Soil microbial communities respond differently to three chemically defined polyphenols

Plant Physiology and Biochemistry

Volumn 72, Issue , 2013, Pages 190-197

  Schmidt, Michael A ^a,c   Kreinberg, Allison J ^a   Gonzalez, Javier M ^b   Halvorson, Jonathan J ^b   French, Elizabeth ^a   Bollmann, Annette ^a   Hagerman, Ann E ^a  

^a MIAMI UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c LAKE ERIE COLLEGE OF OSTEOPATHIC MEDICINE   (United States)

Author keywords

Ammonia oxidizing species; AOX; Community level physiological profiling (CLPP); Denaturing gradient gel electrophoresis (DGGE); Microresp ; Soil nitrogen cycle; Tannin

Indexed keywords

ARCHAEA; BACTERIA (MICROORGANISMS);

EPIGALLOCATECHIN GALLATE; POLYPHENOL; TANNIN; TANNIN DERIVATIVE;

AMMONIA MONOOXYGENASE GENE; AMMONIA OXIDIZING SPECIES; AMMONIA-OXIDIZING ARCHAEA; AMMONIA-OXIDIZING BACTERIA; AMO-A; AOA; AOB; AOX; ARCHAEON; ARTICLE; BACTERIUM; CHEMISTRY; CLPP; COMMUNITY LEVEL PHYSIOLOGICAL PROFILING; COMMUNITY LEVEL PHYSIOLOGICAL PROFILING (CLPP); DENATURING GRADIENT GEL ELECTROPHORESIS; DENATURING GRADIENT GEL ELECTROPHORESIS (DGGE); DGGE; DRUG EFFECT; EGCG; MICROBIOLOGY; MICRORESP™; QPCR; R(0); REAL TIME QUANTITATIVE POLYMERASE CHAIN REACTION; SOIL NITROGEN CYCLE; STARTING FLUORESCENCE;

AMMONIA MONOOXYGENASE GENE; AMMONIA OXIDIZING SPECIES; AMMONIA-OXIDIZING ARCHAEA; AMMONIA-OXIDIZING BACTERIA; AMO-A; AOA; AOB; AOX; CLPP; COMMUNITY LEVEL PHYSIOLOGICAL PROFILING; COMMUNITY LEVEL PHYSIOLOGICAL PROFILING (CLPP); DENATURING GRADIENT GEL ELECTROPHORESIS; DENATURING GRADIENT GEL ELECTROPHORESIS (DGGE); DGGE; EGCG; EPIGALLOCATECHIN GALLATE; MICRORESP™; QPCR; R(0); REAL TIME QUANTITATIVE POLYMERASE CHAIN REACTION; SOIL NITROGEN CYCLE; STARTING FLUORESCENCE; TANNIN;

ARCHAEA; BACTERIA; POLYPHENOLS; SOIL MICROBIOLOGY; TANNINS;

EID: 84886585349     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2013.03.003     Document Type: Article

References (65)

