Soil Metagenome of Tropical White Sand Heath Forests in Borneo:What Functional Traits Are Associated with an Extreme Environment Within the Tropical Rainforest?
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摘要
White sand heath forests(WS) or kerangas, an unusual variant of tropical forests in Borneo, characterized by open scrubby vegetation, low productivity, and distinctive plant species composition and soil microbial community, are regarded as a stressful lowpH and/or nutrient environment. We investigated whether the functional soil metagenome also shows a predicted set of indicators of stressful conditions in WS. Based on stress-tolerant strategies exhibited by larger organisms, we hypothesized that genes for stress tolerance, dormancy, sporulation, and nutrient processing are more abundant in the soil microbiota of WS. We also hypothesized that there is less evidence of biotic interaction in white sand soils, with lower connectivity and fewer genes related to organismic interactions. In Brunei, we sampled soils from a WS and a normal primary dipterocarp forest, together with an inland heath, an intermediate forest type. Soil DNA was extracted, and shotgun sequencing was performed using Illumina HiSeq platform, with classification by the Metagenomics Rapid Annotation using Subsystem Technology(MG-RAST). The results, on one hand, supported our hypothesis(on greater abundance of dormancy, virulence, and sporulation-related genes). However, some aspects of our results showed no significant difference(specifically in stress tolerance, antibiotic resistance, viruses, and clustered regularly interspaced short palindrome repeats(CRISPRs)). It appears that in certain respects, the extreme white sand environment produces the predicted strategy of less biotic interaction, but exhibits high soil microbiota connectivity and functional diversity.
White sand heath forests(WS) or kerangas, an unusual variant of tropical forests in Borneo, characterized by open scrubby vegetation, low productivity, and distinctive plant species composition and soil microbial community, are regarded as a stressful lowpH and/or nutrient environment. We investigated whether the functional soil metagenome also shows a predicted set of indicators of stressful conditions in WS. Based on stress-tolerant strategies exhibited by larger organisms, we hypothesized that genes for stress tolerance, dormancy, sporulation, and nutrient processing are more abundant in the soil microbiota of WS. We also hypothesized that there is less evidence of biotic interaction in white sand soils, with lower connectivity and fewer genes related to organismic interactions. In Brunei, we sampled soils from a WS and a normal primary dipterocarp forest, together with an inland heath, an intermediate forest type. Soil DNA was extracted, and shotgun sequencing was performed using Illumina HiSeq platform, with classification by the Metagenomics Rapid Annotation using Subsystem Technology(MG-RAST). The results, on one hand, supported our hypothesis(on greater abundance of dormancy, virulence, and sporulation-related genes). However, some aspects of our results showed no significant difference(specifically in stress tolerance, antibiotic resistance, viruses, and clustered regularly interspaced short palindrome repeats(CRISPRs)). It appears that in certain respects, the extreme white sand environment produces the predicted strategy of less biotic interaction, but exhibits high soil microbiota connectivity and functional diversity.
White sand heath forests(WS) or kerangas, an unusual variant of tropical forests in Borneo, characterized by open scrubby vegetation, low productivity, and distinctive plant species composition and soil microbial community, are regarded as a stressful lowpH and/or nutrient environment. We investigated whether the functional soil metagenome also shows a predicted set of indicators of stressful conditions in WS. Based on stress-tolerant strategies exhibited by larger organisms, we hypothesized that genes for stress tolerance, dormancy, sporulation, and nutrient processing are more abundant in the soil microbiota of WS. We also hypothesized that there is less evidence of biotic interaction in white sand soils, with lower connectivity and fewer genes related to organismic interactions. In Brunei, we sampled soils from a WS and a normal primary dipterocarp forest, together with an inland heath, an intermediate forest type. Soil DNA was extracted, and shotgun sequencing was performed using Illumina HiSeq platform, with classification by the Metagenomics Rapid Annotation using Subsystem Technology(MG-RAST). The results, on one hand, supported our hypothesis(on greater abundance of dormancy, virulence, and sporulation-related genes). However, some aspects of our results showed no significant difference(specifically in stress tolerance, antibiotic resistance, viruses, and clustered regularly interspaced short palindrome repeats(CRISPRs)). It appears that in certain respects, the extreme white sand environment produces the predicted strategy of less biotic interaction, but exhibits high soil microbiota connectivity and functional diversity.
