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The importance of amino sugar turnover to C and N cycling in organic horizons of old-growth Douglas-fir forest soils colonized by ectomycorrhizal mats

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An Erratum to this article was published on 20 September 2012

Abstract

Amino sugar dynamics represent an important but under-investigated component of the carbon (C) and nitrogen (N) cycles in old-growth Douglas-fir forest soils. Because fungal biomass is high in these soils, particularly in areas colonized by rhizomorphic ectomycorrhizal fungal mats, organic matter derived from chitinous cell wall material (or the monomeric building block of chitin, N-acetylglucosamine (NAG)) could be a significant source of C or N to the soil microbiota, and thus an important driver of microbial C and N processing. This paper reports the results of incubation experiments initiated to measure chitin degradation, NAG utilization, and the contribution of these substrates to soil respiration and N mineralization rates in mat-colonized and non-mat soil organic horizons. Amendments of chitin and NAG stimulated respiration, N mineralization, and biomass accumulation in mat and non-mat soils, and responses to NAG amendment were stronger than to chitin amendment. NAG-induced respiration was consistently two-fold higher in mat soils than non-mat soils, but induced N mineralization was similar between the two soil patch types. Assimilation of both C and N into microbial biomass was apparent, biomass C:N ratio decreased in all treatments, and microbial N use efficiency (treatment means 0.25 ± 0.06–0.50 ± 0.05) was greater than C use efficiency (treatment means 0.12 ± 0.04–0.32 ± 0.02). NAGase enzyme response was non-linear and showed the same pattern in chitin and NAG amendments. Responses to NAG and chitin amendment differed between mat and non-mat soils, indicating different mechanisms driving NAG and chitin utilization or differences in saprotrophic community composition between the two soil patch types. Net chitin and NAG processing rates were 0.08–3.4 times the basal respiration rates and 0.07–14 times the ambient net N mineralization rates, high enough for the turnover of total soil amino sugars to potentially occur in days to weeks. The results support the hypotheses that amino sugars are important microbial C and N sources and drivers of C and N cycling in these soils.

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References

  • Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37(5):937–944

    Article  Google Scholar 

  • Amelung W (2001) Methods using amino sugars as markers for microbial residues in soil. In: Lai R, Kimble JM, Follett RF, Stewart BA (eds) Assessment methods for soil carbon. CRC Press LLC, Boca Raton

    Google Scholar 

  • Amelung W (2003) Nitrogen biomarkers and their fate in soil. J Plant Nutr Soil Sci 166(6):677–686

    Article  Google Scholar 

  • Amelung W, Kimble JM, Samson-Liebig S, Follett RF (2001) Restoration of microbial residues in soils of the conservation reserve program. Soil Sci Soc Am J 65(6):1704–1709

    Article  Google Scholar 

  • Andersson M, Kjoller A, Struwe S (2004) Microbial enzyme activities in leaf litter, humus and mineral soil layers of European forests. Soil Biol Biochem 36(10):1527–1537

    Article  Google Scholar 

  • Baldrian P (2009) Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs? Oecologia 161(4):657–660

    Article  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  Google Scholar 

  • Bowman SM, Free SJ (2006) The structure and synthesis of the fungal cell wall. BioEssays 28(8):799–808

    Article  Google Scholar 

  • Brant JB, Myrold DD, Sulzman EW (2006) Root controls on soil microbial community structure in forest soils. Oecologia 148(4):650–659

    Article  Google Scholar 

  • Bremner JM (1954) Studies on the estimation and decomposition of amino sugars in soil. J Agric Sci 44:152

    Article  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen—a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17(6):837–842

    Article  Google Scholar 

  • Cromack K, Sollins P, Graustein WC, Speidel K, Todd AW, Spycher G, Li CY, Todd RL (1979) Calcium-oxalate accumulation and soil weathering in mats of the hypogeous fungus Hysterangium crassum. Soil Biol Biochem 11(5):463–468

    Article  Google Scholar 

  • Decock C, Denef K, Bode S, Six J, Boeckx P (2009) Critical assessment of the applicability of gas chromatography-combustion-isotope ratio mass spectrometry to determine amino sugar dynamics in soil. Rapid Commun Mass Spectrom 23(8):1201–1211

    Article  Google Scholar 

  • Dimitriu PA, Prescott CE, Quideau SA, Grayston SJ (2010) Impact of reclamation of surface-mined boreal forest soils on microbial community composition and function. Soil Biol Biochem 42(12):2289–2297

