Phenological Stage, Plant Biomass, and Drought Stress Affect Microbial Biomass and Enzyme Activities in the Rhizosphere of Enteropogon macrostachyus
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摘要
Indigenous grasses have been effectively used to rehabilitate degraded African drylands. Despite their success, studies examining their effects on soil bioindicators such as microbial biomass carbon(C) and enzyme activities are scarce. This study elucidates the effects of drought stress and phenological stages of a typical indigenous African grass, Enteropogon macrostachyus, on microbial biomass and enzyme activities(β-glucosidase, cellobiohydrolase, and chitinase) in the rhizosphere soil. Enteropogon macrostachyus was grown under controlled conditions. Drought stress(partial watering) was simulated during the last 10 d of plant growth, and data were compared with those from optimum moisture conditions. The rhizosphere soil was sampled after 40 d(seedling stage), 70 d(elongation stage), and 80 d(simulated drought stress). A high root:shoot ratio at seedling stage compared with elongation and reproduction stages demonstrated that E. macrostachyus invested more on root biomass in early development, to maximise the uptake of nutrients and water. Microbial biomass and enzyme activities increased with root biomass during plant growth. Ten-day drought at reproduction stage increased the microbial biomass and enzyme activities, accompanying a decrease in binding affinity and catalytic efficiency. In conclusion, drought stress controls soil organic matter decomposition and nutrient mobilization, as well as the competition between plant and microorganisms for nutrient uptake.
Indigenous grasses have been effectively used to rehabilitate degraded African drylands. Despite their success, studies examining their effects on soil bioindicators such as microbial biomass carbon(C) and enzyme activities are scarce. This study elucidates the effects of drought stress and phenological stages of a typical indigenous African grass, Enteropogon macrostachyus, on microbial biomass and enzyme activities(β-glucosidase, cellobiohydrolase, and chitinase) in the rhizosphere soil. Enteropogon macrostachyus was grown under controlled conditions. Drought stress(partial watering) was simulated during the last 10 d of plant growth, and data were compared with those from optimum moisture conditions. The rhizosphere soil was sampled after 40 d(seedling stage), 70 d(elongation stage), and 80 d(simulated drought stress). A high root:shoot ratio at seedling stage compared with elongation and reproduction stages demonstrated that E. macrostachyus invested more on root biomass in early development, to maximise the uptake of nutrients and water. Microbial biomass and enzyme activities increased with root biomass during plant growth. Ten-day drought at reproduction stage increased the microbial biomass and enzyme activities, accompanying a decrease in binding affinity and catalytic efficiency. In conclusion, drought stress controls soil organic matter decomposition and nutrient mobilization, as well as the competition between plant and microorganisms for nutrient uptake.
Indigenous grasses have been effectively used to rehabilitate degraded African drylands. Despite their success, studies examining their effects on soil bioindicators such as microbial biomass carbon(C) and enzyme activities are scarce. This study elucidates the effects of drought stress and phenological stages of a typical indigenous African grass, Enteropogon macrostachyus, on microbial biomass and enzyme activities(β-glucosidase, cellobiohydrolase, and chitinase) in the rhizosphere soil. Enteropogon macrostachyus was grown under controlled conditions. Drought stress(partial watering) was simulated during the last 10 d of plant growth, and data were compared with those from optimum moisture conditions. The rhizosphere soil was sampled after 40 d(seedling stage), 70 d(elongation stage), and 80 d(simulated drought stress). A high root:shoot ratio at seedling stage compared with elongation and reproduction stages demonstrated that E. macrostachyus invested more on root biomass in early development, to maximise the uptake of nutrients and water. Microbial biomass and enzyme activities increased with root biomass during plant growth. Ten-day drought at reproduction stage increased the microbial biomass and enzyme activities, accompanying a decrease in binding affinity and catalytic efficiency. In conclusion, drought stress controls soil organic matter decomposition and nutrient mobilization, as well as the competition between plant and microorganisms for nutrient uptake.
引文
Arriaga L,Castellanos A E,Moreno E,Alarc′on J.2004.Potential ecological distribution of alien invasive species and risk assessment:A case study of buffel grass in arid regions of Mexico.Conserv Biol.18:1504-1514.
Asmar F,Eiland F,Nielsen N E.1994.Effect of extracellularenzyme activities on solubilization rate of soil organic nitrogen.Biol Fert Soils.17:32-38.
