Metagenomic approach revealed effects of forest thinning on bacterial communities in the forest soil of Mt. Janggunbong, South Korea
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摘要
The soil microbiome that plays important ecological roles in mountains and forests is influenced by anthropogenic and natural causes.Human activity,particularly harvesting or thinning,affects the soil microbiome in forests by altering environmental conditions,such as vegetation,microclimate,and soil physicochemical properties.The purpose of this study was to investigate the effects on forest thinning on the diversity and composition of the soil bacterial community.From next-generation sequencing results of the 16S rRNA gene,we examined differences in soil bacterial diversity and community composition before and after thinning at Mt.Janggunbong,South Korea.We identified 40 phyla,103 classes,192 orders,412families,947 genera,and 3,145 species from the soil samples.Acidobacteria and Proteobacteria were the most dominant bacterial phyla in the forest soil of Mt.Janggunbong.Soil bacterial diversity measures(richness,Shannon diversity index,and evenness)at the phylum level increased after thinning,whereas species-level taxonomic richness decreased after thinning.Thinning provided new opportunities for bacterial species in Chloroflexi,Verrucomicrobia,Nitrospirae,and other nondominant bacterial taxa,especially for those not found in Mt.Janggunbong before thinning,to settle and adapt to the changing environment.Our results suggested that thinning affected the diversity and composition of soil bacterial communities in forests and mountains.
The soil microbiome that plays important ecological roles in mountains and forests is influenced by anthropogenic and natural causes.Human activity,particularly harvesting or thinning,affects the soil microbiome in forests by altering environmental conditions,such as vegetation,microclimate,and soil physicochemical properties.The purpose of this study was to investigate the effects on forest thinning on the diversity and composition of the soil bacterial community.From next-generation sequencing results of the 16S rRNA gene,we examined differences in soil bacterial diversity and community composition before and after thinning at Mt.Janggunbong,South Korea.We identified 40 phyla,103 classes,192 orders,412families,947 genera,and 3,145 species from the soil samples.Acidobacteria and Proteobacteria were the most dominant bacterial phyla in the forest soil of Mt.Janggunbong.Soil bacterial diversity measures(richness,Shannon diversity index,and evenness)at the phylum level increased after thinning,whereas species-level taxonomic richness decreased after thinning.Thinning provided new opportunities for bacterial species in Chloroflexi,Verrucomicrobia,Nitrospirae,and other nondominant bacterial taxa,especially for those not found in Mt.Janggunbong before thinning,to settle and adapt to the changing environment.Our results suggested that thinning affected the diversity and composition of soil bacterial communities in forests and mountains.
The soil microbiome that plays important ecological roles in mountains and forests is influenced by anthropogenic and natural causes.Human activity,particularly harvesting or thinning,affects the soil microbiome in forests by altering environmental conditions,such as vegetation,microclimate,and soil physicochemical properties.The purpose of this study was to investigate the effects on forest thinning on the diversity and composition of the soil bacterial community.From next-generation sequencing results of the 16S rRNA gene,we examined differences in soil bacterial diversity and community composition before and after thinning at Mt.Janggunbong,South Korea.We identified 40 phyla,103 classes,192 orders,412families,947 genera,and 3,145 species from the soil samples.Acidobacteria and Proteobacteria were the most dominant bacterial phyla in the forest soil of Mt.Janggunbong.Soil bacterial diversity measures(richness,Shannon diversity index,and evenness)at the phylum level increased after thinning,whereas species-level taxonomic richness decreased after thinning.Thinning provided new opportunities for bacterial species in Chloroflexi,Verrucomicrobia,Nitrospirae,and other nondominant bacterial taxa,especially for those not found in Mt.Janggunbong before thinning,to settle and adapt to the changing environment.Our results suggested that thinning affected the diversity and composition of soil bacterial communities in forests and mountains.