    Article  Google Scholar 

  • Dixon JJ (2003) Applying GIS to soil-geomorphic landscape mapping in the Lookout Creek valley, Western Cascades, Oregon. Master’s Thesis, Department of Crop and Soil Sciences. Oregon State University, Corvallis

  • Doi H, Cherif M, Iwabuchi T, Katano I, Stegen JC, Striebel M (2010) Integrating elements and energy through the metabolic dependencies of gross growth efficiency and the threshold elemental ratio. Oikos 119(5):752–765

    Google Scholar 

  • Dunham SM, Larsson KH, Spatafora JW (2007) Species richness and community composition of mat-forming ectomycorrhizal fungi in old- and second-growth Douglas-fir forests of the HJ Andrews Experimental Forest, Oregon, USA. Mycorrhiza 17(8):633–645

    Article  Google Scholar 

  • Duo-Chuan L (2006) Review of fungal chitinases. Mycopathologia 161(6):345–360

    Article  Google Scholar 

  • Felse PA, Panda T (1999) Regulation and cloning of microbial chitinase genes. Appl Microbiol Biotechnol 51(2):141–151

    Article  Google Scholar 

  • Finlay RD, Frostegard A, Sonnerfeldt AM (1992) Utilization of organic and inorganic nitrogen sources by ectomycorrhizal fungi in pure culture and in symbiosis with Pinus contorta dougl ex. loud. New Phytol 120(1):105–115

    Article  Google Scholar 

  • Geisseler D, Horwath WR, Joergensen RG, Ludwig B (2010) Pathways of nitrogen utilization by soil microorganisms—a review. Soil Biol Biochem 42(12):2058–2067

    Article  Google Scholar 

  • Griffiths RP, Caldwell BA, Cromack K, Morita RY (1990) Douglas-fir forest soils colonized by ectomycorrhizal mats. 1. Seasonal-variation in nitrogen chemistry and nitrogen-cycle transformation rates. Can J For Res 20(2):211–218

    Google Scholar 

  • Griffiths RP, Castellano MA, Caldwell BA (1991a) Hyphal mats formed by 2 ectomycorrhizal fungi and their association with Douglas-fir seedlings—a case-study. Plant Soil 134(2):255–259

    Article  Google Scholar 

  • Griffiths RP, Ingham ER, Caldwell BA, Castellano MA, Cromack K (1991b) Microbial characteristics of ectomycorrhizal mat communities in Oregon and California. Biol Fertil Soils 11(3):196–202

    Article  Google Scholar 

  • Griffiths RP, Bradshaw GA, Marks B, Lienkaemper GW (1996) Spatial distribution of ectomycorrhizal mats in coniferous forests of the Pacific Northwest, USA. Plant Soil 180(1):147–158

    Article  Google Scholar 

  • Guggenberger G, Frey SD, Six J, Paustian K, Elliott ET (1999) Bacterial and fungal cell-wall residues in conventional and no-tillage agroecosystems. Soil Sci Soc Am J 63(5):1188–1198

    Article  Google Scholar 

  • Hart SC, Stark JM (1997) Nitrogen limitation of the microbial biomass in an old-growth forest soil. Ecoscience 4(1):91–98

    Google Scholar 

  • Herron PM, Stark JM, Holt C, Hooker T, Cardon ZG (2009) Microbial growth efficiencies across a soil moisture gradient assessed using C-13-acetic acid vapor and N-15-ammonia gas. Soil Biol Biochem 41(6):1262–1269

    Article  Google Scholar 

  • Kirchman DL, White J (1999) Hydrolysis and mineralization of chitin in the Delaware Estuary. Aquat Microb Ecol 18(2):187–196

    Article  Google Scholar 

  • Kluber LA, Tinnesand KM, Caldwell BA, Dunham SM, Yarwood RR, Bottomley PJ, Myrold DD (2010) Ectomycorrhizal mats alter forest soil biogeochemistry. Soil Biol Biochem 42(9):1607–1613

    Article  Google Scholar 

  • Kluber LA, Smith JE, Myrold DD (2011) Distinctive fungal and bacterial communities are associated with mats formed by ectomycorrhizal fungi. Soil Biol Biochem 43(5):1042–1050

    Article  Google Scholar 

  • Lengeler J, Drews G, Schlegel H (1999) Biology of the prokaryotes. Georg Thieme, Stuttgart

    Google Scholar 

  • Means JE, Macmillan PC, Cromack K (1992) Biomass and nutrient content of Douglas-fir logs and other detrital pools in an old-growth forest, Oregon, USA. Can J For Res 22(10):1536–1546