Bais H P,Weir T L,Perry L G,Gilroy S,Vivanco J M.2006.The role of root exudates in rhizosphere interactions with plants and other organisms.Annu Rev Plant Biol.57:233-266.
Baldwin J,Hochachka P W.1970.Functional significance of isoenzymes in thermal acclimatization.Acetylcholinesterase from trout brain.Biochemical J.116:883-887.
Benizri E,Nguyen C,Piutti S,Slezack-Deschaumes S,Philippot L.2007.Additions of maize root mucilage to soil changed the structure of the bacterial community.Soil Biol Biochem.39:1230-1233.
Blagodatskaya E V,Blagodatsky S A,Anderson T H,Kuzyakov Y.2009.Contrasting effects of glucose,living roots and maize straw on microbial growth kinetics and substrate availability in soil.Eur J Soil Sci.60:186-197.
Bradford M A.2013.Thermal adaptation of decomposer communities in warming soils.Front Microbiol.4:333.
Caldwell B A.2005.Enzyme activities as a component of soil biodiversity:A review.Pedobiologia.49:637-644.
Carminati A,Schneider C L,Moradi A B,Zarebanadkouki M,Vetterlein D,Vogel H J,Hildebrandt A,Weller U,Sch¨uler L,Oswald S E.2011.How the rhizosphere may favor water availability to roots.Vadose Zone J.10:988-998.
Cheng W X,Coleman D C.1990.Effect of living roots on soil organic matter decomposition.Soil Biol Biochem.22:781-787.
Coronado M H E,Castillo A M,Cerecedo M S,Romo R C,Castro J J.2005.Emergence and survival of native and introduced grasses in an arid environment under different wet-dry sequences in three soil types.T′ec Pecu M′ex.43:101-115.
Curl E A,Truelove B.1986.Root exudates.In Curl E A,Truelove B(eds.)The Rhizosphere.Springer,Berlin,Heidelberg.pp.55-92.
Farrar J F,Jones D L.2000.The control of carbon acquisition by roots.New Phytol.147:43-53.
Frank D A,Groffman P M.2009.Plant rhizospheric N processes:What we don’t know and why we should care.Ecology.90:1512-1519.
Hinsinger P,Bengough A G,Vetterlein D,Young I M.2009.Rhizosphere:Biophysics,biogeochemistry and ecological relevance.Plant Soil.321:117-152.
Hoang D T T,Razavi B S,Kuzyakov Y,Blagodatskaya E.2016.Earthworm burrows:Kinetics and spatial distribution of enzymes of C-,N-and P-cycles.Soil Biol Biochem.99:94-103.
H¨ogberg P,Read D J.2006.Towards a more plant physiological perspective on soil ecology.Trends Ecol Evol.21:548-554.
Jones D L,Hodge A,Kuzyakov Y.2004.Plant and mycorrhizal regulation of rhizodeposition.New Phytol.163:459-480.
Jones D L,Nguyen C,Finlay D R.2009.Carbon flow in the rhizosphere:Carbon trading at the soil-root interface.Plant Soil.321:5-33.
J¨orgensen R G.1996.The fumigation-extraction method to estimate soil microbial biomass:Calibration of the kECvalue.Soil Biol Biochem.28:25-31.
Koch O,Tscherko D,Kandeler E.2007.Temperature sensitivity of microbial respiration,nitrogen mineralization,and potential soil enzyme activities in organic alpine soils.Global Biogeochem Cycles.21:GB4017.
Kreyling J,Beierkuhnlein C,Elmer M,Pritsch K,Radovski M,Schloter M,W¨ollecke J,Jentsch A.2008.Soil biotic processes remain remarkably stable after 100-year extreme weather events in experimental grassland and heath.Plant Soil.308:175-188.
Kuzyakov Y V.2001.Tracer studies of carbon translocation by plants from the atmosphere into the soil(a review).Eur Soil Sci.34:28-42.
Kuzyakov Y,Biryukova O,Kuznetzova T,M¨olter K,Kandeler E,Stahr K.2002.Carbon partitioning in plant and soil,carbon dioxide fluxes and enzyme activities as affected by cutting ryegrass.Biol Fertil Soils.35:348-358.
Kuzyakov Y,Raskatov A,Kaupenjohann M.2003.Turnover and distribution of root exudates of Zea mays.Plant Soil.254:317-327.
Lloret F,Casanovas C,Peˇnuelas J.1999.Seedling survival of Mediterranean shrubland species in relation to root:Shoot ratio,seed size and water and nitrogen use.Funct Ecol.13:210-216.
