Thermal acclimation of organic matter decomposition in an artificial forest soil is related to shifts in microbial community structure

Soil Biology and Biochemistry

Volumn 71, Issue , 2014, Pages 1-12

  Wei, Hui ^a,d   Guenet, Bertrand ^b   Vicca, Sara ^b   Nunan, Naoise ^c   AbdElgawad, Hamada ^b   Pouteau, Valérie ^c   Shen, Weijun ^a   Janssens, Ivan A ^b  

^a SOUTH CHINA INSTITUTE OF BOTANY   (China)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c CNRS   (France)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Acclimatization; Carbon cycling; Heterotrophic respiration; Microbial adaptation; Phospholipid fatty acids (PLFAs); Substrate availability; Temperate forest

Indexed keywords

ACCLIMATIZATION; CARBON CYCLING; HETEROTROPHIC RESPIRATION; MICROBIAL ADAPTATION; PHOSPHOLIPID FATTY ACIDS; SUBSTRATE AVAILABILITIES; TEMPERATE FORESTS;

BACTERIA; BIOGEOCHEMISTRY; BIOLOGICAL MATERIALS; CARBON; CARBON DIOXIDE; EXPERIMENTS; FORESTRY; GLOBAL WARMING; ORGANIC COMPOUNDS; PHOSPHOLIPIDS; REGRESSION ANALYSIS; SOCIAL SCIENCES;

SOILS;

ACCLIMATION; ADAPTATION; BACTERIUM; BIOMASS; CARBON CYCLE; CARBON DIOXIDE; COMMUNITY STRUCTURE; DECOMPOSITION; FOREST SOIL; FUNGUS; GLOBAL WARMING; MICROBIAL COMMUNITY; ORGANIC CARBON; ORGANIC MATTER; PHOSPHOLIPID; SOIL MICROORGANISM; SOIL ORGANIC MATTER; TEMPERATE FOREST; TEMPERATURE EFFECT;

BACTERIA; BIOCHEMISTRY; FATTY ACIDS; FORESTS; GEOCHEMISTRY; LIPIDS; ORGANIC COMPOUNDS; REGRESSION ANALYSIS; RESPIRATION; SOIL; SUBSTRATES;

EID: 84893138479     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2014.01.003     Document Type: Article

References (75)

