Skip to main content
SpringerLink
Log in

Soil microbial community responses to altered lignin biosynthesis in Populus tremuloides vary among three distinct soils

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

The development and use of transgenic plants has steadily increased, but there are still little data about the responses of soil microorganisms to these genetic modifications. We utilized a greenhouse trial approach to evaluate the effects of altered stem lignin in trembling aspen (Populus tremuloides) on soil microbial communities in three soils which differed in their chemical and physical properties; they included a sandy loam (CO-Colorado), a silt loam (KS-Kansas), and a clay loam (TX-Texas). Three transgenic aspen lines were developed from a natural clone common to the Great Lakes region of North America. The concentrations of stem lignin concentrations were reduced by 35% (Line 23), 40% (Line 141) and 50% (Line 72). Line 72 and Line 141 also had a 40 and 20% increase in syringyl-type stem lignin, respectively. Indirectly, these modifications resulted in increased (5–13%) and decreased (−5 to −57%) levels of root production across the lines and soil types. Responses of the soil microbial communities were investigated using: phospholipid fatty acids (PLFA), neutral lipid fatty acids (NLFA), and 3) extracellular enzyme assays. PLFA analyses indicated that there were large differences in microbial community composition between the three soils. Similarly, there were large differences in total NLFA between soils, with the KS soils having the highest amount and CO the lowest. Enzyme activities did not differ between soils, except for cellubiohydrolase, which was highest in CO soil. Across all three soils, responses to the four genetic lines were not consistent. Interactions between soil type and genetic line make it difficult to assess the potential ecological impacts of transgenic aspen on soil microbial communities and their associated functions. Given these interactions, field trials with transgenic aspen should encompass the wide range of soils targeted for commercial planting in order to determine their effect(s) on the resident soil microbial community.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Amthor JS (2003) Efficiency of lignin biosynthesis: a quantitative analysis. Ann Bot 9:673–695

    Article  CAS  Google Scholar 

  • Anderson LJ, Maherali H, Johnson HB, Polley HW, Jackson RB (2001) Gas exchange and photosynthetic acclimation over subambient to elevated CO2 in a C3-C4 grassland. Glob Change Biol 7:693–707

    Article  Google Scholar 

  • Bååth E (2003) The use of neutral lipid fatty acids to indicate the physiological conditions of soil fungi. Microbial Ecol 45:373–383

    Article  CAS  Google Scholar 

  • Balser TC, Treseder KK, Ekenler M (2005) Using lipid analysis and hyphal length to quantify AM and saprotrophic fungal abundance along a soil chronosequence. Soil Biol Biochem 37:601–604

    Article  CAS  Google Scholar 

  • Bardgett RD, Lovell RD, Hobbs PJ, Jarvis SC (1999a) Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biol Biochem 31:1021–1030

    Article  CAS  Google Scholar 

  • Bardgett RD, Mawdsley JL, Edwards S, Hobbs PJ, Rodwell JS, Davies WJ (1999b) Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Funct Ecol 13:650–660

    Article  Google Scholar 

  • Barnes BV, Wagner WH (2004) Michigan trees. University of Michigan Press, Ann Arbor, MI. 447 p

    Google Scholar 

  • Belnap J, Phillips SL (2001) Soil biota in an ungrazed grassland: response to annual grass (Bromus tectorum) invasion. Ecol Appl 11:1261–1275

    Google Scholar 

  • Blair JM, Parmelee RW, Beare MH (1990) Decay rates, nitrogen fluxes, and decomposer communities of single- and mixed-species foliar litter. Ecology 71:1976–1985

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bouma TJ, Bryla DR (2000) On the assessment of root and soil respiration for soils of different textures: interactions with soil moisture contents and soil CO2 concentrations. Plant Soil 227:215–221

    Article  CAS  Google Scholar 

  • Bouyoucos GJ (1962) Hydrometer method improved for making particle size analysis of soils. Agron J 54:464–465

    Article  Google Scholar 

  • Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9:49–56

    Article  PubMed  CAS  Google Scholar 

  • Collins PJ, Dobson ADW (1997) Generation of species specific DNA probes for the lignin peroxidase genes of white rot fungi. In: Sheehan D (ed) Bioremediation protocols. Humana Press, Totowa, NJ

    Google Scholar 

  • Cox MS, Gerard PD, Abshire MJ (2006) Selected soil properties’ variability and their relationships with yield in three Mississippi fields. Soil Sci 171:541–551

    Article  CAS  Google Scholar 

  • Coyne MS (1999) Soil microbiology: an exploratory approach. Delmar Publishers, Albany, NY. 462 p

    Google Scholar 

  • DeForest JL, Zak DR, Pregitzer KS, Burton AJ (2004) Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Sci Soc Am J 68:132–138

    CAS  Google Scholar 

  • Fang C, Radosevich M, Fuhrmann JJ (2001) Characterization of rhizopshere microbial community structure in five similar grass species using FAME and BIOLOG analyses. Soil Biol Biochem 33:679–682