Marshall V M,Lewis M M,Ostendorf B.2012.Buffel grass(Cenchrus ciliaris)as an invader and threat to biodiversity in arid environments:A review.J Arid Environ.78:1-12.
Marx M C,Wood M,Jarvis S C.2001.A microplate fluorimetric assay for the study of enzyme diversity in soils.Soil Biol Biochem.33:1633-1640.
Mganga K Z,Musimba N K R,Nyariki D M,Nyangito M M,Mwang’ombe A W.2015a.The choice of grass species to combat desertification in semi-arid Kenyan rangelands is greatly influenced by their forage value for livestock.Grass For Sci.70:161-167.
Mganga K Z,Musimba N K R,Nyariki D M.2015b.Competition indices of three perennial grasses used to rehabilitate degraded semi-arid rangelands in Kenya.Rangeland J.37:489-495.
Mganga K Z,Razavi B S,Kuzyakov Y.2016.Land use affects soil biochemical properties in Mt.Kilimanjaro region.Catena.141:22-29.
Nannipieri P,Gianfreda L.1998.Kinetics of enzyme reactions in soil environments.In Huang P M,Senesi N,Buffle J(eds.)Structure and Surface Reactions of Soil Particles.John Wiley&Sons,New York.pp.449-479.
Parkin T B.1993.Spatial variability of microbial processes in soil-a review.J Environ Qual.22:409-417.
Pritsch K,Raidl S,Marksteiner E,Blaschke H,Agerer R,Schloter M,Hartmann A.2004.A rapid and highly sensitive method for measuring enzyme activities in single mycorrhizal tips using 4-methylumbelliferone-labelled fluorogenic substrates in a microplate system.J Microbiol Methods.58:233-241.
Ravi S,Breshears D D,Huxman T E,D’Odorico P.2010.Land degradation in drylands:Interactions among hydrologicaeolian erosion and vegetation dynamics.Geomorphology.116:236-245.
Razavi B S,Blagodatskaya E,Kuzyakov Y.2015.Nonlinear temperature sensitivity of enzyme kinetics explains canceling effect-a case study on loamy haplic Luvisol.Front Microbiol.6:Article 1126.
Razavi B S,Blagodatskaya E,Kuzyakov Y.2016.Temperature selects for static soil enzyme systems to maintain high catalytic efficiency.Soil Biol Biochem.97:15-22.
Razavi B S,Liu S B,Kuzyakov Y.2017.Hot experience for coldadapted microorganisms:Temperature sensitivity of soil enzymes.Soil Biol Biochem.105:236-243.
Saif S R.1987.Growth responses of tropical forage plant species to vesicular-arbuscular mycorrhizae:I.Growth,mineral uptake and mycorrhizal dependency.Plant Soil.97:25-35.
Sanaullah M,Blagodatskaya E,Chabbi A,Rumpel C,Kuzyakov Y.2011.Drought effects on microbial biomass and enzyme activities in the rhizosphere of grasses depend on plant community composition.Appl Soil Ecol.48:38-44.
Segel I H.1975.Enzyme Kinetics:Behavior and Analysis of Rapid Equilibrium and Steady-state Enzyme Systems.Willey,New York.
Steinweg J M,Dukes J S,Paul E A,Wallenstein M D.2013.Microbial responses to multi-factor climate change:Effects on soil enzymes.Front Microbiol.4:Article 146.
Stone M M,Weiss M S,Goodale C L,Adams M B,Fernandez IJ,German D P,Allison S D.2012.Temperature sensitivity of soil enzyme kinetics under N-fertilization in two temperate forests.Glob Change Biol.18:1173-1184.
Tischer A,Blagodatskaya E,Hamer U.2015.Microbial community structure and resource availability drive the catalytic efficiency of soil enzymes under land-use change conditions.Soil Biol Biochem.89:226-237.
Vance E D,Brookes P C,Jenkinson D S.1987.An extraction method for measuring soil microbial biomass C.Soil Biol Biochem.19:703-707.
Wertin T M,McGuire M A,Teskey R O.2010.The influence of elevated temperature,elevated atmospheric CO2 concentration and water stress on net photosynthesis of loblolly pine(Pinus taeda L.)at northern,central and southern sites in its native range.Glob Change Biol.16:2089-2103.
Asmar F,Eiland F,Nielsen N E.1994.Effect of extracellularenzyme activities on solubilization rate of soil organic nitrogen.Biol Fert Soils.17:32-38.