1. Bossio D.A., Scow K.M., Gunapala N., Graham K.J. Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb. Ecol. 1998, 36:1-12.
2. Sheik C.S., Beasley W.H., Elshahed M.S., Zhou X.H., Luo Y.Q., Krumholz L.R. Effect of warming and drought on grassland microbial communities. ISME J. 2011, 5:1692-1700.
3. Butenschoen O., Scheu S., Eisenhauer N. Interactive effects of warming, soil humidity and plant diversity on litter decomposition and microbial activity. Soil Biol. Biochem. 2011, 43:1902-1907.
4. 2 vent. Geochim. Cosmochim. Acta 2010, 74:2697-2716.
5. Fan F., Yang Q., Li Z., Wei D., Cui X.a., Liang Y. Impacts of organic and inorganic fertilizers on nitrification in a cold climate soil are linked to the bacterial ammonia oxidizer community. Microb. Ecol. 2011, 62:982-990.
6. Marschner P., Kandeler E., Marschner B. Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol. Biochem. 2003, 35:453-461.
7. Schweitzer J.A., Fischer D.G., Rehill B.J., Wooley S.C., Woolbright S.A., Lindroth R.L., Whitham T.G., Zak D.R., Hart S.C. Forest gene diversity is correlated with the composition and function of soil microbial communities. Popul. Ecol. 2011, 53:35-46.
8. Kraus T.E.C., Dahlgren R.A., Zasoski R.J. Tannins in nutrient dynamics of forest ecosystems - a review. Plant Soil 2003, 256:41-66.
9. Quideau S., Deffieux D., Douat-Casassus C., Pouysegu L. Plant polyphenols: chemical properties, biological activities, and synthesis. Angew. Chem. Int. Ed. 2011, 50:586-621.
10. Yoshida T., Hatano T., Ito H. High molecular weight plant polyphenols (tannins): prospective functions. Chemical Ecology and Phytochemistry of Forest Ecosystems 2005, 163-190. Elsevier Inc., San Diego, CA, USA. J.T. Romeo (Ed.).
11. Scioneaux A.N., Schmidt M.A., Moore M.A., Lindroth R.L., Wooley S.C., Hagerman A.E. Qualitative variation in proanthocyanidin composition of Populus species and hybrids: genetics is the key. J.Chem. Ecol. 2011, 37:57-70.
12. Salminen J.-P., Roslin T., Karonen M., Sinkkonen J., Pihlaja K., Pulkkinen P. Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. J.Chem. Ecol. 2004, 30:1693-1711.
13. Schweitzer J.A., Madritch M.D., Bailey J.K., LeRoy C.J., Fischer D.G., Rehill B.J., Lindroth R.L., Hagerman A.E., Wooley S.C., Hart S.C., Whitham T.G. From genesto ecosystems: the genetic basis of condensed tannins and their role innutrient regulation in a Populus model system. Ecosystems 2008, 11:1005-1020.
14. Hattenschwiler S., Hagerman A., Vitousek P. Polyphenols in litter from tropical Montane forests across a wide range in soil fertility. Biogeochemistry 2003, 64:129-148.
15. Rice E.L., Pancholy S.K. Inhibition of nitrification by climax ecosystems. IIAdditional evidence and possible role of tannins. Am. J. Bot. 1973, 60:691-702.
16. Talbot J.M., Finzi A.C. Differential effects of sugar maple, red oak, and hemlock tannins on carbon and nitrogen cycling in temperate forest soils. Oecologia 2008, 155:583-592.
17. Baptist F., Zinger L., Clement J.C., Gallet C., Guillemin R., Martins J.M.F., Sage L., Shahnavez B., Choler P., Geremia R. Tannin impacts on microbial diversity and the functioning of alpine soils: a multidisciplinary approach. Environ. Microbiol. 2008, 10:799-809.
18. Bais H.P., Walker T.S., Stermitz F.R., Hufabauer R.A., Vivanco J.M. Enantiomeric-dependent phytotoxic and antimicrobial activity of (+/-)-catechin. A rhizosecreted racemic mixture from spotted knapweed. Plant Physiol. 2002, 128:1173-1179.
19. Scalbert A. Antimicrobial properties of tannins. Phytochemistry 1991, 30:3875-3883.
20. Kraal P., Nierop K.G.J., Kaal J., Tietema A. Carbon respiration and nitrogen dynamics in Corsican pine litter amended with aluminium and tannins. Soil Biol. Biochem. 2009, 41:2318-2327.
21. Norris C.E., Preston C.M., Hogg K.E., Titus B.D. The influence of condensed tannin structure on rate of microbial mineralization and reactivity to chemical assays. J.Chem. Ecol. 2011, 37:311-319.