引文
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Bakker MG,Schlatter DC,Otto-Hanson L,et al.(2014)Diffuse symbioses:roles of plant-plant,plant-microbe and microbemicrobe interactions in structuring the soil microbiome.Molecular ecology 23(6):1571-1583.https://doi.org/10.1111/mec.12571
Boerner RE,Sutherland EK(1997)The chemical characteristics of soil in control and experimentally thinned plots in mesic oak forests along a historical deposition gradient.Applied Soil Ecology7(1):59-71.https://doi.org/10.1016/S0929-1393(97)00023-1
Box GE,Cox DR(1964)An analysis of transformations.Journal of the Royal Statistical Society.Series B(Methodological)26(2):211-252.
Burd GI,Dixon DG,Glick BR(2000)Plant growth-promoting bacteria that decrease heavy metal toxicity in plants.Canadian journal of microbiology 46(3):237-245.https://doi.org/10.1139/w99-143
Burd GI,Dixon DG,Glick BR(1998)A plant growth-promoting bacterium that decreases nickel toxicity in seedlings.Applied and Environmental Microbiology 64(10):3663-3668.
Byeon S,Yun C(2016)Stand structure of actual vegetation in the natural forests and plantation area of Mt.Janggunbong,Bonghwa-Gun.Korean Journal of Environment and Ecology30(6):1032-1046.(In Korean)
Chin K,Liesack W,Janssen PH(2001)Opitutus terrae gen.nov.,sp.nov.,to accommodate novel strains of the division'Verrucomicrobia'isolated from rice paddy soil.International Journal of Systematic and Evolutionary Microbiology 51(6):1965-1968.https://doi.org/10.1099/00207713-51-6-1965
Chun J,Kim KY,Lee J,et al.(2010)The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX Titanium pyrosequencer.BMC microbiology10:101.https://doi.org/10.1186/1471-2180-10-101
Dannenmann M,Butterbach-Bahl K,Gasche R,et al.(2008)Dinitrogen emissions and the N 2:N 2 O emission ratio of a Rendzic Leptosol as influenced by p H and forest thinning.Soil Biology and Biochemistry 40(9):2317-2323.https://doi.org/10.1016/j.soilbio.2008.05.009
Edwards DP,Larsen TH,Docherty TD,et al.(2011)Degraded lands worth protecting:the biological importance of Southeast Asia's repeatedly logged forests.Proceedings.Biological sciences278(1702):82-90.https://doi.org/10.1098/rspb.2010.1062
Fierer N,Bradford MA,Jackson RB(2007)Toward an ecological classification of soil bacteria.Ecology 88(6):1354-1364.https://doi.org/10.1890/05-1839
Gondard H,Romane F,Aronson J,et al.(2003)Impact of soil surface disturbances on functional group diversity after clear-cutting in Aleppo pine(Pinus halepensis)forests in southern France.Forest Ecology and Management 180(1):165-174.https://doi.org/10.1016/S0378-1127(02)00597-2
Grigal DF(2000)Effects of extensive forest management on soil productivity.Forest Ecology and Management 138(1):167-185.https://doi.org/10.1016/S0378-1127(00)00395-9
Hartmann M,Howes CG,Van Insberghe D,et al.(2012)Significant and persistent impact of timber harvesting on soil microbial communities in Northern coniferous forests.The ISME journal6(12):2199-2218.https://doi.org/10.1038/ismej.2012.84
Hartmann M,Niklaus PA,Zimmermann S,et al.(2014)Resistance and resilience of the forest soil microbiome to logging-associated compaction.The ISME journal 8(1):226-244.https://doi.org/10.1038/ismej.2013.141
Hornbeck JW(1992)Comparative impacts of forest harvest and acid precipitation on soil and streamwater acidity.Environmental Pollution 77(2-3):151-155.https://doi.org/10.1016/0269-7491(92)90071-H
Hortal S,Bastida F,Armas C,et al.(2013)Soil microbial community under a nurse-plant species changes in composition,biomass and activity as the nurse grows.Soil Biology and Biochemistry 64:139-146.https://doi.org/10.1016/j.soilbio.2013.04.018
Huber T,Faulkner G,Hugenholtz P(2004)Bellerophon:a program to detect chimeric sequences in multiple sequence alignments.Bioinformatics(Oxford,England)20(14):2317-2319.https://doi.org/10.1093/bioinformatics/bth226
Hur M,Kim Y,Song HR,et al.(2011)Effect of genetically modified poplars on soil microbial communities during the phytoremediation of waste mine tailings.Applied and Environmental Microbiology 77(21):7611-7619.https://doi.org/10.1128/AEM.06102-11
Imfeld G,Vuilleumier S(2012)Measuring the effects of pesticides on bacterial communities in soil:a critical review.European Journal of Soil Biology 49:22-30.https://doi.org/10.1016/j.ejsobi.2011.11.010
Jurgensen M,Harvey A,Graham R,et al.(1997)Impacts of timber harvesting on soil organic matter,nitrogen,productivity,and health of Inland Northwest forests.Forest Science 43(2):234-251.
