The role of soil redox conditions in microbial phosphorus cycling in humid tropical forests.
NanoSIMS
anoxic conditions
carbon use efficiency
humid tropical ecosystem
microbial stoichiometry
phosphorus cycle
soil redox
Journal
Ecology
ISSN: 1939-9170
Titre abrégé: Ecology
Pays: United States
ID NLM: 0043541
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
13
11
2018
revised:
16
07
2019
accepted:
25
09
2019
pubmed:
13
11
2019
medline:
26
9
2020
entrez:
13
11
2019
Statut:
ppublish
Résumé
Humid tropical forests are among the most productive ecosystems globally, yet they often occur on soils with high phosphorus (P) sorption capacity, lowering P availability to biota. Short-term anoxic events are thought to release sorbed P and enhance its acquisition by soil microbes. However, the actual effects of anoxic conditions on microbial P acquisition in humid tropical forest soils are surprisingly poorly studied. We used laboratory incubations of bulk soils, NanoSIMS analysis of single microbial cells, and landscape-scale measurements in the Luquillo Experimental Forest (LEF), Puerto Rico to test the hypothesis that anoxic conditions increase microbial P acquisition in humid tropical forests. In laboratory and field experiments, we found that microbial P uptake generally decreased under anoxic conditions, leading to high microbial carbon (C) to P ratios in anoxic soils. The decreased P acquisition under anoxic conditions was correlated with lower microbial C use efficiency (CUE), an index of microbial energy transfer in ecosystems. Phosphorus amendments to anoxic soils led to increased microbial P uptake and higher CUE suggesting that microbes were less able to access and utilize P under natural low redox conditions. Under oxic conditions, microbial C:P ratios and CUE did not respond to changes in substrate stoichiometry. These results challenge the existing paradigm by showing that anoxic conditions can decrease microbial P uptake and ultimately constrain microbial CUE. Our findings indicate that soil redox conditions tightly couple soil P and C cycles and advance our understanding of controls on P cycling in humid tropical forest ecosystems.
Substances chimiques
Soil
0
Phosphorus
27YLU75U4W
Carbon
7440-44-0
Nitrogen
N762921K75
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e02928Subventions
Organisme : US-Israeli Bi National Agricultural Research and Development Postdoctoral Fellowship
Pays : International
Organisme : Department of Energy
ID : TES-DE-FOA-0000749
Pays : International
Organisme : National Science Foundation
ID : DEB-1457805
Pays : International
Organisme : OBER Genomic Sciences Early Career Research Program Award
ID : SCW1478
Pays : International
Organisme : Luquillo CZO
ID : EAR-1331841
Pays : International
Organisme : LTER
ID : DEB-0620910
Pays : International
Organisme : USDA National Institute of Food and Agriculture, McIntire Stennis Project
ID : CA-B-ECO-7673-MS
Pays : International
Informations de copyright
© 2019 by the Ecological Society of America.
Références
Barone, J. A., J. Thomlinson, P. A. Cordero, and J. K. Zimmerman. 2008. Metacommunity structure of tropical forest along an elevation gradient in Puerto Rico. Journal of Tropical Ecology 24:525-534.
Beinroth, F. J. G.. 1982. Some highly weathered soils of Puerto Rico, 1. Morphology, formation and classification. 27:1-73.
Brant, J. B., E. W. Sulzman, and D. D. Myrold. 2006. Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biology and Biochemistry 38:2219-2232.
Brookes, P., D. Powlson, and D. Jenkinson. 1982. Measurement of microbial biomass phosphorus in soil. Soil Biology and Biochemistry 14:319-329.
Brown, S., A. E. Lugo, S. Silander, and L. Liegel. 1983. Research history and opportunities in the Luquillo Experimental Forest. Southern Forest Experiment Station, Rio Piedras, Puerto Rico, USA.
Chacon, N., W. L. Silver, E. A. Dubinsky, and D. F. Cusack. 2006. Iron reduction and soil phosphorus solubilization in humid tropical forests soils: The roles of labile carbon pools and an electron shuttle compound. Biogeochemistry 78:67-84.
Chadwick, R., P. Good, G. Martin, and D. P. Rowell. 2016. Large rainfall changes consistently projected over substantial areas of tropical land. Nature Climate Change 6:177-181.