引文
Aanderud Z T,Vert J C,Lennon J T,Magnusson T W,Breakwell D P,Harker A R.2016.Bacterial dormancy is more prevalent in freshwater than hypersaline lakes.Front Microbiol.7:853.
Adeney J M,Christensen N L,Vicentini A,Cohn-Haft M.2016.White-sand ecosystems in Amazonia.Biotropica.48:7-23.
Allen S E,Grimshaw H M,Parkinson J A,Quarmby C.1974.Chemical Analysis of Ecological Materials.Blackwell Scientific Publications,Oxford.
Barber′an A,Bates S T,Casamayor E O,Fierer N.2012.Using network analysis to explore co-occurrence patterns in soil microbial communities.ISME J.6:343-351.
Bijlsma K,Loeschcke V.2013.Environmental Stress,Adaptation and Evolution.Birkh¨auser,Basel.
Charles J K,Ang B B.2010.Non-volant small mammal community responses to fragmentation of kerangas forests in Brunei Darussalam.Biodiver Conserv.19:543-561.
Chen S Y,Xu J,Maestre F T,Chu C J,Wang G,Xiao S.2009.Beyond dual-lattice models:Incorporating plant strategies when modeling the interplay between facilitation and competition along environmental severity gradients.J Theor Biol.258:266-273.
Choi S,Song H,Tripathi B M,Kerfahi D,Kim H,Adams J M.2017.Effect of experimental soil disturbance and recovery on structure and function of soil community:A metagenomic and metagenetic approach.Sci Rep.7:2260.
Cotrufo M F,Wallenstein M D,Boot C M,Denef K,Paul E.2013.The microbial efficiency-matrix stabilization(MEMS)framework integrates plant litter decomposition with soil organic matter stabilization:Do labile plant inputs form stable soil organic matter?Glob Change Biol.19:988-995.
Din H,Metali F,Sukri R S.2015.Tree diversity and community composition of the Tutong white sands,Brunei Darussalam:A rare tropical heath forest ecosystem.Int J Ecol.2015:807-876.
Disz T,Akhter S,Cuevas D,Olson R,Overbeek R,Vonstein V,Stevens R,Edwards R A.2010.Accessing the SEEDgenome databases via Web services API:Tools for programmers.BMC Bioinfor.11:319.
Dworkin J,Shah I M.2010.Exit from dormancy in microbial organisms.Nat Rev Microbiol.8:890-896.
Faust K,Raes J.2012.Microbial interactions:From networks to models.Nat Rev Microbiol.10:538-550.
Fierer N,Leff J W,Adams B J,Nielsen U N,Bates S T,Lauber C L,Owens S,Gilbert J A,Wall D H,Caporaso J G.2012.Cross-biome metagenomic analyses of soil microbial communities and their functional attributes.Proc Natl Acad Sci USA.109:21390-21395.
Frasier C L,Albert V A,Struwe L.2008.Amazonian lowland,white sand areas as ancestral regions for South American biodiversity:Biogeographic and phylogenetic patterns in Potalia(Angiospermae:Gentianaceae).Organisms Diver Evol.8:44-57.
Friedmann E I,Galun M.1974.Desert algae,lichens,and fungi.In Brown G W Jr(ed.)Desert Biology.Academic Press,New York.pp.165-212.
Grant K,Kreyling J,Heilmeier H,Beierkuhnlein C,Jentsch A.2014.Extreme weather events and plant-plant interactions:Shifts between competition and facilitation among grassland species in the face of drought and heavy rainfall.Ecol Res.29:991-1001.