1. Allison S.D., Wallenstein M.D., Bradford M.A. Soil-carbon response to warming dependent on microbial physiology. Nature Geoscience 2010, 3:336-340.
2. Baldrian P., Šnajdr J., Merhautová V., Dobiášová P., Cajthaml T., Valášková V. Responses of the extracellular enzyme activities in hardwood forest to soil temperature and seasonality and the potential effects of climate change. Soil Biology and Biochemistry 2013, 56:60-68.
3. Balser T.C., Wixon D.L. Investigating biological control over soil carbon temperature sensitivity. Global Change Biology 2009, 15:2935-2949.
4. Benini S., Rypniewski W.R., Wilson K.S., Miletti S., Ciurli S., Mangani S. Anew proposal for urease mechanism based on the crystal structures of the native and inhibited enzyme from Bacillus pasteurii: why urea hydrolysis costs two nickels. Structure 1999, 7:205-216.
5. Biasi C., Meyer H., Rusalimova O., Hammerle R., Kaiser C., Baranyi C., Daims H., Lashchinsky N., Barsukov P., Richter A. Initial effects of experimental warming on carbon exchange rates, plant growth and microbial dynamics of a lichen-rich dwarf shrub tundra in Siberia. Plant and Soil 2008, 307:191-205.
6. Biasi C., Rusalimova O., Meyer H., Kaiser C., Wanek W., Barsukov P., Junger H., Richter A. Temperature-dependent shift from labile to recalcitrant carbon sources of arctic heterotrophs. Rapid Communications in Mass Spectrometry 2005, 19:1401-1408.
7. Bossio D.A., Scow K.M. Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecology 1998, 35:265-278.
8. Bradford M.A., Davies C.A., Frey S.D., Maddox T.R., Melillo J.M., Mohan J.E., Reynolds J.F., Treseder K.K., Wallenstein M.D. Thermal adaptation of soil microbial respiration to elevated temperature. Ecology Letters 2008, 11:1316-1327.
9. Bradford M.A., Watts B.W., Davies C.A. Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Global Change Biology 2010, 16:1576-1588.
10. Boyer J.N., Groffman P.M. Bioavailability of water extractable organic carbon fractions in forest and agricultural soil profiles. Soil Biology and Biochemistry 1996, 28:783-790.
11. Burns R.G., DeForest J.L., Marxsen J., Sinsabaugh R.L., Stromberger M.E., Wallenstein M.D., Weintraub M.N., Zoppini A. Soil enzymes in a changing environment: current knowledge and future directions. Soil Biology & Biochemistry 2013, 58:216-234.
12. Castro H.F., Classen A.T., Austin E.E., Norby R.J., Schadt C.W. Soil microbial community responses to multiple experimental climate change drivers. Applied and Environmental Microbiology 2010, 76:999-1007.
13. Christ M.J., David M.B. Temperature and moisture effects on the production of dissolved organic carbon in a spodosol. Soil Biology & Biochemistry 1996, 28:1191-1199.
14. Conant R.T., Ryan M.G., Ågren G.I., Birge H.E., Davidson E.A., Eliasson P.E., Evans S.E., Frey S.D., Giardina C.P., Hopkins F.M., Hyvönen R., Kirschbaum M.U., Lavallee J.M., Leifeld J., Parton W.J., Sternweg J.M., Wallenstein M.D., Wetterstedt J.Ǻ.M., Bradford M.A. Temperature and soil organic matter decomposition rates - synthesis of current knowledge and a way forward. Global Change Biology 2011, 17:3392-3404.
15. Craine J., Spurr R., McLauchlan K., Fierer N. Landscape-level variation in temperature sensitivity of soil organic carbon decomposition. Soil Biology & Biochemistry 2010, 42:373-375.
16. Crowther T.W., Bradford M.A. Thermal acclimation in widespread heterotrophic soil microbes. Ecology Letters 2013, 16:469-477.
17. Crowther T.W., Littleboy A., Jones T.H., Boddy L. Interactive effects of warming and invertebrate grazing on the outcomes of competitive fungal interactions. FEMS Microbiology Ecology 2012, 81:419-426.
18. 2 efflux. Biogeochemistry 2010, 98:127-138.
19. Davidson E.A., Janssens I.A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 2006, 440:165-173.
20. 10. Global Change Biology 2006, 12:154-164.
21. DeForest J.L. The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and L-DOPA. Soil Biology & Biochemistry 2009, 41:1180-1186.
22. 2 and temperature. Global Change Biology 2012, 18:2681-2693.
23. 2 flux to soil warming. Global Change Biology 2005, 11:167-181.
24. Feng X.J., Simpson M.J. Temperature and substrate controls on microbial phospholipid fatty acid composition during incubation of grassland soils contrasting in organic matter quality. Soil Biology & Biochemistry 2009, 41:804-812.