Cleveland, C. C., and D. Liptzin. 2007. C : N : P stoichiometry in soil: is there a "Redfield ratio" for the microbial biomass? Biogeochemistry 85:235-252.
Cleveland, C. C., B. Z. Houlton, W. K. Smith, A. R. Marklein, S. C. Reed, W. Parton, S. J. Del Grosso, and S. W. Running. 2013. Patterns of new versus recycled primary production in the terrestrial biosphere. Proceedings of the National Academy of Sciences USA 110:12733-12737.
Comeau, Y., K. Hall, R. Hancock, and W. Oldham. 1986. Biochemical model for enhanced biological phosphorus removal. Water Research 20:1511-1521.
Davelaar, D. 1993. Ecological significance of bacterial polyphosphate metabolism in sediments. Hydrobiologia 253:179-192.
DeAngelis, K. M., W. L. Silver, A. W. Thompson, and M. K. J. E. M. Firestone. 2010. Microbial communities acclimate to recurring changes in soil redox potential status. Environmental Microbiology 12:3137-3149.
Eichorst, S. A., F. Strasser, T. Woyke, A. Schintlmeister, M. Wagner, and D. Woebken. 2015. Advancements in the application of NanoSIMS and Raman microspectroscopy to investigate the activity of microbial cells in soils. FEMS Microbiology Ecology 91:101-106.
Elser, J., R. Sterner, E. Gorokhova, W. Fagan, T. Markow, J. Cotner, J. Harrison, S. Hobbie, G. Odell, and L. Weider. 2000. Biological stoichiometry from genes to ecosystems. Ecology Letters 3:540-550.
Fanin, N., N. Fromin, B. Buatois, and S. Hättenschwiler. 2013. An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter-microbe system. Ecology Letters 16:764-772.
Frey, S., V. Gupta, E. Elliott, and K. Paustian. 2001. Protozoan grazing affects estimates of carbon utilization efficiency of the soil microbial community. Soil Biology and Biochemistry 33:1759-1768.
Frey, S. D., J. Lee, J. M. Melillo, and J. Six. 2013. The temperature response of soil microbial efficiency and its feedback to climate. Nature Climate Change 3:395-398.
Geyer, K. M., E. Kyker-Snowman, A. S. Grandy, and S. D. Frey. 2016. Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry 127:173-188.
Gross, A., B. L. Turner, S. J. Wright, E. V. J. Tanner, M. Reichstein, T. Weiner, and A. Angert. 2015. Oxygen isotope ratios of plant available phosphate in lowland tropical forest soils. Soil Biology and Biochemistry 88:354-361.
Gross, A., J. Pett-Ridge, and W. J. S. S. Silver. 2018. Soil oxygen limits microbial phosphorus utilization in humid tropical forest soils. Soil Systems 2:65.
Hall, S. J., and W. L. Silver. 2015. Reducing conditions, reactive metals, and their interactions can explain spatial patterns of surface soil carbon in a humid tropical forest. Biogeochemistry 125:149-165.
Hall, S. J., J. Treffkorn, and W. L. Silver. 2014. Breaking the enzymatic latch: impacts of reducing conditions on hydrolytic enzyme activity in tropical forest soils. Ecology 95:2964-2973.
Hall, S. J., W. L. Silver, V. I. Timokhin, and K. E. Hammel. 2015. Lignin decomposition is sustained under fluctuating redox conditions in humid tropical forest soils. Global Change Biology 21:2818-2828.
He, S., D. L. Gall, and K. D. J. A. E. M. McMahon. 2007. “Candidatus Accumulibacter” population structure in enhanced biological phosphorus removal sludges as revealed by polyphosphate kinase genes. Applied and Enironmental Microbiology 73:5865-5874.
Herrmann, A. M., K. Ritz, N. Nunan, P. L. Clode, J. Pett-Ridge, M. R. Kilburn, D. V. Murphy, A. G. O’Donnell, and E. A. Stockdale. 2007. Nano-scale secondary ion mass spectrometry-A new analytical tool in biogeochemistry and soil ecology: A review article. Soil Biology and Biochemistry 39:1835-1850.
Heuck, C., A. Weig, and M. Spohn. 2015. Soil microbial biomass C: N: P stoichiometry and microbial use of organic phosphorus. Soil Biology and Biochemistry 85:119-129.