Grime J P.1989.The stress debate:Symptom of impending synthesis?Biol J Linn Soc.37:3-17.
Grime J P.2006.Plant Strategies,Vegetation Processes,and Ecosystem Properties.2nd Edn.John Wiley&Sons,New York.
Herman D J,Firestone M K,Nuccio E,Hodge A.2012.Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition.FEMSMicrobiol Ecol.80:236-247.
Jiang L,Kulczycki A.2004.Competition,predation and species responses to environmental change.Oikos.106:217-224.
Katagiri S,Yamakura T,Lee S H.1991.Properties of soils in kerangas forest on sandstone at Bako national park,Sarawak,East Malaysia.Jpn J Southeast Asian Stud.29:35-48.
Kerfahi D,Tripathi B M,Porazinska D L,Park J,Go R,Adams J M.2016.Do tropical rain forest soils have greater nematode diversity than high Arctic tundra?A metagenetic comparison of Malaysia and Svalbard.Glob Ecol Biogeogr.25:716-728.
Lennon J T,Jones S E.2011.Microbial seed banks:The ecological and evolutionary implications of dormancy.Nat Rev Microbiol.9:119-130.
Levitt J.1980.Responses of Plants to Environmental Stress,Volume 1:Chilling,Freezing,and High Temperature Stresses.2nd Edn.Academic Press,New York.
Longton R E.1997.The role of bryophytes and lichens in polar ecosystems.Special Publication-British Ecol Soc.13:69-96.
Lubzens E,Cerda J,Clark M.2010.Dormancy and Resistance in Harsh Environments.Springer Science&Business Media,Berlin,Heidelberg.
L¨utzow M V,K¨ogel-Knabner I,Ekschmitt K,Matzner E,Guggenberger G,Marschner B,Flessa H.2006.Stabilization of organic matter in temperate soils:Mechanisms and their relevance under different soil conditions-a review.Eur J Soil Sci.57:426-445.
Maestre F T,Callaway R M,Valladares F,Lortie C J.2009.Refining the stress-gradient hypothesis for competition and facilitation in plant communities.J Ecol.97:199-205.
Mendes L W,Kuramae E E,Navarrete A A,van Veen J A,Tsai S M.2014.Taxonomical and functional microbial community selection in soybean rhizosphere.ISME J.8:1577-1587.
Meyer F,Paarmann D,D’Souza M,Olson R,Glass E M,Kubal M,Paczian T,Rodriguez A,Stevens R,Wilke A,Wilkening J,Edwards R A.2008.The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes.BMC Bioinfor.9:386.
Miyamoto K,Kohyama T S,Rahajoe J S,Mirmanto E,Simbolon H.2016a.Forest structure and productivity of tropical heath and peatland forests.In Osaki M,Tsuji N(eds.)Tropical Peatland Ecosystems.Springer,Tokyo.pp.151-166.
Miyamoto K,Suzuki E,Kohyama T,Seino T,Mirmanto E,Simbolon H.2003.Habitat differentiation among tree species with small-scale variation of humus depth and topography in a tropical heath forest of Central Kalimantan,Indonesia.J Trop Ecol.19:43-54.
Miyamoto K,Wagai R,Aiba S I,Nilus R.2016b.Variation in the aboveground stand structure and fine-root biomass of Bornean heath(kerangas)forests in relation to altitude and soil nitrogen availability.Trees.30:385-394.
Moran J A,Barker M G,Moran A J,Becker P,Ross S M.2000.Acomparison of the soil water,nutrient status,and litterfall characteristics of tropical heath and mixed-dipterocarp forest sites in Brunei.Biotropica.32:2-13.
Nadeem S M,Ahmad M,Zahir Z A,Javaid A,Ashraf M.2014.The role of mycorrhizae and plant growth promoting rhizobacteria(PGPR)in improving crop productivity under stressful environments.Biotechnol Adv.32:429-448.