Keenan RJ,Kimmins J(1993)The ecological effects of clear-cutting.Environmental Reviews 1(2):121-144.https://doi.org/10.1139/a93-010
Kim B,Kim JN,Yoon S,et al.(2012a)Impact of enrofloxacin on the human intestinal microbiota revealed by comparative molecular analysis.Anaerobe 18(3):310-320.https://doi.org/10.1016/j.anaerobe.2012.01.003
Kim O,Cho Y,Lee K,et al.(2012b)Introducing Ez Taxon-e:a prokaryotic 16S r RNA gene sequence database with phylotypes that represent uncultured species.International Journal of Systematic and Evolutionary Microbiology 62(3):716-721.https://doi.org/10.1099/ijs.0.038075-0
Kourtev PS,Ehrenfeld JG,H?ggblom M(2002)Exotic plant species alter the microbial community structure and function in the soil.Ecology 83(11):3152-3166.https://doi.org/10.1890/0012-9658(2002)083[3152:EPSATM]2.0.CO;2
Krug EC,Frink CR(1983)Acid rain on acid soil:A new perspective.Science 217(4610):520-525.https://doi.org/10.1126/science.221.4610.520
Lee BJ and Eo SH(In Press)Comparison of soil bacterial diversity and community composition between clear-cut logging and control sites in a temperate deciduous broad-leaved forest in Mt.Sambong,South Korea.Journal of Forestry Research.
Lee-Cruz L,Edwards DP,Tripathi BM,et al.(2013)Impact of logging and forest conversion to oil palm plantations on soil bacterial communities in Borneo.Applied and Environmental Microbiology 79(23):7290-7297.https://doi.org/10.1128/AEM.02541-13
Li H,Ye D,Wang X,et al.(2014)Soil bacterial communities of different natural forest types in Northeast China.Plant and Soil383(1-2):203-216.https://doi.org/10.1007/s11104-014-2165-y
Lin W,Chen W,Wang P(2011)Effects of forest thinning on diversity and function of macrofungi and soil microbes.Sydowia 63(1):67-77.
Lyashevska O,Farnsworth KD(2012)How many dimensions of biodiversity do we need?Ecological Indicators 18:485-492.https://doi.org/10.1016/j.ecolind.2011.12.016
Madigan M,Martinko J,Stahl D,et al.(2012)Brock Biology of Microorganisms.(13 Eth)Pearson Education.San Francisco,USA,pp 268-269.