25. Fishbein W.N., Carbone P.P. Urease catalysis II. Inhibition of the enzyme by hydroxyurea, hydroxylamine, and acetohydroxamic acid. Journal of Biological Chemistry 1965, 240:2407-2414.
26. Frey S.D., Drijber R., Smith H., Melillo J. Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biology & Biochemistry 2008, 40:2904-2907.
27. Frostegård Å., Bååth E., Tunlio A. Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biology & Biochemistry 1993, 25:723-730.
28. Guenet B., Leloup J., Hartmann C., Barot S., Abbadie L. Anew protocol for an artificial soil to analyse soil microbiological processes. Applied Soil Ecology 2011, 48:243-246.
29. Harris R.F. Effect of water potential on microbial growth and activity. Water Potential Relations in Soil Microbiology 1981, 23-95. Soil Science Society of America, Madison, Wisconsin. J.F. Parr, W.R. Gardner, L.F. Elliott (Eds.).
30. Hartley I.P., Heinemeyer A., Ineson P. Effects of three years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response. Global Change Biology 2007, 13:1761-1770.
31. Hartley I.P., Hopkins D.W., Garnett M.H., Sommerkorn M., Wookey P.A. Soil microbial respiration in arctic soil does not acclimate to temperature. Ecology Letters 2008, 11:1092-1100.
32. Hartley I.P., Ineson P. Substrate quality and the temperature sensitivity of soil organic matter decomposition. Soil Biology & Biochemistry 2008, 40:1567-1574.
33. Henry H.A.L. Soil extracellular enzyme dynamics in a changing climate. Soil Biology & Biochemistry 2012, 47:53-59.
34. IPCC Climate change 2007: synthesis report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change 2007, Intergovernmental Panel on Climate Change.
35. 10 of soil respiration in a beech forest. Global Change Biology 2003, 9:911-918.
36. Janssens I.A., Sampson D.A., Cermak J., Meiresonne L., Riguzzi F., Overloop S., Ceulemans R. Above- and belowground phytomass and carbon storage in a Belgian Scots pine stand. Annals of Forest Science 1999, 56:81-90.
37. 2 emissions from soil in response to global warming. Nature 1991, 351:304-306.
38. Kirschbaum M.U.F. The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage. Soil Biology & Biochemistry 1995, 27:753-760.
39. Kirschbaum M.U.F. Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss?. Global Change Biology 2004, 10:1870-1877.
40. Klose S., Tabatabai M.A. Urease activity of microbial biomass in soils. Soil Biology & Biochemistry 1999, 31:205-211.
41. Knorr W., Prentice I.C., House J.I., Holland E.A. Long-term sensitivity of soil carbon turnover to warming. Nature 2005, 433:298-301.
42. Kourtev P.S., Ehrenfeld J.G., Häggblom M. Exotic plant species alter the microbial community structure and function in the soil. Ecology 2002, 83:3152-3166.
43. Kuffner M., Hai B., Rattei T., Melodelima C., Schloter M., Zechmeister-Boltenstern S., Jandl R., Schindlbacher A., Sessitsch A. Effects of season and experimental warming on the bacterial community in a temperate mountain forest soil assessed by 16S rRNA gene pyrosequencing. FEMS Microbiology Ecology 2012, 82:551-562.
44. Lloyd J., Taylor J.A. On the temperature dependence of soil respiration. Functional ecology 1994, 8:315-323.
45. Luo Y.Q. Terrestrial carbon-cycle feedback to climate warming. Annual Review of Ecology, Evolution and Systematics 2007, 38:683-712.
46. Luo Y.Q., Wan S.Q., Hui D.F., Wallace L.L. Acclimatization of soil respiration to warming in a tall grass prairie. Nature 2001, 413:622-625.
47. Luo Y.Q., Weng E.S. Dynamic disequilibrium of the terrestrial carbon cycle under global change. Trends in Ecology and Evolution 2011, 26:96-104.
48. Malcolm G.M., Lopez-Gutierrez J.C., Koide R.T., Eissenstat D.M. Acclimation to temperature and temperature sensitivity of metabolism by ectomycorrhizal fungi. Global Change Biology 2008, 14:1169-1180.
49. Manzoni S., Taylor P., Richter A., Porporato A., Ågren G.I. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytologist 2012, 196:79-91.
50. Marschner B., Bredow A. Temperature effects on release and ecologically relevant properties of dissolved organic carbon in sterilised and biologically active soil samples. Soil Biology & Biochemistry 2002, 34:459-466.
51. Raich J.W., Schlesinger W.H. The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus B 1992, 44:81-99.