Newbery D M.1991.Floristic variation within kerangas(heath)forest:Re-evaluation of data from Sarawak and Brunei.Vegetatio.96:43-86.
Odum H T.1971.Environment,Power,and Society.Wiley-Interscience,New York,USA.
Odum H T.2007.Environment,Power,and Society for the Twenty-First Century:The Hierarchy of Energy.Columbia University Press,Columbia.
Oksanen J,Kindt R,Legendre P,O’Hara B,Stevens M H H,Oksanen M J,Suggests M.2007.The vegan package.Commun Ecol Package.10:631-637.
Osaki M,Tsuji N.2015.Tropical Peatland Ecosystems.Springer,Tokyo.
Parker E D,Forbes V E,Nielsen S L,Ritter C,Barata C,Baird D J,Admiraal W,Levin L,Loeschke V,Lyytik¨ainenSaarenmaa P,H?gh-Jensen H,Calow P,Ripley B J.1999.Stress in ecological systems.Oikos.86:179-184.
Proctor J.1999.Heath forests and acid soils.Bot J Scot.51:1-14.
Proctor J,Anderson J M,Chai P,Vallack H W.1983.Ecological studies in four contrasting lowland rain forests in Gunung Mulu national park,Sarawak:I.Forest environment,structure and floristics.J Ecol.71:237-260.
Rodriguez R J,Redman R S,Henson J M.2004.The role of fungal symbioses in the adaptation of plants to high stress environments.Mitig Adapt Strat Global Change.9:261-272.
Schimel J,Balser T C,Wallenstein M.2007.Microbial stressresponse physiology and its implications for ecosystem function.Ecology.88:1386-1394.
Tripathi B M,Edwards D P,Mendes L W,Kim M,Dong K,Kim H,Adams J M.2016a.The impact of tropical forest logging and oil palm agriculture on the soil microbiome.Mol Ecol.25:2244-2257.
Tripathi B M,Kim M,Tateno R,Kim W,Wang J J,Lai-Hoe A,Shukor N A A,Rahim R A,Go R,Adams J M.2015.Soil pH and biome are both key determinants of soil archaeal community structure.Soil Biol Biochem.88:1-8.
Tripathi B M,Lee-Cruz L,Kim M,Singh D,Go R,Shukor N AA,Husni M H A,Chun J,Adams J M.2014.Spatial scaling effects on soil bacterial communities in Malaysian tropical forests.Microb Ecol.68:247-258.
Tripathi B M,Song W,Slik J W F,Sukri R S,Jaafar S,Dong K,Adams J M.2016b.Distinctive tropical forest variants have unique soil microbial communities,but not always low microbial diversity.Front Microbiol.7:376.
van der Heijden M G,Martin F M,Selosse M A,Sanders IR.2015.Mycorrhizal ecology and evolution:The past,the present,and the future.New Phytol.205:1406-1423.
van Horn D J,Okie J G,Buelow H N,Gooseff M N,Barrett J E,Takacs-Vesbach C D.2014.Soil microbial responses to increased moisture and organic resources along a salinity gradient in a polar desert.Appl Environ Microbiol.80:3034-3043.
Varin T,Lovejoy C,Jungblut A D,Vincent W F,Corbeil J.2012.Metagenomic analysis of stress genes in microbial mat communities from Antarctica and the high Arctic.Appl Environ Microbiol.78:549-559.
Vert J C.2013.Hypersaline Lake Environments Exhibit Reduced Microbial Dormancy.Brigham Young University,Brigham.
Wagg C,Bender S F,Widmer F,van der Heijden M G A.2014.Soil biodiversity and soil community composition determine ecosystem multifunctionality.Proc Natl Acad Sci USA.111:5266-5270.
Whitmore T C.1990.An Introduction to Tropical Rain Forests.Clarendon Press,Oxford.