    Article  Google Scholar 

  • Miller M, Palojarvi A, Rangger A, Reeslev M, Kjoller A (1998) The use of fluorogenic substrates to measure fungal presence and activity in soil. Appl Environ Microbiol 64(2):613–617

    Google Scholar 

  • Niemi RM, Vepsalainen M, Erkomaa K, Ilvesniemi H (2007) Microbial activity during summer in humus layers under Pinus silvestris and Alnus incana. For Ecol Manage 242(2–3):314–323

    Article  Google Scholar 

  • Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49(2):175–190

    Article  Google Scholar 

  • Parham JA, Deng SP (2000) Detection, quantification and characterization of beta-glucosaminidase activity in soil. Soil Biol Biochem 32(8–9):1183–1190

    Article  Google Scholar 

  • Phillips CL, Kluber LA, Martin J, Caldwell BA, Bond BJ (2012) Contributions of ectomycorrhizal fungal mats to forest soil respiration. Biogeosciences 9:1635–1666. doi:10.5194/bgd-9-1635-2012

    Article  Google Scholar 

  • Roberts P, Bol R, Jones DL (2007) Free amino sugar reactions in soil in relation to soil carbon and nitrogen cycling. Soil Biol Biochem 39(12):3081–3092

    Article  Google Scholar 

  • Rodriguez-Kabana R, Godoy G, Morganjones G, Shelby RA (1983) The determination of soil chitinase activity—conditions for assay and ecological-studies. Plant Soil 75(1):95–106

    Article  Google Scholar 

  • Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563

    Article  Google Scholar 

  • Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60(1):1–24

    Article  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusak D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    Google Scholar 

  • Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70(2):555–569

    Article  Google Scholar 

  • Sollins P, Grier CC, McCorison FM, Cromack K, Fogel R (1980) The internal element cycles of an old-growth Douglas-fir ecosystem in western Oregon. Ecol Monogr 50(3):261–285

    Article  Google Scholar 

  • Stevenson FJ (1982) Organic forms of soil nitrogen. In: Stevenson FJ (ed) Nitrogen in agricultural soils, vol 22. ASA, CSSA, pp 67–122

    Google Scholar 

  • Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22(6):955–963

    Article  Google Scholar 

  • Thiet RK, Frey SD, Six J (2006) Do growth yield efficiencies differ between soil microbial communities differing in fungal: bacterial ratios? Reality check and methodological issues. Soil Biol Biochem 38(4):837–844

    Article  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19(6):703–707

    Article  Google Scholar 

  • Vignon C, Plassard C, Mousain D, Salsac L (1986) Assay of fungal chitin and estimation of mycorrhizal infection. Physiol Veg 24(2):201–207

    Google Scholar 

  • Wallenstein MD, Weintraub MN (2008) Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol Biochem 40(9):2098–2106

    Article  Google Scholar 

  • Zeglin LH, Stursova M, Sinsabaugh RL, Collins SL (2007) Microbial responses to nitrogen addition in three contrasting grassland ecosystems. Oecologia 154(2):349–359

    Article  Google Scholar 

  • Zhang XD, Amelung W (1996) Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biol Biochem 28(9):1201–1206

    Article  Google Scholar 

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Acknowledgments

The H. J. Andrews Experimental Forest and LTER personnel provided site access and collaborative energy, and Rockie Yarwood, Elizabeth Brewer, Calvin Elser and Michele Noble provided valuable laboratory advice and/or assistance. Bruce Caldwell and Bob Sinsabaugh contributed thoughtful discussion on the experimental results, Peter Bottomley provided constructive feedback on the experiments, data and manuscript, and the manuscript was improved by the thoughtful comments of two anonymous reviewers. This project was funded by NSF Grant No. 0348689 to DDM.

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  1. Department of Crop and Soil Sciences, Oregon State University, 3017 Agriculture and Life Sciences Building, Corvallis, OR, 97331, USA

    Lydia H. Zeglin, Laurel A. Kluber & David D. Myrold

  2. Department of Biology, Case Western Reserve University, Cleveland, OH, 44106, USA

    Laurel A. Kluber

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  1. Lydia H. Zeglin
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  2. Laurel A. Kluber
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Correspondence to Lydia H. Zeglin.

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Zeglin, L.H., Kluber, L.A. & Myrold, D.D. The importance of amino sugar turnover to C and N cycling in organic horizons of old-growth Douglas-fir forest soils colonized by ectomycorrhizal mats. Biogeochemistry 112, 679–693 (2013). https://doi.org/10.1007/s10533-012-9746-8

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