    Article  CAS  Google Scholar 

  • Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fert Soils 22:59–65

    Google Scholar 

  • Frostegård Å, Tunlid A, Bååth E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Methods 14:151–163

    Article  Google Scholar 

  • Giardina CP, Ryan MG, Hubbard RM, Binkley D (2001) Tree species and soil textural controls on carbon and nitrogen mineralization rates. Soil Sci Soc Am J 65:1272–1279

    Article  CAS  Google Scholar 

  • Grayston SJ, Griffith GS, Mawdsley JL, Campbell CD, Bardgett RD (2001) Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol Biochem 33:533–551

    Article  CAS  Google Scholar 

  • Halpin C, Thain SC, Tilston EL, Guiney E, Lapierre C, Hopkins DW (2007) Ecological impacts of trees with modified lignin. Tree Genetics & Genomes 3:101–110

    Article  Google Scholar 

  • Hancock JE, Loya WM, Giardina CP, Li L, Chiang VL, Pregitzer KS (2007) Plant growth, biomass partitioning and soil carbon formation in response to altered lignin biosynthesis in Populus tremuloides. New Phytol 173:732–742

    Article  PubMed  CAS  Google Scholar 

  • Hart SC, Nason GE, Myrold DD, Perry DA (1994) Dynamics of gross nitrogen transformation in an old-growth forest: the carbon connection. Ecology 75: 880–891

    Article  Google Scholar 

  • Hassett JE, Zak DR (2005) Aspen harvest intensity decreases microbial biomass, extracellular enzyme activity, and soil nitrogen cycling. Soil Sci Soc Am J 69:227–235

    Article  CAS  Google Scholar 

  • Hénault C, English LC, Halpin C, Andreux F, Hopkins DW (2006) Microbial community structure in soils with decomposing residues from plants with genetic modifications to lignin biosynthesis. FEMS Microbiol Lett 263:68–75

    Article  PubMed  CAS  Google Scholar 

  • Herrera S (2005) Struggling to see the forest through the trees. Nat Biotechnol 23:165–167

    Article  PubMed  CAS  Google Scholar 

  • Hobbie SE, Reich PB, Oleksyn J, Ogdahl M, Zytkowiak R, Hale C, Karolewski P (2006) Tree species effects on decomposition and forest floor dynamics in a common garden. Ecology 87:2288–2297

    Article  PubMed  Google Scholar 

  • Hu WJ, Harding SA, Lung J, Popko JL, Ralph J, Stokke DD, Tsai CJ, Chiang VL (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nature Biotechnol 17:808–812

    Article  CAS  Google Scholar 

  • Karnosky DF, Gagnon ZE, Dickson RE, Coleman MD, Lee EH, Isebrands JG (1996) Changes in growth, leaf abscission, and biomass associated with seasonal tropospheric ozone exposures of Populus tremuloides clones and seedlings. Can J For Res-Rev Can Rech For 26:23–37

    CAS  Google Scholar 

  • Knops JMH, Bradley KL, Wedin DA (2002) Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol Lett 5:454–466

    Article  Google Scholar 

  • Larson JL, Zak DR, Sinsabaugh RL (2002) Extracellular enzyme activity beneath temperate trees growing under elevated carbon dioxide and ozone. Soil Sci Soc Am J 66:1848–1856

    Article  CAS  Google Scholar 

  • Li L, Popko JL, Umezawa T, Chiang VL (2000) 5-Hydroxyconiferyl aldehyde modulates enzymatic methylation for syringyl monolignol formation, a new view of monolignol biosynthesis in angiosperms. J Biol Chem 275:6537–6545

    Article  PubMed  CAS  Google Scholar 

  • Li L, Zhou Y, Cheng X, Sun J, Marita JM, Ralph J, Chiang VL (2003) Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc Natl Acad Sci USA 100:4939–4944

    Article  PubMed  CAS  Google Scholar 

  • Littell RC, Stroup WW, Freund RJ (2002) SAS for linear models. SAS Institute Inc., Cary, NC. 466 p

    Google Scholar 

  • Lorenz K, Lal R (2005) The depth distribution of soil organic carbon in relation to land use and management and the potential of carbon sequestration in subsoil horizons. In Advances in Agronomy, vol 88, pp 35–66

  • Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577

    Article  PubMed  CAS  Google Scholar 

  • Madritch M, Donaldson JR, Lindroth RL (2006) Genetic identity of Populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems 9:529–537

    Article  CAS  Google Scholar 

  • Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445

    Article  CAS  Google Scholar 

  • Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C, Leple JC, Pollet B, Mila I, Webster EA, Marstorp HG, Hopkins DW, Jouanin L, Boerjan W, Schuch W, Cornu D, Halpin C (2002) Field and pulping performances of transgenic trees with altered lignification. Nat Biotechnol 20:607–612

    Article  PubMed  CAS  Google Scholar 

  • Ruess L, Tiunov A, Haubert D, Richnow HH, Haggblom MM, Scheu S (2005) Carbon stable isotope fractionation and trophic transfer of fatty acids in fungal based soil food chains. Soil Biol Biochem 37:945–953