Yang J,Kloepper J W,Ryu C M.2009.Rhizosphere bacteria help plants tolerate abiotic stress.Trends Plant Sci.14:1-4.
Zeller B,Liu J X,Buchmann N,Richter A.2008.Tree girdling increases soil N mineralisation in two spruce stands.Soil Biol Biochem.40:1155-1166.
Adeney J M,Christensen N L,Vicentini A,Cohn-Haft M.2016.White-sand ecosystems in Amazonia.Biotropica.48:7-23.
Allen S E,Grimshaw H M,Parkinson J A,Quarmby C.1974.Chemical Analysis of Ecological Materials.Blackwell Scientific Publications,Oxford.
Barber′an A,Bates S T,Casamayor E O,Fierer N.2012.Using network analysis to explore co-occurrence patterns in soil microbial communities.ISME J.6:343-351.
Bijlsma K,Loeschcke V.2013.Environmental Stress,Adaptation and Evolution.Birkh¨auser,Basel.
Charles J K,Ang B B.2010.Non-volant small mammal community responses to fragmentation of kerangas forests in Brunei Darussalam.Biodiver Conserv.19:543-561.
Chen S Y,Xu J,Maestre F T,Chu C J,Wang G,Xiao S.2009.Beyond dual-lattice models:Incorporating plant strategies when modeling the interplay between facilitation and competition along environmental severity gradients.J Theor Biol.258:266-273.
Choi S,Song H,Tripathi B M,Kerfahi D,Kim H,Adams J M.2017.Effect of experimental soil disturbance and recovery on structure and function of soil community:A metagenomic and metagenetic approach.Sci Rep.7:2260.
Cotrufo M F,Wallenstein M D,Boot C M,Denef K,Paul E.2013.The microbial efficiency-matrix stabilization(MEMS)framework integrates plant litter decomposition with soil organic matter stabilization:Do labile plant inputs form stable soil organic matter?Glob Change Biol.19:988-995.
Din H,Metali F,Sukri R S.2015.Tree diversity and community composition of the Tutong white sands,Brunei Darussalam:A rare tropical heath forest ecosystem.Int J Ecol.2015:807-876.
Disz T,Akhter S,Cuevas D,Olson R,Overbeek R,Vonstein V,Stevens R,Edwards R A.2010.Accessing the SEEDgenome databases via Web services API:Tools for programmers.BMC Bioinfor.11:319.
Dworkin J,Shah I M.2010.Exit from dormancy in microbial organisms.Nat Rev Microbiol.8:890-896.
Faust K,Raes J.2012.Microbial interactions:From networks to models.Nat Rev Microbiol.10:538-550.
Fierer N,Leff J W,Adams B J,Nielsen U N,Bates S T,Lauber C L,Owens S,Gilbert J A,Wall D H,Caporaso J G.2012.Cross-biome metagenomic analyses of soil microbial communities and their functional attributes.Proc Natl Acad Sci USA.109:21390-21395.
Frasier C L,Albert V A,Struwe L.2008.Amazonian lowland,white sand areas as ancestral regions for South American biodiversity:Biogeographic and phylogenetic patterns in Potalia(Angiospermae:Gentianaceae).Organisms Diver Evol.8:44-57.
Friedmann E I,Galun M.1974.Desert algae,lichens,and fungi.In Brown G W Jr(ed.)Desert Biology.Academic Press,New York.pp.165-212.
Grant K,Kreyling J,Heilmeier H,Beierkuhnlein C,Jentsch A.2014.Extreme weather events and plant-plant interactions:Shifts between competition and facilitation among grassland species in the face of drought and heavy rainfall.Ecol Res.29:991-1001.
Grime J P.1989.The stress debate:Symptom of impending synthesis?Biol J Linn Soc.37:3-17.
Grime J P.2006.Plant Strategies,Vegetation Processes,and Ecosystem Properties.2nd Edn.John Wiley&Sons,New York.
