The effects of afforestation on soil bacterial communities in temperate grassland are modulated by soil chemical properties

PeerJ - Tập 7 - Trang e6147
Shuhong Wu1, Bing Huang2, Jian Gao3, Siqi Wang1, Pei‐Chun Liao2
1School of Nature Conservation, Beijing Forestry University, Beijing, China
2Department of Life Science, National Taiwan Normal University, Taipei, Taiwan
3Faculty of Resources and Environment, Baotou Teachers’ College, Inner Mongolia University of Science and Technology, Inner Mongolia, China

Tóm tắt

Grassland afforestation dramatically affects the abiotic, biotic, and ecological function properties of the original ecosystems. Interference from afforestation might disrupt the stasis of soil physicochemical properties and the dynamic balance of microbiota. Some studies have suggested low sensitivity of soil properties and bacterial community to afforestation, but the apparent lack of a significant relationship is probably due to the confounding effects of the generalist habitat and rare bacterial communities. In this study, soil chemical and prokaryotic properties in a 30-year-old Mongolia pine (Pinus sylvestrisvar.mongolicaLitv.) afforested region and adjacent grassland in Inner Mongolia were classified and quantified. Our results indicate that the high richness of rare microbes accounts for the alpha-diversity of the soil microbiome. Few OTUs of generalist (core bacteria) and habitat-specialist bacteria are present. However, the high abundance of this small number of OTUs governs the beta-diversity of the grassland and afforested land bacterial communities. Afforestation has changed the soil chemical properties, thus indirectly affecting the soil bacterial composition rather than richness. The contents of soil P, Ca2+, and Fe3+account for differentially abundant OTUs such as Planctomycetes and subsequent changes in the ecologically functional potential of soil bacterial communities due to grassland afforestation. We conclude that grassland afforestation has changed the chemical properties and composition of the soil and ecological functions of the soil bacterial community and that these effects of afforestation on the microbiome have been modulated by changes in soil chemical properties.

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Tài liệu tham khảo

Ahrends, 2017, China’s fight to halt tree cover loss, Proceedings of the Royal Society B: Biological Sciences, 284, 10.1098/rspb.2016.2559

Ai, 2013, Migration and niche partitioning simultaneously increase species richness and rarity, Ecological Modelling, 258, 33, 10.1016/j.ecolmodel.2013.03.001

Arnáez, 2015, Effects of farming terraces on hydrological and geomorphological processes. A review, CATENA, 128, 122, 10.1016/j.catena.2015.01.021

Beever, 1981, Phosphorus uptake, storage and utilization by fungi, Advances in Botanical Research, 8, 127, 10.1016/S0065-2296(08)60034-8

Berger, 2015, Decomposition of beech (Fagus sylvatica) and pine (Pinus nigra) litter along an Alpine elevation gradient: decay and nutrient release, Geoderma, 251–252, 92, 10.1016/j.geoderma.2015.03.024

Bond, 2012, Carbon dioxide and the uneasy interactions of trees and savannah grasses, Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 601, 10.1098/rstb.2011.0182

Buckley, 2006, Diversity of Planctomycetes in soil in relation to soil history and environmental heterogeneity, Applied and Environmental Microbiology, 72, 4522, 10.1128/AEM.00149-06

Burke, 2011, Bacterial community assembly based on functional genes rather than species, Proceedings of the National Academy of Sciences of the United States of America, 108, 14288, 10.1073/pnas.1101591108

Caporaso, 2010, QIIME allows analysis of high-throughput community sequencing data, Nature Methods, 7, 335, 10.1038/nmeth.f.303

Chazdon, 2011, A novel statistical method for classifying habitat generalists and specialists, Ecology, 92, 1332, 10.1890/10-1345.1

Chen, 2008, Impacts of grassland afforestation with coniferous trees on soil phosphorus dynamics and associated microbial processes: a review, Forest Ecology and Management, 255, 396, 10.1016/j.foreco.2007.10.040