    Article  CAS  Google Scholar 

  • SAS (1999) SAS/STAT® User’s Guide, Version 8. SAS Institute Inc., Cary, NC

    Google Scholar 

  • Schweitzer JA, Bailey JK, Rehill BJ, Martinsen GD, Hart SC, Lindroth RL, Keim P, Whitham TG (2004) Genetically based trait in a dominant tree affects ecosystem processes. Ecol Lett 7:127–134

    Article  Google Scholar 

  • Sinsabaugh RL, Gallo ME, Lauber C, Waldrop MP, Zak DR (2005) Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75:201–215

    Article  CAS  Google Scholar 

  • Six J, Feller C, Denef K, Ogle S, Sa JCM, Albrecht A (2002) Organic matter, biota and aggregation in temperate and tropical soils – Effects of no-tillage. Agronomie: Agric Environ 22:755–775

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

    Article  CAS  Google Scholar 

  • Tilston EL, Halpin C, Hopkins DW (2004) Genetic modifications to lignin biosynthesis in field-grown poplar trees have inconsistent effects on the rate of woody trunk decomposition. Soil Biol Biochem 36:1903–1906

    Article  CAS  Google Scholar 

  • Tsai C-J, Podila GK, Chiang VL (1994) Agrobacterium-mediated transformation of quaking aspen (Populus tremuloides) and regeneration of transgenic plants. Plant Cell Reports 14:94–97.

    Article  CAS  Google Scholar 

  • van Aarle IM, Olsson PA (2003) Fungal lipid accumulation and development of mycelial structures by two arbuscular mycorrhizal fungi. Appl Environ Microbiol 69:6762–6767

    Article  PubMed  CAS  Google Scholar 

  • Waldrop MP, Firestone MK (2006) Response of microbial community composition and function to soil climate change. Microbial Ecol 52:716–724

    Article  CAS  Google Scholar 

  • Webster EA, Halpin C, Chudek JA, Tilston EL, Hopkins DW (2005) Decomposition in soil of soluble, insoluble and lignin-rich fractions of plant material from tobacco with genetic modifications to lignin biosynthesis. Soil Biol Biochem 37:751–760

    Article  CAS  Google Scholar 

  • Weltzin JF, Loik ME, Schwinning S, Williams DG, Fay PA, Haddad BM, Harte J, Huxman TE, Knapp AK, Lin GH, Pockman WT, Shaw MR, Small EE, Smith MD, Smith SD, Tissue DT, Zak JC (2003) Assessing the response of terrestrial ecosystems to potential changes in precipitation. Bioscience 53:941–952

    Article  Google Scholar 

  • Zak DR, Blackwood CB, Waldrop MP (2006) A molecular dawn for biogeochemistry. Trends Ecol Evol 21:288–295

    Article  PubMed  Google Scholar 

  • Zak DR, Tilman D, Parmenter RR, Rice CW, Fisher FM, Vose J, Milchunas D, Martin CW (1994) Plant production and soil microorganisms in late-successional ecosystems: a continental-scale study. Ecology 75:2333–2347

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River, N. J

    Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

    Article  CAS  Google Scholar 

  • Zelles L, Bai GY, Beck T, Beese F (1992) Signature fatty acids in phospholipids and lipopolysaccharides as indicators of microbial biomass and community structure in agricultural soils. Soil Biol Biochem 24:317–323

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Cassie Miller for her assistance in the greenhouse and the lab, and Joe Bump, Alan Talhelm, and two anonymous reviewers for comments on earlier versions of this manuscript. We thank the Central Plains Experimental Range, Konza Prairie Biological Station, and the Blackland Research and Extension Center in Temple, Texas, for access to soils used in this experiment. This work was funded by the US Department of Energy BER, the North Central Research Station of the USDA Forest Service, and the graduate school of Michigan Technological University.

Author information

Authors and Affiliations

  1. Ecosystem Science Center, School of Forest Resources and Environmental Science, Michigan Technological University, 1400 Townsend Drive, Houghton, MI, 49931, USA

    Kate L. Bradley, Jessica E. Hancock & Kurt S. Pregitzer

  2. USDA Forest Service, North Central Research Station, 410 MacInnes Drive, Houghton, MI, 49931, USA

    Jessica E. Hancock

  3. Institute of Pacific Islands Forestry - USDA Forest Service, PSW Research Station 60 Nowelo Street, Hilo, HA, 96720, USA

    Christian P. Giardina

Authors
  1. Kate L. Bradley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jessica E. Hancock
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian P. Giardina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kurt S. Pregitzer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kate L. Bradley.

Additional information

Responsible Editor: Barbara Wick

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bradley, K.L., Hancock, J.E., Giardina, C.P. et al. Soil microbial community responses to altered lignin biosynthesis in Populus tremuloides vary among three distinct soils. Plant Soil 294, 185–201 (2007). https://doi.org/10.1007/s11104-007-9246-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-007-9246-0

Keywords

Search

Navigation