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Surprising relationships between soil pH and microbial biomass and activity in a northern hardwood forest

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Abstract

Soil microbes mediate major biogeochemical processes in forest ecosystems. Soil pH is considered a “master variable” with a strong positive effect on many biogeochemical processes. To better understand how soil pH influences microbial activity and nitrogen (N) dynamics in forests, we utilized a set of long-term measurements of surface soil pH, N availability, and microbial biomass and respiration from the Hubbard Brook Experimental Forest (HBEF), a northern hardwood forest in New Hampshire, USA. We compared the strengths of these relationships in an unmanipulated watershed, where naturally acidic soils have been further acidified by anthropogenic acid deposition, to those in a nearby watershed, where soils were treated with calcium silicate to ameliorate the effects of acid deposition. While we expected to observe strong positive relationships between soil pH and microbial biomass and activity, we instead found weak and/or curvilinear relationships. In many cases, microbial biomass and activity peaked at unexpectedly low pH values (~ 4.5), and decreased at higher pH values, especially in the calcium-treated soils. It is likely that complexities in plant-microbial interactions inhibit and/or mask microbial response to changes in pH in these acidic soils. These results raise questions about pH as a controller of microbial processes and how ecosystems recover in response to decreases in acid deposition.

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Data availability

Data are available at: https://portal.edirepository.org/nis/mapbrowse?scope=knb-lter-hbr&identifier=252.

References

  • Bahram M, Hildebrand F, Forslund SK, Anderson JL, Soudzilovskaia NA, Bodegom PM, Bengtsson-Palme J, Anslan S, Coelho LP, Harend H, Huerta-Cepas J, Medema MH, Maltz MR, Mundra S, Olsson PA, Pent M, Põlme S, Sunagawa S, Ryberg M, Tedersoo L, Bork P (2018) Structure and function of the global topsoil microbiome. Nature 560(7717):233–237

    Article  Google Scholar 

  • Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515(7528):505–511

    Article  Google Scholar 

  • Battles JJ, Fahey TJ, Driscoll CT Jr, Blum JD, Johnson CE (2014) Restoring soil calcium reverses forest decline. Environ Sci Technol Lett 1(1):15–19

    Article  Google Scholar 

  • Bohlen PJ, Groffman PM, Driscoll CT, Fahey TJ, Siccama TG (2001) Plant-soil-microbial interactions in a northern hardwood forest. Ecology 82(4):965–978

    Google Scholar 

  • Campbell JL, Rustad LE, Bailey SW, Bernhardt ES, Driscoll CT, Green MB, Groffman PM, Lovett GM, McDowell WH, McGuire KJ, Rosi EJ (2021) Watershed studies at the Hubbard Brook Experimental Forest: building on a long legacy of research with new approaches and sources of data. Hydrol Process 35(1):e14016

    Article  Google Scholar 

  • Cho Y, Driscoll C, Johnson C, Siccama T (2010) Chemical changes in soil and soil solution after calcium silicate addition to a northern hardwood forest. Biogeochemistry 100(1):3–20

    Article  Google Scholar 

  • Cho Y, Driscoll CT, Johnson CE, Blum JD, Fahey TJ (2012) Watershed-level responses to calcium silicate treatment in a northern hardwood forest. Ecosystems 15(3):416–434

    Article  Google Scholar 

  • Coleman DC, Callaham MA, Crossley DA Jr (2017) Fundamentals of soil ecology, 3rd edn. Elsevier Academic Press, Oxford

    Google Scholar 

  • Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD, Maestre FT, Singh BK, Fierer N (2018) A global atlas of the dominant bacteria found in soil. Science 359(6373):320–325

    Article  Google Scholar 

  • Drake JE, Gallet-Budynek A, Hofmockel KS, Bernhardt ES, Billings SA, Jackson RB, Johnsen KS, Lichter J, McCarthy HR, McCormack ML, Moore DJP, Oren R, Palmroth S, Phillips RP, Pippen JS, Pritchard SG, Treseder KK, Schlesinger WH, DeLucia EH, Finzi AC (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14(4):349–357

    Article  Google Scholar 

  • Driscoll CT, Lawrence GB, Bulger AJ, Butler TJ, Cronan CS, Eagar C, Lambert KF, Likens GE, Stoddard JL, Weathers KC (2001) Acidic deposition in the northeastern United States: sources and inputs, ecosystem effects, and management strategies. Bioscience 51(3):180–198

    Article  Google Scholar 

  • Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12(11):1238–1249

    Article  Google Scholar 

  • Fiorentino I, Fahey TJ, Groffman PM, Driscoll CT, Eagar C, Siccama TG (2003) Initial responses of phosphorus biogeochemistry to calcium addition in a northern hardwood forest ecosystem. Can J for Res 33(10):1864–1873

    Article  Google Scholar 

  • Gadgil RL, Gadgil P (1971) Mycorrhiza and litter decomposition. Nature 233(5315):133–133

    Article  Google Scholar 

  • Garcia MO, Templer PH, Sorensen PO, Sanders-DeMott R, Groffman PM, Bhatnagar JM (2020) Soil microbes trade-off biogeochemical cycling for stress tolerance traits in response to year-round climate change. Front Microbiol 11:616