Navarrete AA,Tsai SM,Mendes LW,et al.(2015)Soil microbiome responses to the short‐term effects of Amazonian deforestation.Molecular ecology 24(10):2433-2448.https://doi.org/10.1111/mec.13172
Otaki M,Takeuchi F,Tsuyuzaki S(2016)Changes in microbial community composition in the leaf litter of successional communities after volcanic eruptions of Mount Usu,northern Japan.Journal of Mountain Science 13(9):1652-1662.https://doi.org/10.1007/s11629-016-3835-4
Palleroni NJ(1997)Prokaryotic diversity and the importance of culturing.Antonie van Leeuwenhoek 72(1):3-19.https://doi.org/10.1023/A:1000394109961
Park N,Lee K,Jung S(2009)Estimation of Site Productivity of Pinus densiflora by the Soil Physico-chemical Properties.Korean Journal of Soil Science and Fertilizer 42(3):160-166.(In Korean)
Pfennig N(1975)The phototrophic bacteria and their role in the sulfur cycle.Plant and Soil 43(1-3):1-16.https://doi.org/10.1007/BF01928472
Pielou EC(1966)The measurement of diversity in different types of biological collections.Journal of theoretical biology 13:131-144.https://doi.org/10.1016/0022-5193(66)90013-0
Ratcliff AW,Busse MD,Shestak CJ(2006)Changes in microbial community structure following herbicide(glyphosate)additions to forest soils.Applied Soil Ecology 34(2):114-124.https://doi.org/10.1016/j.apsoil.2006.03.002
Rodr??guez H,Fraga R(1999)Phosphate solubilizing bacteria and their role in plant growth promotion.Biotechnology Advances17(4):319-339.https://doi.org/10.1016/S0734-9750(99)00014-2
Shaffer B,Widmer F,Porteous L,et al.(2000)Temporal and spatial distribution of the nif H gene of N2 fixing bacteria in forests and clearcuts in western Oregon.Microbial ecology 39(1):12-21.
Shannon CE(1948)A Mathematical Theory of Communication.Bell System Technical Journal 27(3):379-423.https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
Shuman L,Boswell F,Ohki K,et al.(1983)Effects of HC1 acid and lime amendments on soil ph and extractable Ca and Mg in a sandy soil.Communications in Soil Science&Plant Analysis 14(6):481-495.https://doi.org/10.1007/s002489900183
?ibanc N,Dumbrell AJ,Mandi?-Mulec I,et al.(2014)Impacts of naturally elevated soil CO2 concentrations on communities of soil archaea and bacteria.Soil Biology and Biochemistry 68:348-356.http://doi.org/10.1016/j.soilbio.2013.10.018
Smith SE,Read DJ(2010)Mycorrhizal symbiosis.Academic Press,USA.
Smith NR,Kishchuk BE,Mohn WW(2008)Effects of wildfire and harvest disturbances on forest soil bacterial communities.Applied and Environmental Microbiology 74(1):216-224.https://doi.org/10.1128/AEM.01355-07
Sokal Robert R,James RF(1969)Biometry.The principles and practice of statistics in biological research.San Francisco,USA.
?tursováM,?if?ákováL,Leigh MB,et al.(2012)Cellulose utilization in forest litter and soil:identification of bacterial and fungal decomposers.FEMS microbiology ecology 80(3):735-746.https://doi.org/10.1111/j.1574-6941.2012.01343.x
Torsvik V,Ovreas L,Thingstad TF(2002)Prokaryotic diversity--magnitude,dynamics,and controlling factors.Science 296(5570):1064-1066.https://doi.org/10.1126/science.1071698
van der Putten W,H.,Klironomos JN,Wardle DA(2007)Microbial ecology of biological invasions.1(1):28-37.https://doi.org/doi:10.1038/ismej.2007.9
Vesterdal L,Dalsgaard M,Felby C,et al.(1995)Effects of thinning and soil properties on accumulation of carbon,nitrogen and phosphorus in the forest floor of Norway spruce stands.Forest Ecology and Management 77(1-3):1-10.https://doi.org/10.1016/0378-1127(95)03579-Y
Warren-Rhodes KA,Rhodes KL,Pointing SB,et al.(2006)Hypolithic cyanobacteria,dry limit of photosynthesis,and microbial ecology in the hyperarid Atacama Desert.Microbial ecology 52(3):389-398.https://doi.org/10.1007/s00248-006-9055-7
Wright IJ,Westoby M(2003)Nutrient concentration,resorption and lifespan:leaf traits of Australian sclerophyll species.Functional Ecology 17(1):10-19.https://doi.org/10.1046/j.1365-2435.2003.00694.x
Wu L,Nie Y,Yang Z,et al.(2016)Responses of soil inhabiting nitrogen-cycling microbial communities to wetland degradation on the Zoige Plateau,China.Journal of Mountain Science 13(12):2192-2204.https://doi.org/10.1007/s11629-016-4004-5
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Zhang X,Liu S,Li X,et al.(2016)Changes of soil prokaryotic communities after clear-cutting in a karst forest:evidences for cutting-based disturbance promoting deterministic processes.FEMS microbiology ecology 92(3):fiw026.https://doi.org/10.1093/femsec/fiw026
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Bakker MG,Schlatter DC,Otto-Hanson L,et al.(2014)Diffuse symbioses:roles of plant-plant,plant-microbe and microbemicrobe interactions in structuring the soil microbiome.Molecular ecology 23(6):1571-1583.https://doi.org/10.1111/mec.12571
Boerner RE,Sutherland EK(1997)The chemical characteristics of soil in control and experimentally thinned plots in mesic oak forests along a historical deposition gradient.Applied Soil Ecology7(1):59-71.https://doi.org/10.1016/S0929-1393(97)00023-1
Box GE,Cox DR(1964)An analysis of transformations.Journal of the Royal Statistical Society.Series B(Methodological)26(2):211-252.