Johnson, A. H., J. Frizano, and D. R. Vann. 2003. Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure. Oecologia 135:487-499.
Kerrn-Jespersen, J. P., and M. Henze. 1993. Biological phosphorus uptake under anoxic and aerobic conditions. Water Research 27:617-624.
Khalyani, A. H., W. A. Gould, E. Harmsen, A. Terando, M. Quinones, and J. A. Collazo. 2016. Climate change implications for tropical islands: interpolating and interpreting statistically downscaled GCM projections for management and planning. Journal of Applied Meteorology and Climatology 55:265-282.
Kouno, K., Y. Tuchiya, and T. Ando. 1995. Measurement of soil microbial biomass phosphorus by an anion-exchange membrane method. Soil Biology & Biochemistry 27:1353-1357.
Li, J., Z. Li, F. Wang, B. Zou, Y. Chen, J. Zhao, Q. Mo, Y. Li, X. Li, and H. Xia. 2015. Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China. Biology and Fertility of Soils 51:207-215.
Lin, Y., A. Bhattacharyya, A. N. Campbell, P. S. Nico, J. Pett-Ridge, and W. L. Silver. 2018. Phosphorus fractionation responds to dynamic redox conditions in a humid tropical forest soil. Journal of Geophysical Research: Biogeosciences 123:3016-3027.
Liptzin, D., and W. L. Silver. 2009. Effects of carbon additions on iron reduction and phosphorus availability in a humid tropical forest soil. Soil Biology & Biochemistry 41:1696-1702.
Liptzin, D., and W. L. Silver. 2015. Spatial patterns in oxygen and redox sensitive biogeochemistry in tropical forest soils. Ecosphere 6:1-14.
Liptzin, D., W. L. Silver, and M. Detto. 2011. Temporal dynamics in soil oxygen and greenhouse gases in two humid tropical forests. Ecosystems 14:171-182.
Manzoni, S., P. Taylor, A. Richter, A. Porporato, and G. I. Ågren. 2012. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytologist 196:79-91.
Manzoni, S., P. Čapek, P. Porada, M. Thurner, M. Winterdahl, C. Beer, V. Brüchert, J. Frouz, A. M. Herrmann, and B. D. Lindahl. 2018. Reviews and syntheses: Carbon use efficiency from organisms to ecosystems-definitions, theories, and empirical evidence. Biogeosciences 15:5929-5949.
Miller, A. J., E. A. G. Schuur, and O. A. Chadwick. 2001. Redox control of phosphorus pools in Hawaiian montane forest soils. Geoderma 102:219-237.
Mino, T., M. Van Loosdrecht, and J. Heijnen. 1998. Microbiology and biochemistry of the enhanced biological phosphate removal process. Water Research 32:3193-3207.
Mueller, C. W., P. K. Weber, M. R. Kilburn, C. Hoeschen, M. Kleber, and J. Pett-Ridge. 2013. Advances in the analysis of biogeochemical interfaces: NanoSIMS to investigate soil microenvironments. Pages 1-46 in D. L. Sparks, editor.Advances in agronomy. Volume 121. Elsevier, San Diego, CA, USA.
Murphy, S. F., R. F. Stallard, M. A. Scholl, G. González, and A. J. Torres-Sánchez. 2017. Reassessing rainfall in the Luquillo Mountains, Puerto Rico: Local and global ecohydrological implications. PLoS ONE 12:e0180987.
Neelin, J. D., M. Münnich, H. Su, J. E. Meyerson, and C. E. Holloway. 2006. Tropical drying trends in global warming models and observations. Proceedings of the National Academy of Sciences USA 103:6110-6115.
Newman, S., and K. Reddy. 1993. Alkaline phosphatase activity in the sediment-water column of a hypereutrophic lake. Journal of Environmental Quality 22:832-838.
O’Connell, C. S., L. Ruan, and W. L. Silver. 2018. Drought drives rapid shifts in tropical rainforest soil biogeochemistry and greenhouse gas emissions. Nature Communications 9:1348.
Olander, L. P., and P. M. Vitousek. 2004. Biological and geochemical sinks for phosphorus in soil from a wet tropical forest. Ecosystems 7:404-419.