Bais H P,Weir T L,Perry L G,Gilroy S,Vivanco J M.2006.The role of root exudates in rhizosphere interactions with plants and other organisms.Annu Rev Plant Biol.57:233-266.
Baldwin J,Hochachka P W.1970.Functional significance of isoenzymes in thermal acclimatization.Acetylcholinesterase from trout brain.Biochemical J.116:883-887.
Benizri E,Nguyen C,Piutti S,Slezack-Deschaumes S,Philippot L.2007.Additions of maize root mucilage to soil changed the structure of the bacterial community.Soil Biol Biochem.39:1230-1233.
Blagodatskaya E V,Blagodatsky S A,Anderson T H,Kuzyakov Y.2009.Contrasting effects of glucose,living roots and maize straw on microbial growth kinetics and substrate availability in soil.Eur J Soil Sci.60:186-197.
Bradford M A.2013.Thermal adaptation of decomposer communities in warming soils.Front Microbiol.4:333.
Caldwell B A.2005.Enzyme activities as a component of soil biodiversity:A review.Pedobiologia.49:637-644.
Carminati A,Schneider C L,Moradi A B,Zarebanadkouki M,Vetterlein D,Vogel H J,Hildebrandt A,Weller U,Sch¨uler L,Oswald S E.2011.How the rhizosphere may favor water availability to roots.Vadose Zone J.10:988-998.
Cheng W X,Coleman D C.1990.Effect of living roots on soil organic matter decomposition.Soil Biol Biochem.22:781-787.
Coronado M H E,Castillo A M,Cerecedo M S,Romo R C,Castro J J.2005.Emergence and survival of native and introduced grasses in an arid environment under different wet-dry sequences in three soil types.T′ec Pecu M′ex.43:101-115.
Curl E A,Truelove B.1986.Root exudates.In Curl E A,Truelove B(eds.)The Rhizosphere.Springer,Berlin,Heidelberg.pp.55-92.
Farrar J F,Jones D L.2000.The control of carbon acquisition by roots.New Phytol.147:43-53.
Frank D A,Groffman P M.2009.Plant rhizospheric N processes:What we don’t know and why we should care.Ecology.90:1512-1519.
Hinsinger P,Bengough A G,Vetterlein D,Young I M.2009.Rhizosphere:Biophysics,biogeochemistry and ecological relevance.Plant Soil.321:117-152.
Hoang D T T,Razavi B S,Kuzyakov Y,Blagodatskaya E.2016.Earthworm burrows:Kinetics and spatial distribution of enzymes of C-,N-and P-cycles.Soil Biol Biochem.99:94-103.
H¨ogberg P,Read D J.2006.Towards a more plant physiological perspective on soil ecology.Trends Ecol Evol.21:548-554.
Jones D L,Hodge A,Kuzyakov Y.2004.Plant and mycorrhizal regulation of rhizodeposition.New Phytol.163:459-480.
Jones D L,Nguyen C,Finlay D R.2009.Carbon flow in the rhizosphere:Carbon trading at the soil-root interface.Plant Soil.321:5-33.
J¨orgensen R G.1996.The fumigation-extraction method to estimate soil microbial biomass:Calibration of the kECvalue.Soil Biol Biochem.28:25-31.
Koch O,Tscherko D,Kandeler E.2007.Temperature sensitivity of microbial respiration,nitrogen mineralization,and potential soil enzyme activities in organic alpine soils.Global Biogeochem Cycles.21:GB4017.
Kreyling J,Beierkuhnlein C,Elmer M,Pritsch K,Radovski M,Schloter M,W¨ollecke J,Jentsch A.2008.Soil biotic processes remain remarkably stable after 100-year extreme weather events in experimental grassland and heath.Plant Soil.308:175-188.
Kuzyakov Y V.2001.Tracer studies of carbon translocation by plants from the atmosphere into the soil(a review).Eur Soil Sci.34:28-42.
Kuzyakov Y,Biryukova O,Kuznetzova T,M¨olter K,Kandeler E,Stahr K.2002.Carbon partitioning in plant and soil,carbon dioxide fluxes and enzyme activities as affected by cutting ryegrass.Biol Fertil Soils.35:348-358.
Kuzyakov Y,Raskatov A,Kaupenjohann M.2003.Turnover and distribution of root exudates of Zea mays.Plant Soil.254:317-327.