    Article  Google Scholar 

  • Groffman PM, Fisk MC (2011a) Calcium constrains plant control over forest ecosystem nitrogen cycling. Ecology 92:2035–2042

    Article  Google Scholar 

  • Groffman PM, Fisk MC (2011b) Phosphate additions have no effect on microbial biomass and activity in a northern hardwood forest. Soil Biol Biochem 43:2441–2449

    Article  Google Scholar 

  • Groffman PM, Holland EA, Myrold DD, Robertson GP, Zou X (1999) Denitrification. In: Robertson GP, Bledsoe CS, Coleman DC, Sollins P (eds) Standard soil methods for long term ecological research. Oxford University Press, New York, pp 272–288

    Google Scholar 

  • Groffman PM, Fisk MC, Driscoll CT, Likens GE, Fahey TJ, Eagar C, Pardo LH (2006) Calcium additions and microbial nitrogen cycle processes in a northern hardwood forest. Ecosystems 9(8):1289–1305

    Article  Google Scholar 

  • Groffman PM, Discoll CT, Duran J, Campbell JL, Christenson LM, Fahey TJ, Fisk MC, Fuss C, Likens GE, Lovett GM, Rustad L, Templer P (2018) Nitrogen oligotrophication in northern hardwood forests. Biogeochemistry 141:123–129

    Article  Google Scholar 

  • Groffman PM (2019) Long-term measurements of microbial biomass and activity at the Hubbard Brook Experimental Forest, 1994—present. In Environmental data initiative. https://doi.org/10.6073/pasta/2a0482218fa34bs667e501c8cc48f8be8. Dataset accessed 01/31/2022.

  • Hartman WH, Richardson CJ, Vilgalys R, Bruland GL (2008) Environmental and anthropogenic controls over bacterial communities in wetland soils. Proc Natl Acad Sci 105(46):17842–17847

    Article  Google Scholar 

  • Haynes W (2013) Bonferroni correction. In: Dubitzky W, Wolkenhauer O, Cho K-H, Yokota H (eds) Encyclopedia of systems biology. Springer, New York, pp 154–154

    Chapter  Google Scholar 

  • Jandl R, Smidt S, Mutsch F, Fürst A, Zechmeister H, Bauer H, Dirnböck T (2012) Acidification and nitrogen eutrophication of Austrian forest soils. Appl Environ Soil Sci 2012:632602

    Article  Google Scholar 

  • Jenkinson DS, Powlson DS (1976) The effects of biocidal treatments on metabolism in soil V: a method for measuring soil biomass. Soil Biol Biochem 8:209–213

    Article  Google Scholar 

  • Johnson CE, Driscoll CT, Siccama TG, Likens GE (2000) Element fluxes and landscape position in a northern hardwood forest watershed ecosystem. Ecosystems 3(2):159–184

    Article  Google Scholar 

  • Johnson CE, Driscoll CT, Blum JD, Fahey TJ, Battles JJ (2014) Soil chemical dynamics after calcium silicate addition to a northern hardwood forest. Soil Sci Soc Am J 78(4):1458–1468

    Article  Google Scholar 

  • Juice SM, Fahey TJ, Siccama TG, Driscoll CT, Denny EG, Eagar C, Cleavitt NL, Minocha R, Richardson AD (2006) Response of sugar maple to calcium addition to northern hardwood forest. Ecology 87(5):1267–1280

    Article  Google Scholar 

  • Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199

    Article  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75(15):5111–5120

    Article  Google Scholar 

  • Lawrence GB, David MB, Shortle WC (1995) A new mechanism for calcium loss in forest-floor soils. Nature 378(6553):162–165

    Article  Google Scholar 

  • Likens GE, Driscoll CT, Buso DC (1996) Long-term effects of acid rain: response and recovery of a forest ecosystem. Science 272(5259):244–246

    Article  Google Scholar 

  • Likens GE, Driscoll CT, Buso DC, Siccama TG, Johnson CE, Lovett GM, Fahey TJ, Reiners WA, Ryan DF, Martin CW, Bailey SW (1998) The biogeochemistry of calcium at Hubbard Brook. Biogeochemistry 41(2):89–173

    Article  Google Scholar 

  • Likens GE, Buso DC, Bernhardt ES, Rosi E (2021) A century of change: reconstructing the biogeochemical history of Hubbard Brook. Hydrol Process 35(6):e14256

    Article  Google Scholar 

  • McInnes KJ, Weaver RW, Savage MJ (1994) Soil water potential. In: Weaver RW (ed) Methods of soil analysis, part 2—microbiological and biochemical properties. Soil Science Society of America, Madison, pp 53–58

    Google Scholar 

  • Meng C, Tian D, Zeng H, Li Z, Yi C, Niu S (2019) Global soil acidification impacts on belowground processes. Environ Res Lett 14(7):074003

    Article  Google Scholar 

  • Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10(11):2966–2978

    Article  Google Scholar 

  • Oulehle F, Evans CD, Hofmeister J, Krejci R, Tahovska K, Persson T, Cudlin P, Hruska J (2011) Major changes in forest carbon and nitrogen cycling caused by declining sulphur deposition. Glob Change Biol 17(10):3115–3129