Pan, Y., R. A. Birdsey, O. L. Phillips, and R. B. Jackson. 2013. The structure, distribution, and biomass of the world's forests. Annual Review of Ecology, Evolution, and Systematics 44:593-622.
Peretyazhko, T., and G. Sposito. 2005. Iron(III) reduction and phosphorous solubilization in humid tropical forest soils. Geochimica et Cosmochimica Acta 69:3643-3652.
Pett-Ridge, J., and M. K. Firestone. 2005. Redox fluctuation structures microbial communities in a wet tropical soil. Applied and Environment Microbiology 71:6998-7007.
Pett-Ridge, J., and P. K. Weber. 2012. NanoSIP: NanoSIMS applications for microbial biology. Microbial Systems Biology: Methods and Protocols 881:375-408.
Pett-Ridge, J., W. L. Silver, and M. K. Firestone. 2006. Redox fluctuations frame microbial community impacts on N-cycling rates in a humid tropical forest soil. Biogeochemistry 81:95-110.
Phillips, O. L., Y. Malhi, N. Higuchi, W. F. Laurance, P. V. Núnez, R. M. Vásquez, S. G. Laurance, L. V. Ferreira, M. Stern, and S. Brown. 1998. Changes in the carbon balance of tropical forests: evidence from long-term plots. Science 282:439-442.
R Core Team. 2019. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.R-project.org
Richardson, A. E., and R. J. Simpson. 2011. Soil microorganisms mediating phosphorus availability. Plant Physiology 156:989-996.
Silver, W. L., A. Lugo, and M. Keller. 1999. Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils. Biogeochemistry 44:301-328.
Silver, W. L., D. Liptzin, and M. Almaraz. 2013. Soil redox dynamics and biogeochemistry along a tropical elevation gradient. Ecological Bulletins 54:195-209.
Sinsabaugh, R. L., S. Manzoni, D. L. Moorhead, and A. Richter. 2013. Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecology Letters 9:930-939.
Turner, B. L., H. Lambers, L. M. Condron, M. D. Cramer, J. R. Leake, A. E. Richardson, and S. E. Smith. 2013. Soil microbial biomass and the fate of phosphorus during long-term ecosystem development. Plant and Soil 367:225-234.
Vance, E., P. Brookes, and D. Jenkinson. 1987. An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry 19:703-707.
Vitousek, P. M. 1984. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285-298.
Vitousek, P. M., and R. Sanford. 1986. Nutrient cycling in moist tropical forest. Annual Review of Ecology and Systematics 17:137-1677.
Vitousek, P. M., S. Porder, B. Z. Houlton, and O. A. Chadwick. 2010. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications 20:5-15.
Weaver, P. L., and P. G. Murphy. 1990. Forest structure and productivity in Puerto Rico's Luquillo Mountains. Biotropica 22:69-82.
Wilcoxon, F. 1945. Individual comparisons by ranking methods. Biometrics Bulletin 1:80-83.
Willig, M. R., S. J. Presley, C. P. Bloch, I. Castro-Arellano, L. M. Cisneros, C. L. Higgins, and B. T. Klingbeil. 2011. Tropical metacommunities along elevational gradients: effects of forest type and other environmental factors. Oikos 120:1497-1508.
Willig, M. R., S. J. Presley, C. P. Bloch, and J. Alvarez. 2013. Population, community, and metacommunity dynamics of terrestrial gastropods in the Luquillo Mountains: a gradient perspective. Ecological Bulletins 54:117-140.
Wolf, J., G. Brocard, J. Willenbring, S. Porder, and M. Uriarte. 2016. Abrupt change in forest height along a tropical elevation gradient detected using airborne lidar. Remote Sensing 8:864.
Wright, R., B. Lockaby, and M. Walbridge. 2001. Phosphorus availability in an artificially flooded southeastern floodplain forest soil. Soil Science Society of America Journal 65:1293-1302.
Wright, S. J., et al. 2011. Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616-1625.
Xu, X., P. E. Thornton, and W. M. Post. 2013. A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Global Ecology and Biogeography 22:737-749.
Yeoman, S., T. Stephenson, J. Lester, and R. Perry. 1988. The removal of phosphorus during wastewater treatment: a review. Environmental Pollution 49:183-233.