22. Smolander A., Kanerva S., Adamczyk B., Kitunen V. Nitrogen transformations in boreal forest soils-does composition of plant secondary compounds give any explanations?. Plant Soil 2012, 350:1-26.
23. Halvorson J., Gonzalez J., Hagerman A.E. Changes in soluble-N in forest and pasture soils after repeated applications of tannins and related phenolic compounds. Int. J. Agron. 2012, 10.1155/2012/163054.
24. Schmidt M., Halvorson J., Gonzalez J., Hagerman A. Kinetics and binding capacity of six soils for structurally defined hydrolyzable and condensed tannins and related phenols. J.Soils Sed. 2012, 12:366-375.
25. Hagerman A.E. Fifty years of polyphenol-protein complexes. Recent Adv. Polyphenol Res. 2012, 3:71-97.
26. Verkaik E., Jongkind A.G., Berendse F. Short-term and long-term effects of tannins on nitrogen mineralisation and litter decomposition in kauri (Agathis australis (D. Don) Lindl.) forests. Plant Soil 2006, 287:337-345.
27. Joanisse G.D., Bradley R.L., Preston C.M. Do late-successional tannin-rich plant communities occurring on highly acidic soils increase the DON/DIN ratio. Biol. Fertil. Soils 2008, 44:903-907.
28. Joanisse G., Bradley R., Preston C., Bending G. Sequestration of soil nitrogen as tannin-protein complexes may improve the competitive ability of sheep laurel (Kalmia angustifolia) relative to black spruce (Picea mariana). New Phytol. 2009, 181:187-198.
29. 4 and condensed tannins extracted from Kalmia angustifolia and balsam fir. Soil Biol. 2000, 32:1227-1240.
30. Adamczyk B., Kitunen V., Smolander A. Polyphenol oxidase, tannase and proteolytic activity in relation to tannin concentration in the soil organic horizon under silver birch and Norway spruce. Soil Biol. Biochem. 2009, 41:2085-2093.
31. Joanisse G., Bradley R., Preston C., Munson A. Soil enzyme inhibition by condensed litter tannins may drive ecosystem structure and processes: the case of Kalmia angustifolia. New Phytol. 2007, 175:535-546.
32. Ollivier J., Toewe S., Bannert A., Hai B., Kastl E.-M., Meyer A., Su M.X., Kleineidam K., Schloter M. Nitrogen turnover in soil and global change. FEMS Microbiol. Ecol. 2011, 78:3-16.
33. Wurzburger N., Hendrick R.L. Rhododendron thickets alter N cycling and soil extracellular enzyme activities in southern Appalachian hardwood forests. Pedobiologia 2007, 50:563-576.
34. Wurzburger N., Hendrick R.L. Plant litter chemistry and mycorrhizal roots promote a nitrogen feedback in a temperate forest. J.Ecol. 2009, 97:528-536.
35. Nierop K.G.J., Preston C.M., Verstraten J.M. Linking the B ring hydroxylation pattern of condensed tannins to C, N and P mineralization. A case study using four tannins. Soil Biol. Biochem. 2006, 38:2794-2802.
36. Kraus T.E.C., Zasoski R.J., Dahlgren R.A., Horwath W.R., Preston C.M. Carbon and nitrogen dynamics in a forest soil amended with purified tannins from different plant species. Soil Biol. Biochem. 2004, 36:309-321.
37. Ammar H., Lopez S., Kammoun M., Bodas R., Giraldez F.J., Gonzalez J.S. Feeding quebracho tannins to sheep enhances rumen fermentative activity to degrade browse shrubs. Anim. Feed Sci. Technol. 2009, 149:1-15.
38. Campbell C.D., Chapman S.J., Cameron C.M., Davidson M.S., Potts J.M. Arapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl. Environ. Microbiol. 2003, 69:3593-3599.
39. Muyzer G., Dewaal E.C., Uitterlinden A.G. Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16s ribosomal-RNA. Appl. Environ. Microbiol. 1993, 59:695-700.
40. Inselsbacher E., Hinko-Najera Umana N., Stange F.C., Gorfer M., Schueller E., Ripka K., Zechmeister-Boltenstern S., Hood-Novotny R., Strauss J., Wanek W. Short-term competition between crop plants and soil microbes for inorganic N fertilizer. Soil Biol. Biochem. 2010, 42:360-372.
41. Fierer N., Schimel J.P., Cates R.G., Zou J. Influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils. Soil Biol. Biochem. 2001, 33:1827-1839.
42. Chapman S.J., Campbell C.D., Artz R.R.E. Assessing CLPPs using MicroResp: a comparison with Biolog and multi-SIR. J.Soils Sed. 2007, 7:406-410.