Lloret F,Casanovas C,Peˇnuelas J.1999.Seedling survival of Mediterranean shrubland species in relation to root:Shoot ratio,seed size and water and nitrogen use.Funct Ecol.13:210-216.
Marshall V M,Lewis M M,Ostendorf B.2012.Buffel grass(Cenchrus ciliaris)as an invader and threat to biodiversity in arid environments:A review.J Arid Environ.78:1-12.
Marx M C,Wood M,Jarvis S C.2001.A microplate fluorimetric assay for the study of enzyme diversity in soils.Soil Biol Biochem.33:1633-1640.
Mganga K Z,Musimba N K R,Nyariki D M,Nyangito M M,Mwang’ombe A W.2015a.The choice of grass species to combat desertification in semi-arid Kenyan rangelands is greatly influenced by their forage value for livestock.Grass For Sci.70:161-167.
Mganga K Z,Musimba N K R,Nyariki D M.2015b.Competition indices of three perennial grasses used to rehabilitate degraded semi-arid rangelands in Kenya.Rangeland J.37:489-495.
Mganga K Z,Razavi B S,Kuzyakov Y.2016.Land use affects soil biochemical properties in Mt.Kilimanjaro region.Catena.141:22-29.
Nannipieri P,Gianfreda L.1998.Kinetics of enzyme reactions in soil environments.In Huang P M,Senesi N,Buffle J(eds.)Structure and Surface Reactions of Soil Particles.John Wiley&Sons,New York.pp.449-479.
Parkin T B.1993.Spatial variability of microbial processes in soil-a review.J Environ Qual.22:409-417.
Pritsch K,Raidl S,Marksteiner E,Blaschke H,Agerer R,Schloter M,Hartmann A.2004.A rapid and highly sensitive method for measuring enzyme activities in single mycorrhizal tips using 4-methylumbelliferone-labelled fluorogenic substrates in a microplate system.J Microbiol Methods.58:233-241.
Ravi S,Breshears D D,Huxman T E,D’Odorico P.2010.Land degradation in drylands:Interactions among hydrologicaeolian erosion and vegetation dynamics.Geomorphology.116:236-245.
Razavi B S,Blagodatskaya E,Kuzyakov Y.2015.Nonlinear temperature sensitivity of enzyme kinetics explains canceling effect-a case study on loamy haplic Luvisol.Front Microbiol.6:Article 1126.
Razavi B S,Blagodatskaya E,Kuzyakov Y.2016.Temperature selects for static soil enzyme systems to maintain high catalytic efficiency.Soil Biol Biochem.97:15-22.
Razavi B S,Liu S B,Kuzyakov Y.2017.Hot experience for coldadapted microorganisms:Temperature sensitivity of soil enzymes.Soil Biol Biochem.105:236-243.
Saif S R.1987.Growth responses of tropical forage plant species to vesicular-arbuscular mycorrhizae:I.Growth,mineral uptake and mycorrhizal dependency.Plant Soil.97:25-35.
Sanaullah M,Blagodatskaya E,Chabbi A,Rumpel C,Kuzyakov Y.2011.Drought effects on microbial biomass and enzyme activities in the rhizosphere of grasses depend on plant community composition.Appl Soil Ecol.48:38-44.
Segel I H.1975.Enzyme Kinetics:Behavior and Analysis of Rapid Equilibrium and Steady-state Enzyme Systems.Willey,New York.
Steinweg J M,Dukes J S,Paul E A,Wallenstein M D.2013.Microbial responses to multi-factor climate change:Effects on soil enzymes.Front Microbiol.4:Article 146.
Stone M M,Weiss M S,Goodale C L,Adams M B,Fernandez IJ,German D P,Allison S D.2012.Temperature sensitivity of soil enzyme kinetics under N-fertilization in two temperate forests.Glob Change Biol.18:1173-1184.
Tischer A,Blagodatskaya E,Hamer U.2015.Microbial community structure and resource availability drive the catalytic efficiency of soil enzymes under land-use change conditions.Soil Biol Biochem.89:226-237.
Vance E D,Brookes P C,Jenkinson D S.1987.An extraction method for measuring soil microbial biomass C.Soil Biol Biochem.19:703-707.
Wertin T M,McGuire M A,Teskey R O.2010.The influence of elevated temperature,elevated atmospheric CO2 concentration and water stress on net photosynthesis of loblolly pine(Pinus taeda L.)at northern,central and southern sites in its native range.Glob Change Biol.16:2089-2103.