    Article  Google Scholar 

  • Oulehle F, Chuman T, Hruška J, Krám P, McDowell WH, Myška O, Navrátil T, Tesař M (2017) Recovery from acidification alters concentrations and fluxes of solutes from Czech catchments. Biogeochemistry 132(3):251–272

    Article  Google Scholar 

  • Palmer SM, Driscoll CT, Johnson CE (2004) Long-term trends in soil solution and stream water chemistry at the Hubbard Brook Experimental Forest: relationship with landscape position. Biogeochemistry 68(1):51–70

    Article  Google Scholar 

  • Paul EA (ed) (2014) Soil microbiology, ecology, and biochemistry, 4th edn. Academic Press, Amsterdam

    Google Scholar 

  • Payne WJ (1981) Denitrification. Wiley, New Yrok

    Google Scholar 

  • R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Roco CA, Dörsch P, Booth JG, Pepe-Ranney C, Groffman PM, Fahey TJ, Yavitt JB, Shapleigh JP (2019) Using metagenomics to reveal landscape scale patterns of denitrifiers in a montane forest ecosystem. Soil Biol Biochem 138:107585

    Article  Google Scholar 

  • Rosi-Marshall EJ, Bernhardt ES, Buso DC, Driscoll CT, Likens GE (2016) Acid rain mitigation experiment shifts a forested watershed from a net sink to a net source of nitrogen. Proc Natl Acad Sci 113(27):7580–7583

    Article  Google Scholar 

  • Smith MS, Tiedje JM (1979) Phases of denitrification following oxygen depletion in soil. Soil Biol Biochem 11:262–267

    Article  Google Scholar 

  • Sorensen PO, Templer PH, Christenson L, Duran J, Fahey T, Fisk MC, Groffman PM, Morse JL, Finzi AC (2016) Reduced snow cover alters root-microbe interactions and decreases nitrification rates in a northern hardwood forest. Ecology 97(12):3359–3368

    Article  Google Scholar 

  • Sorensen PO, Bhatnagar JM, Christenson L, Duran J, Fahey T, Fisk MC, Finzi AC, Groffman PM, Morse JL, Templer PH (2019) Roots mediate the effects of snowpack decline on soil bacteria, fungi, and nitrogen cycling in a northern hardwood forest. Front Microbiol. https://doi.org/10.3389/fmicb.2019.00926

    Article  Google Scholar 

  • Sridevi G, Minocha R, Turlapati SA, Goldfarb KC, Brodie EL, Tisa LS, Minocha SC (2012) Soil bacterial communities of a calcium-supplemented and a reference watershed at the Hubbard Brook Experimental Forest (HBEF), New Hampshire, USA. FEMS Microbiol Ecol 79(3):728–740

    Article  Google Scholar 

  • van Breemen N, Mulder J, Driscoll CT (1983) Acidification and alkalinization of soils. Plant Soil 75(3):283–308

    Article  Google Scholar 

  • Voroney RP, Paul EA (1984) Determination of kc and kn in situ for calibration of the chloroform fumigation-incubation method. Soil Biol Biochem 16:9–14

    Article  Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  • Wickham H, François R (2022) dplyr: a grammar of data manipulation. https://dplyr.tidyverse.org, https://github.com/tidyverse/dplyr

  • Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L, Han W, Singh BK (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77(13):4618–4625

    Article  Google Scholar 

  • Zhalnina K, Dias R, de Quadros PD, Davis-Richardson A, Camargo FAO, Clark IM, McGrath SP, Hirsch PR, Triplett EW (2015) Soil pH determines microbial diversity and composition in the park grass experiment. Microb Ecol 69(2):395–406

    Article  Google Scholar 

  • Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61(4):533–616

    Google Scholar 

Download references

Funding

This research was supported by a Grant from the U.S. National Science Foundation Long-Term Ecological Research Program (Award # 1637685). We thank Lisa Martel for help with field, laboratory and data analysis and Clare Kohler for help with statistical analysis and graphing.

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Authors and Affiliations

  1. Department of Earth and Environmental Sciences, Brooklyn College of the City University of New York, Brooklyn, NY, 11210, USA

    Renata Ontman, Peter M. Groffman & Zhongqi Cheng

  2. City University of New York, Advanced Science Research Center at the Graduate Center, New York, NY, 10031, USA

    Peter M. Groffman

  3. Cary Institute of Ecosystem Studies, New York, NY, 12545, USA

    Peter M. Groffman

  4. Department of Civil and Environmental Engineering, Syracuse University, Syracuse, NY, 13244, USA

    Charles T. Driscoll

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  1. Renata Ontman
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  2. Peter M. Groffman
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Correspondence to Peter M. Groffman.

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Ontman, R., Groffman, P.M., Driscoll, C.T. et al. Surprising relationships between soil pH and microbial biomass and activity in a northern hardwood forest. Biogeochemistry 163, 265–277 (2023). https://doi.org/10.1007/s10533-023-01031-0

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