52. Rinnan R., Rousk J., Yergeau E., Kowalchuk G.A., Bååth E. Temperature adaptation of soil bacterial communities along an Antarctic climate gradient: predicting responses to climate warming. Global Change Biology 2009, 15:2615-2625.
53. Rousk J., Frey S.D., Bååth E. Temperature adaptation of bacterial communities in experimentally warmed forest soils. Global Change Biology 2012, 18:3252-3258.
54. Saiya-Cork K.R., Sinsabaugh R.L., Zak D.R. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biology & Biochemistry 2002, 34:1309-1315.
55. Schimel J., Balser T.C., Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology 2007, 88:1386-1394.
56. Schindlbacher A., Rodler A., Kuffner M., Kitzler B., Sessitsch A., Zechmeister-Boltenstern S. Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biology & Biochemistry 2011, 43:1417-1425.
57. Schmidt M.W.I., Torn M.S., Abiven S., Dittmar T., Guggenberger G., Janssens I.A., Kleber M., Kogel-Knabner I., Lehmann J., Manning D.A.C. Persistence of soil organic matter as an ecosystem property. Nature 2011, 478:49-56.
58. 2]: a simulation analysis. Global Change Biology 2009, 15:2274-2294.
59. Šnajdr J., Dobiášová P., Urbanová M., Petránková M., Cajthaml T., Frouz J., Baldrian P. Dominant trees affect microbial community composition and activity in post-mining afforested soils. Soil Biology & Biochemistry 2013, 56:105-115.
60. Swift M.J., Heal O.W., Anderson J.M. Decomposition in terrestrial ecosystems. Studies in Ecology 1979, vol. 5:66-112. University of California Press, Berkeley and Los Angeles.
61. Thiessen S., Gleixner G., Wutzler T., Reichstein M. Both priming and temperature sensitivity of soil organic matter decomposition depend on microbial biomass - an incubation study. Soil Biology & Biochemistry 2013, 57:739-748.
62. Tucker C.L., Bell J., Pendall E., Ogle K. Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming?. Global Change Biology 2013, 19:252-263.
63. Vance E.D., Brookes P.C., Jenkinson D. An extraction method for measuring soil microbial biomass C. Soil Biology & Biochemistry 1987, 19:703-707.
64. Vicca S., Fivez L., Kockelbergh F., van Pelt D., Segers J.J.R., Meire P., Ceulemans R., Janssens I.A. No signs of thermal acclimation of heterotrophic respiration from peat soils exposed to different water levels. Soil Biology & Biochemistry 2009, 41:2014-2016.
65. Waldrop M.P., Balser T.C., Firestone M.K. Linking microbial community composition to function in a tropical soil. Soil Biology & Biochemistry 2000, 32:1837-1846.
66. Weand M.P., Arthur M.A., Lovett G.M., McCulley R.L., Weathers K.C. Effects of tree species and N additions on forest floor microbial communities and extracellular enzyme activities. Soil Biology & Biochemistry 2010, 42:2161-2173.
67. Weedon J.T., Kowalchuk G.A., Aerts R., van Hal J., van Logtestijn R., Tas N., Roling W.F.M., van Bodegom P.M. Summer warming accelerates sub-arctic peatland nitrogen cycling without changing enzyme pools or microbial community structure. Global Change Biology 2012, 18:138-150.
68. Whitby T.G., Madritch M.D. Native temperature regime influences soil response to simulated warming. Soil Biology & Biochemistry 2013, 60:202-209.
69. Wu J., Joergensen R.G., Pommerening B., Chaussod R., Brookes P.C. Measurement of soil microbial biomass C by fumigation-extraction-an automated procedure. Soil Biology & Biochemistry 1990, 22:1167-1169.
70. Wu Y.P., Yu X.S., Wang H.Z., Ding N., Xu J.M. Does history matter? Temperature effects on soil microbial biomass and community structure based on the phospholipid fatty acid (PLFA) analysis. Journal of Soils and Sediments 2010, 10:223-230.
71. Zelles L. Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 1997, 35:275-294.
72. Zelles L. Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biology and fertility of soils 1999, 29:111-129.
73. Zhang W., Parker K.M., Luo Y., Wan S., Wallace L.L., Hu S. Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Global Change Biology 2005, 11:266-277.
74. Ziegler S.E., Billings S.A., Lane C.S., Li J.W., Fogel M.L. Warming alters routing of labile and slower-turnover carbon through distinct microbial groups in boreal forest organic soils. Soil Biology & Biochemistry 2013, 60:23-32.
75. Zogg G.P., Zak D.R., Ringelberg D.B., MacDonald N.W., Pregitzer K.S., White D.C. Compositional and functional shifts in microbial communities due to soil warming. Soil Science Society of America Journal 1997, 61:475-481.