Burd GI,Dixon DG,Glick BR(2000)Plant growth-promoting bacteria that decrease heavy metal toxicity in plants.Canadian journal of microbiology 46(3):237-245.https://doi.org/10.1139/w99-143
Burd GI,Dixon DG,Glick BR(1998)A plant growth-promoting bacterium that decreases nickel toxicity in seedlings.Applied and Environmental Microbiology 64(10):3663-3668.
Byeon S,Yun C(2016)Stand structure of actual vegetation in the natural forests and plantation area of Mt.Janggunbong,Bonghwa-Gun.Korean Journal of Environment and Ecology30(6):1032-1046.(In Korean)
Chin K,Liesack W,Janssen PH(2001)Opitutus terrae gen.nov.,sp.nov.,to accommodate novel strains of the division'Verrucomicrobia'isolated from rice paddy soil.International Journal of Systematic and Evolutionary Microbiology 51(6):1965-1968.https://doi.org/10.1099/00207713-51-6-1965
Chun J,Kim KY,Lee J,et al.(2010)The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX Titanium pyrosequencer.BMC microbiology10:101.https://doi.org/10.1186/1471-2180-10-101
Dannenmann M,Butterbach-Bahl K,Gasche R,et al.(2008)Dinitrogen emissions and the N 2:N 2 O emission ratio of a Rendzic Leptosol as influenced by p H and forest thinning.Soil Biology and Biochemistry 40(9):2317-2323.https://doi.org/10.1016/j.soilbio.2008.05.009
Edwards DP,Larsen TH,Docherty TD,et al.(2011)Degraded lands worth protecting:the biological importance of Southeast Asia's repeatedly logged forests.Proceedings.Biological sciences278(1702):82-90.https://doi.org/10.1098/rspb.2010.1062
Fierer N,Bradford MA,Jackson RB(2007)Toward an ecological classification of soil bacteria.Ecology 88(6):1354-1364.https://doi.org/10.1890/05-1839
Gondard H,Romane F,Aronson J,et al.(2003)Impact of soil surface disturbances on functional group diversity after clear-cutting in Aleppo pine(Pinus halepensis)forests in southern France.Forest Ecology and Management 180(1):165-174.https://doi.org/10.1016/S0378-1127(02)00597-2
Grigal DF(2000)Effects of extensive forest management on soil productivity.Forest Ecology and Management 138(1):167-185.https://doi.org/10.1016/S0378-1127(00)00395-9
Hartmann M,Howes CG,Van Insberghe D,et al.(2012)Significant and persistent impact of timber harvesting on soil microbial communities in Northern coniferous forests.The ISME journal6(12):2199-2218.https://doi.org/10.1038/ismej.2012.84
Hartmann M,Niklaus PA,Zimmermann S,et al.(2014)Resistance and resilience of the forest soil microbiome to logging-associated compaction.The ISME journal 8(1):226-244.https://doi.org/10.1038/ismej.2013.141
Hornbeck JW(1992)Comparative impacts of forest harvest and acid precipitation on soil and streamwater acidity.Environmental Pollution 77(2-3):151-155.https://doi.org/10.1016/0269-7491(92)90071-H
Hortal S,Bastida F,Armas C,et al.(2013)Soil microbial community under a nurse-plant species changes in composition,biomass and activity as the nurse grows.Soil Biology and Biochemistry 64:139-146.https://doi.org/10.1016/j.soilbio.2013.04.018