Herman D J,Firestone M K,Nuccio E,Hodge A.2012.Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition.FEMSMicrobiol Ecol.80:236-247.
Jiang L,Kulczycki A.2004.Competition,predation and species responses to environmental change.Oikos.106:217-224.
Katagiri S,Yamakura T,Lee S H.1991.Properties of soils in kerangas forest on sandstone at Bako national park,Sarawak,East Malaysia.Jpn J Southeast Asian Stud.29:35-48.
Kerfahi D,Tripathi B M,Porazinska D L,Park J,Go R,Adams J M.2016.Do tropical rain forest soils have greater nematode diversity than high Arctic tundra?A metagenetic comparison of Malaysia and Svalbard.Glob Ecol Biogeogr.25:716-728.
Lennon J T,Jones S E.2011.Microbial seed banks:The ecological and evolutionary implications of dormancy.Nat Rev Microbiol.9:119-130.
Levitt J.1980.Responses of Plants to Environmental Stress,Volume 1:Chilling,Freezing,and High Temperature Stresses.2nd Edn.Academic Press,New York.
Longton R E.1997.The role of bryophytes and lichens in polar ecosystems.Special Publication-British Ecol Soc.13:69-96.
Lubzens E,Cerda J,Clark M.2010.Dormancy and Resistance in Harsh Environments.Springer Science&Business Media,Berlin,Heidelberg.
L¨utzow M V,K¨ogel-Knabner I,Ekschmitt K,Matzner E,Guggenberger G,Marschner B,Flessa H.2006.Stabilization of organic matter in temperate soils:Mechanisms and their relevance under different soil conditions-a review.Eur J Soil Sci.57:426-445.
Maestre F T,Callaway R M,Valladares F,Lortie C J.2009.Refining the stress-gradient hypothesis for competition and facilitation in plant communities.J Ecol.97:199-205.
Mendes L W,Kuramae E E,Navarrete A A,van Veen J A,Tsai S M.2014.Taxonomical and functional microbial community selection in soybean rhizosphere.ISME J.8:1577-1587.
Meyer F,Paarmann D,D’Souza M,Olson R,Glass E M,Kubal M,Paczian T,Rodriguez A,Stevens R,Wilke A,Wilkening J,Edwards R A.2008.The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes.BMC Bioinfor.9:386.
Miyamoto K,Kohyama T S,Rahajoe J S,Mirmanto E,Simbolon H.2016a.Forest structure and productivity of tropical heath and peatland forests.In Osaki M,Tsuji N(eds.)Tropical Peatland Ecosystems.Springer,Tokyo.pp.151-166.
Miyamoto K,Suzuki E,Kohyama T,Seino T,Mirmanto E,Simbolon H.2003.Habitat differentiation among tree species with small-scale variation of humus depth and topography in a tropical heath forest of Central Kalimantan,Indonesia.J Trop Ecol.19:43-54.
Miyamoto K,Wagai R,Aiba S I,Nilus R.2016b.Variation in the aboveground stand structure and fine-root biomass of Bornean heath(kerangas)forests in relation to altitude and soil nitrogen availability.Trees.30:385-394.
Moran J A,Barker M G,Moran A J,Becker P,Ross S M.2000.Acomparison of the soil water,nutrient status,and litterfall characteristics of tropical heath and mixed-dipterocarp forest sites in Brunei.Biotropica.32:2-13.
Nadeem S M,Ahmad M,Zahir Z A,Javaid A,Ashraf M.2014.The role of mycorrhizae and plant growth promoting rhizobacteria(PGPR)in improving crop productivity under stressful environments.Biotechnol Adv.32:429-448.
Newbery D M.1991.Floristic variation within kerangas(heath)forest:Re-evaluation of data from Sarawak and Brunei.Vegetatio.96:43-86.
Odum H T.1971.Environment,Power,and Society.Wiley-Interscience,New York,USA.
