LLNL-JRNL-671997

Journal Information:: New Phytologist, Vol. 210, Issue 2; ISSN 0028-646X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 90 works

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Spore-Positive and Spore-Negative Nodules Schwintzer, Christa R. The Biology of Frankia and Actinorhizal Plants https://doi.org/10.1016/B978-0-12-633210-0.50014-9	book	January 1990
Microbial Dysbiosis During Simian Immunodeficiency Virus Infection is Partially Reverted with Combination Anti-retroviral Therapy Blum, Faith C.; Hardy, Britney L.; Bishop-Lilly, Kimberly A. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-63196-0	journal	April 2020
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Acetobacter diazotrophicus sp. nov., a Nitrogen-Fixing Acetic Acid Bacterium Associated with Sugarcane Gillis, M.; Kersters, K.; Hoste, B. International Journal of Systematic Bacteriology, Vol. 39, Issue 4 https://doi.org/10.1099/00207713-39-4-502	journal	October 1989

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Nitrogen fixation does not balance fire‐induced nitrogen losses in longleaf pine savannas Tierney, Julie A.; Hedin, Lars O.; Wurzburger, Nina Ecology, Vol. 100, Issue 7 https://doi.org/10.1002/ecy.2735	journal	May 2019
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Nitrogen Fixing Endophytes in Forest Trees Oses, Rómulo; Frank, A. Carolin; Valenzuela, Sofía Endophytes of Forest Trees https://doi.org/10.1007/978-3-319-89833-9_9	book	January 2018
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Bacterial endophyte communities in Pinus flexilis are structured by host age, tissue type, and environmental factors Carper, Dana L.; Carrell, Alyssa A.; Kueppers, Lara M. Plant and Soil, Vol. 428, Issue 1-2 https://doi.org/10.1007/s11104-018-3682-x	journal	May 2018
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Endophytic nitrogen fixation – a possible ‘hidden’ source of nitrogen for lodgepole pine trees growing at unreclaimed gravel mining sites Padda, Kiran Preet; Puri, Akshit; Chanway, Chris FEMS Microbiology Ecology, Vol. 95, Issue 11 https://doi.org/10.1093/femsec/fiz172	journal	October 2019
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Plant host identity and soil macronutrients explain little variation in sapling endophyte community composition: Is disturbance an alternative explanation? Griffin, Eric A.; Harrison, Joshua G.; Kembel, Steven W. Journal of Ecology, Vol. 107, Issue 4 https://doi.org/10.1111/1365-2745.13145	journal	February 2019
Substrate stoichiometry determines nitrogen fixation throughout succession in southern Chinese forests Zheng, Mianhai; Chen, Hao; Li, Dejun Ecology Letters, Vol. 23, Issue 2 https://doi.org/10.1111/ele.13437	journal	December 2019
Global pattern and controls of biological nitrogen fixation under nutrient enrichment: A meta‐analysis Zheng, Mianhai; Zhou, Zhenghu; Luo, Yiqi Global Change Biology, Vol. 25, Issue 9 https://doi.org/10.1111/gcb.14705	journal	May 2019
The importance of phyllosphere on plant functional ecology: a phyllo trait manifesto Rosado, Bruno H. P.; Almeida, Lidiane C.; Alves, Luciana F. New Phytologist, Vol. 219, Issue 4 https://doi.org/10.1111/nph.15235	journal	May 2018
Niche differentiation rather than biogeography shapes the diversity and composition of microbiome of Cycas panzhihuaensis Zheng, Ying; Gong, Xun Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0770-y	journal	December 2019
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Putative Nitrogen-Fixing Bacteria Associated With the Rhizosphere and Root Endosphere of Wheat Plants Grown in an Andisol From Southern Chile Rilling, Joaquin I.; Acuña, Jacquelinne J.; Sadowsky, Michael J. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02710	journal	November 2018
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Bacteriome from Pinus arizonica and P. durangensis: Diversity, Comparison of Assemblages, and Overlapping Degree with the Gut Bacterial Community of a Bark Beetle That Kills Pines Gonzalez-Escobedo, Roman; Briones-Roblero, Carlos I.; Pineda-Mendoza, Rosa M. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00077	journal	January 2018
The Effect of Microbial Endophyte Consortia on Pseudotsuga menziesii and Thuja plicata Survival, Growth, and Physiology Across Edaphic Gradients Aghai, Matthew M.; Khan, Zareen; Joseph, Matthew R. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01353	journal	June 2019

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54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES
07 ISOTOPES AND RADIATION SOURCES
37 INORGANIC
ORGANIC
PHYSICAL AND ANALYTICAL CHEMISTRY
nitrogen fixation
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acetic acid bacteria
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Pinus flexilis
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subalpine

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