Huber T,Faulkner G,Hugenholtz P(2004)Bellerophon:a program to detect chimeric sequences in multiple sequence alignments.Bioinformatics(Oxford,England)20(14):2317-2319.https://doi.org/10.1093/bioinformatics/bth226
Hur M,Kim Y,Song HR,et al.(2011)Effect of genetically modified poplars on soil microbial communities during the phytoremediation of waste mine tailings.Applied and Environmental Microbiology 77(21):7611-7619.https://doi.org/10.1128/AEM.06102-11
Imfeld G,Vuilleumier S(2012)Measuring the effects of pesticides on bacterial communities in soil:a critical review.European Journal of Soil Biology 49:22-30.https://doi.org/10.1016/j.ejsobi.2011.11.010
Jurgensen M,Harvey A,Graham R,et al.(1997)Impacts of timber harvesting on soil organic matter,nitrogen,productivity,and health of Inland Northwest forests.Forest Science 43(2):234-251.
Keenan RJ,Kimmins J(1993)The ecological effects of clear-cutting.Environmental Reviews 1(2):121-144.https://doi.org/10.1139/a93-010
Kim B,Kim JN,Yoon S,et al.(2012a)Impact of enrofloxacin on the human intestinal microbiota revealed by comparative molecular analysis.Anaerobe 18(3):310-320.https://doi.org/10.1016/j.anaerobe.2012.01.003
Kim O,Cho Y,Lee K,et al.(2012b)Introducing Ez Taxon-e:a prokaryotic 16S r RNA gene sequence database with phylotypes that represent uncultured species.International Journal of Systematic and Evolutionary Microbiology 62(3):716-721.https://doi.org/10.1099/ijs.0.038075-0
Kourtev PS,Ehrenfeld JG,H?ggblom M(2002)Exotic plant species alter the microbial community structure and function in the soil.Ecology 83(11):3152-3166.https://doi.org/10.1890/0012-9658(2002)083[3152:EPSATM]2.0.CO;2
Krug EC,Frink CR(1983)Acid rain on acid soil:A new perspective.Science 217(4610):520-525.https://doi.org/10.1126/science.221.4610.520
Lee BJ and Eo SH(In Press)Comparison of soil bacterial diversity and community composition between clear-cut logging and control sites in a temperate deciduous broad-leaved forest in Mt.Sambong,South Korea.Journal of Forestry Research.
Lee-Cruz L,Edwards DP,Tripathi BM,et al.(2013)Impact of logging and forest conversion to oil palm plantations on soil bacterial communities in Borneo.Applied and Environmental Microbiology 79(23):7290-7297.https://doi.org/10.1128/AEM.02541-13
Li H,Ye D,Wang X,et al.(2014)Soil bacterial communities of different natural forest types in Northeast China.Plant and Soil383(1-2):203-216.https://doi.org/10.1007/s11104-014-2165-y
Lin W,Chen W,Wang P(2011)Effects of forest thinning on diversity and function of macrofungi and soil microbes.Sydowia 63(1):67-77.
Lyashevska O,Farnsworth KD(2012)How many dimensions of biodiversity do we need?Ecological Indicators 18:485-492.https://doi.org/10.1016/j.ecolind.2011.12.016
Madigan M,Martinko J,Stahl D,et al.(2012)Brock Biology of Microorganisms.(13 Eth)Pearson Education.San Francisco,USA,pp 268-269.