Odum H T.2007.Environment,Power,and Society for the Twenty-First Century:The Hierarchy of Energy.Columbia University Press,Columbia.
Oksanen J,Kindt R,Legendre P,O’Hara B,Stevens M H H,Oksanen M J,Suggests M.2007.The vegan package.Commun Ecol Package.10:631-637.
Osaki M,Tsuji N.2015.Tropical Peatland Ecosystems.Springer,Tokyo.
Parker E D,Forbes V E,Nielsen S L,Ritter C,Barata C,Baird D J,Admiraal W,Levin L,Loeschke V,Lyytik¨ainenSaarenmaa P,H?gh-Jensen H,Calow P,Ripley B J.1999.Stress in ecological systems.Oikos.86:179-184.
Proctor J.1999.Heath forests and acid soils.Bot J Scot.51:1-14.
Proctor J,Anderson J M,Chai P,Vallack H W.1983.Ecological studies in four contrasting lowland rain forests in Gunung Mulu national park,Sarawak:I.Forest environment,structure and floristics.J Ecol.71:237-260.
Rodriguez R J,Redman R S,Henson J M.2004.The role of fungal symbioses in the adaptation of plants to high stress environments.Mitig Adapt Strat Global Change.9:261-272.
Schimel J,Balser T C,Wallenstein M.2007.Microbial stressresponse physiology and its implications for ecosystem function.Ecology.88:1386-1394.
Tripathi B M,Edwards D P,Mendes L W,Kim M,Dong K,Kim H,Adams J M.2016a.The impact of tropical forest logging and oil palm agriculture on the soil microbiome.Mol Ecol.25:2244-2257.
Tripathi B M,Kim M,Tateno R,Kim W,Wang J J,Lai-Hoe A,Shukor N A A,Rahim R A,Go R,Adams J M.2015.Soil pH and biome are both key determinants of soil archaeal community structure.Soil Biol Biochem.88:1-8.
Tripathi B M,Lee-Cruz L,Kim M,Singh D,Go R,Shukor N AA,Husni M H A,Chun J,Adams J M.2014.Spatial scaling effects on soil bacterial communities in Malaysian tropical forests.Microb Ecol.68:247-258.
Tripathi B M,Song W,Slik J W F,Sukri R S,Jaafar S,Dong K,Adams J M.2016b.Distinctive tropical forest variants have unique soil microbial communities,but not always low microbial diversity.Front Microbiol.7:376.
van der Heijden M G,Martin F M,Selosse M A,Sanders IR.2015.Mycorrhizal ecology and evolution:The past,the present,and the future.New Phytol.205:1406-1423.
van Horn D J,Okie J G,Buelow H N,Gooseff M N,Barrett J E,Takacs-Vesbach C D.2014.Soil microbial responses to increased moisture and organic resources along a salinity gradient in a polar desert.Appl Environ Microbiol.80:3034-3043.
Varin T,Lovejoy C,Jungblut A D,Vincent W F,Corbeil J.2012.Metagenomic analysis of stress genes in microbial mat communities from Antarctica and the high Arctic.Appl Environ Microbiol.78:549-559.
Vert J C.2013.Hypersaline Lake Environments Exhibit Reduced Microbial Dormancy.Brigham Young University,Brigham.
Wagg C,Bender S F,Widmer F,van der Heijden M G A.2014.Soil biodiversity and soil community composition determine ecosystem multifunctionality.Proc Natl Acad Sci USA.111:5266-5270.
Whitmore T C.1990.An Introduction to Tropical Rain Forests.Clarendon Press,Oxford.
Yang J,Kloepper J W,Ryu C M.2009.Rhizosphere bacteria help plants tolerate abiotic stress.Trends Plant Sci.14:1-4.
Zeller B,Liu J X,Buchmann N,Richter A.2008.Tree girdling increases soil N mineralisation in two spruce stands.Soil Biol Biochem.40:1155-1166.