43. Tlili A., Marechal M., Montuelle B., Volat B., Dorigo U., Berard A. Use of the MicroResp (TM) method to assess pollution-induced community tolerance to metals for lotic biofilms. Environ. Pollut. 2011, 159:18-24.
44. 2 IRGA analysis and the Solvita gel system. Renew. Agric. Food Syst. 2008, 23:171-176.
45. Padmanabhan P., Padmanabhan S., DeRito C., Gray A., Gannon D., Snape J.R., Tsai C.S., Park W., Jeon C., Madsen E.L. Respiration of C-13-labeled substrates added to soil in the field and subsequent 16S rRNA gene analysis of C-13-labeled soil DNA. Appl. Environ. Microbiol. 2003, 69:1614-1622.
46. Dilly O. Microbial respiratory quotient during basal metabolism and after glucose amendment in soils and litter. Soil Biol. Biochem. 2001, 33:117-127.
47. Garland J.L. Analysis and interpretation of community-level physiological profiles in microbial ecology. FEMS Microbiol. Ecol. 1997, 24:289-300.
48. Garland J.L., Mills A.L. Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level soil-carbon utilization. Appl. Environ. Microbiol. 1991, 57:2351-2359.
49. Lalor B.M., Cookson W.R., Murphy D.V. Comparison of two methods that assess soil community level physiological profiles in a forest ecosystem. Soil Biol. Biochem. 2007, 39:454-462.
50. Degens B.P., Schipper L.A., Sparling G.P., Duncan L.C. Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance?. Soil Biol. Biochem. 2001, 33:1143-1153.
51. Krook M.A., Hagerman A.E. Stability of high molecular weight polyphenols in a simulated digestive system. Food Res. Int. 2012, 49:112-116.
52. Larkin R.P. Characterization of soil microbial communities under different potato cropping systems by microbial population dynamics, substrate utilization, and fatty acid profiles. Soil Biol. Biochem. 2003, 35:1451-1466.
53. Zhang C.-B., Wang J., Liu W.-L., Zhu S.-X., Ge H.-L., Chang S.X., Chang J., Ge Y. Effects of plant diversity on microbial biomass and community metabolic profiles in a full-scale constructed wetland. Ecol. Eng. 2010, 36:62-68.
54. Saleh-Lakha S., Miller M., Campbell R.G., Schneider K., Elahimanesh P., Hart M.M., Trevors J.T. Microbial gene expression in soil: methods, applications and challenges. J.Microbiol. Methods 2005, 63:1-19.
55. Hamer U., Marschner B. Priming effects in different soil types induced by fructose, alanine, oxalic acid and catechol additions. Soil Biol. Biochem. 2005, 37:445-454.
56. Nakatsu C.H. Soil microbial community analysis using denaturing gradient gel electrophoresis. Soil Sci. Soc. Am. J. 2007, 71:562-571.
57. Isobe K., Koba K., Otsuka S., Senoo K. Nitrification and nitrifying microbial communities in forest soils. J.For. Res. 2011, 16:351-362.
58. Mosier A.C., Francis C.A. Determining the distribution of marine and coastal ammonia-oxidizing archaea and bacteria using a quantitative approach. Methods Enzymol 2011, 205-221. Elsevier Academic Press Inc., San Diego. M.G. Klotz (Ed.).
59. Y. Zhao, Simultaneous Determination of Hydrolyzable Tannin and Condensed Tannin, in: MS Thesis in Chemistry & Biochemistry, Miami University, Oxford, OH, 1995.
60. Hagerman A.E. Tannin Handbook 2011, http://www.users.miamioh.edu/hagermae/.
61. Rotthauwe J.H., Witzel K.P., Liesack W. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl. Environ. Microbiol. 1997, 63:4704-4712.
62. Francis C.A., Roberts K.J., Beman J.M., Santoro A.E., Oakley B.B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:14683-14688.
63. Zwart G., Huismans R., van Agterveld M.P., Van de Peer Y., De Rijk P., Eenhoorn H., Muyzer G., van Hannen E.J., Gons H.J., Laanbroek H.J. Divergent members of the bacterial division Verrucomicrobiales in a temperate freshwater lake. FEMS Microbiol. Ecol. 1998, 25:159-169.
64. Garcia-Vallve S., Palau J., Romeu A. Horizontal gene transfer in glycosyl hydrolases inferred from codon usage in Escherichia coli and Bacillus subtilis. Mol. Biol. Evol. 1999, 16:1125-1134.
65. Zhao S., Fernald R.D. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J.Comput. Biol. 2005, 12:1047-1064.