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Nutrient limitation of soil microbial activity during the earliest stages of ecosystem development

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Abstract

A dominant paradigm in ecology is that plants are limited by nitrogen (N) during primary succession. Whether generalizable patterns of nutrient limitation are also applicable to metabolically and phylogenetically diverse soil microbial communities, however, is not well understood. We investigated if measures of N and phosphorus (P) pools inform our understanding of the nutrient(s) most limiting to soil microbial community activities during primary succession. We evaluated soil biogeochemical properties and microbial processes using two complementary methodological approaches—a nutrient addition microcosm experiment and extracellular enzyme assays—to assess microbial nutrient limitation across three actively retreating glacial chronosequences. Microbial respiratory responses in the microcosm experiment provided evidence for N, P and N/P co-limitation at Easton Glacier, Washington, USA, Puca Glacier, Peru, and Mendenhall Glacier, Alaska, USA, respectively, and patterns of nutrient limitation generally reflected site-level differences in soil nutrient availability. The activities of three key extracellular enzymes known to vary with soil N and P availability developed in broadly similar ways among sites, increasing with succession and consistently correlating with changes in soil total N pools. Together, our findings demonstrate that during the earliest stages of soil development, microbial nutrient limitation and activity generally reflect soil nutrient supply, a result that is broadly consistent with biogeochemical theory.

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Acknowledgements

We would like to thank R. Callaway, S. Dobrowski, A. Larson, Y. Lekberg, A. Marklein, M. Nasto, and three anonymous reviewers for comments on early drafts of this manuscript. Authors declare no conflict of interest. This work was supported by a National Science Foundation Grant (NSF DEB-0922306) made to CC, EH, DN, and SS.

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Authors and Affiliations

  1. Department of Ecosystem and Conservation Sciences, University of Montana, Missoula, MT, 59812, USA

    Sarah C. Castle & Cory C. Cleveland

  2. Department of Natural Resources and Environmental Science, University of Nevada, Reno, NV, 89557, USA

    Benjamin W. Sullivan

  3. Institute of Arctic and Alpine Research and Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA

    Joseph Knelman

  4. Environmental Science Program, University of Alaska Southeast, Juneau, AK, 99801, USA

    Eran Hood

  5. Department of Biology, Duke University, Durham, NC, 27708, USA

    Diana R. Nemergut

  6. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA

    Steven K. Schmidt

  7. Department of Plant Pathology, University of Minnesota, 1991 Upper Buford Circle, 495 Borlaug, Saint Paul, MN, 55108, USA

    Sarah C. Castle

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  1. Sarah C. Castle
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  2. Benjamin W. Sullivan
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  3. Joseph Knelman
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  5. Diana R. Nemergut
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  7. Cory C. Cleveland
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SCC and CCC conceived and designed the experiments. SCC performed the experiments and analyzed the data. SCC, BWS, JK, and CCC wrote the manuscript; other authors provided editorial advice and all authors approved of the final version of the manuscript.

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Correspondence to Sarah C. Castle.

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Communicated by Jason P. Kaye.

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Castle, S.C., Sullivan, B.W., Knelman, J. et al. Nutrient limitation of soil microbial activity during the earliest stages of ecosystem development. Oecologia 185, 513–524 (2017). https://doi.org/10.1007/s00442-017-3965-6

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