Navarrete AA,Tsai SM,Mendes LW,et al.(2015)Soil microbiome responses to the short‐term effects of Amazonian deforestation.Molecular ecology 24(10):2433-2448.https://doi.org/10.1111/mec.13172
Otaki M,Takeuchi F,Tsuyuzaki S(2016)Changes in microbial community composition in the leaf litter of successional communities after volcanic eruptions of Mount Usu,northern Japan.Journal of Mountain Science 13(9):1652-1662.https://doi.org/10.1007/s11629-016-3835-4
Palleroni NJ(1997)Prokaryotic diversity and the importance of culturing.Antonie van Leeuwenhoek 72(1):3-19.https://doi.org/10.1023/A:1000394109961
Park N,Lee K,Jung S(2009)Estimation of Site Productivity of Pinus densiflora by the Soil Physico-chemical Properties.Korean Journal of Soil Science and Fertilizer 42(3):160-166.(In Korean)
Pfennig N(1975)The phototrophic bacteria and their role in the sulfur cycle.Plant and Soil 43(1-3):1-16.https://doi.org/10.1007/BF01928472
Pielou EC(1966)The measurement of diversity in different types of biological collections.Journal of theoretical biology 13:131-144.https://doi.org/10.1016/0022-5193(66)90013-0
Ratcliff AW,Busse MD,Shestak CJ(2006)Changes in microbial community structure following herbicide(glyphosate)additions to forest soils.Applied Soil Ecology 34(2):114-124.https://doi.org/10.1016/j.apsoil.2006.03.002
Rodr??guez H,Fraga R(1999)Phosphate solubilizing bacteria and their role in plant growth promotion.Biotechnology Advances17(4):319-339.https://doi.org/10.1016/S0734-9750(99)00014-2
Shaffer B,Widmer F,Porteous L,et al.(2000)Temporal and spatial distribution of the nif H gene of N2 fixing bacteria in forests and clearcuts in western Oregon.Microbial ecology 39(1):12-21.
Shannon CE(1948)A Mathematical Theory of Communication.Bell System Technical Journal 27(3):379-423.https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
Shuman L,Boswell F,Ohki K,et al.(1983)Effects of HC1 acid and lime amendments on soil ph and extractable Ca and Mg in a sandy soil.Communications in Soil Science&Plant Analysis 14(6):481-495.https://doi.org/10.1007/s002489900183
?ibanc N,Dumbrell AJ,Mandi?-Mulec I,et al.(2014)Impacts of naturally elevated soil CO2 concentrations on communities of soil archaea and bacteria.Soil Biology and Biochemistry 68:348-356.http://doi.org/10.1016/j.soilbio.2013.10.018
Smith SE,Read DJ(2010)Mycorrhizal symbiosis.Academic Press,USA.
Smith NR,Kishchuk BE,Mohn WW(2008)Effects of wildfire and harvest disturbances on forest soil bacterial communities.Applied and Environmental Microbiology 74(1):216-224.https://doi.org/10.1128/AEM.01355-07
Sokal Robert R,James RF(1969)Biometry.The principles and practice of statistics in biological research.San Francisco,USA.
?tursováM,?if?ákováL,Leigh MB,et al.(2012)Cellulose utilization in forest litter and soil:identification of bacterial and fungal decomposers.FEMS microbiology ecology 80(3):735-746.https://doi.org/10.1111/j.1574-6941.2012.01343.x
Torsvik V,Ovreas L,Thingstad TF(2002)Prokaryotic diversity--magnitude,dynamics,and controlling factors.Science 296(5570):1064-1066.https://doi.org/10.1126/science.1071698
van der Putten W,H.,Klironomos JN,Wardle DA(2007)Microbial ecology of biological invasions.1(1):28-37.https://doi.org/doi:10.1038/ismej.2007.9
Vesterdal L,Dalsgaard M,Felby C,et al.(1995)Effects of thinning and soil properties on accumulation of carbon,nitrogen and phosphorus in the forest floor of Norway spruce stands.Forest Ecology and Management 77(1-3):1-10.https://doi.org/10.1016/0378-1127(95)03579-Y
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