Chudzińska, 2014, Adaptation strategies and referencing trial of Scots and black pine populations subjected to heavy metal pollution, Environmental Science and Pollution Research, 21, 2165, 10.1007/s11356-013-2081-3

Cibils, 2015, Functional diversity of algal communities from headwater grassland streams: how does it change following afforestation?, Aquatic Ecology, 49, 453, 10.1007/s10452-015-9538-z

Cole, 2007, The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data, Nucleic Acids Research, 35, D169, 10.1093/nar/gkl889

Cunningham, 2015, Balancing the environmental benefits of reforestation in agricultural regions, Perspectives in Plant Ecology, Evolution and Systematics, 17, 301, 10.1016/j.ppees.2015.06.001

De Marco, 2007, Nutrient dynamics during decomposition of four different pine litters, Options Méditerranéennes Série A: Séminaires Méditerranéens, 75, 73

De Vries, 2012, Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities, Ecology Letters, 15, 1230, 10.1111/j.1461-0248.2012.01844.x

DeSantis, 2006, Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB, Applied and Environmental Microbiology, 72, 5069, 10.1128/AEM.03006-05

Dixon, 2003, VEGAN, a package of R functions for community ecology, Journal of Vegetation Science, 14, 927, 10.1658/1100-9233(2003)014[0927:vaporf]2.0.co;2

Edgar, 2013, UPARSE: highly accurate OTU sequences from microbial amplicon reads, Nature Methods, 10, 996, 10.1038/nmeth.2604

Edgar, 2011, UCHIME improves sensitivity and speed of chimera detection, Bioinformatics, 27, 2194, 10.1093/bioinformatics/btr381

Eilers, 2012, Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil, Soil Biology and Biochemistry, 50, 58, 10.1016/j.soilbio.2012.03.011

Emerson, 2015, Microbial iron oxidation in the arctic tundra and its implications for biogeochemical cycling, Applied and Environmental Microbiology, 81, 8066, 10.1128/AEM.02832-15

Ewing, 1998, Base-calling of automated sequencer traces using Phred. II. error probabilities, Genome Research, 8, 186, 10.1101/gr.8.3.186

Ewing, 1998, Base-calling of automated sequencer traces using Phred.I. Accuracy, assessment, Genome Research, 8, 175, 10.1101/gr.8.3.175

Falkowski, 2008, The microbial engines that drive earth’s biogeochemical cycles, Science, 320, 1034, 10.1126/science.1153213

Fenchel, 2012, Chapter 1—bacterial metabolism, Bacterial biogeochemistry, 3, 1, 10.1016/B978-0-12-415836-8.00001-3

Fenchel, 2012, Chapter 6—biogeochemical cycling in soils, Bacterial biogeochemistry, 3, 89, 10.1016/B978-0-12-415836-8.00006-2

Fierer, 2003, Variations in microbial community composition through two soil depth profiles, Soil Biology and Biochemistry, 35, 167, 10.1016/S0038-0717(02)00251-1

García-Fernández, 2004, Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimized nitrogen utilization in oligotrophic environments, Microbiology and Molecular Biology Reviews, 68, 630, 10.1128/MMBR.68.4.630-638.2004

Gobet, 2012, Diversity and dynamics of rare and of resident bacterial populations in coastal sands, ISME Journal, 6, 542, 10.1038/ismej.2011.132

Gudelj, 2010, An integrative approach to understanding microbial diversity: from intracellular mechanisms to community structure, Ecology Letters, 13, 1073, 10.1111/j.1461-0248.2010.01507.x

Gunina, 2017, Response of soil microbial community to afforestation with pure and mixed species, Plant and Soil, 412, 357, 10.1007/s11104-016-3073-0

He, 2008, Forest change of China in recent 300 years, Journal of Geographical Sciences, 18, 59, 10.1007/s11442-008-0059-8

Hurme, 1997, Climatic adaptation of bud set and frost hardiness in Scots pine (Pinus sylvestris), Canadian Journal of Forest Research, 27, 716, 10.1139/x97-052

Jangid, 2011, Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties, Soil Biology and Biochemistry, 43, 2184, 10.1016/j.soilbio.2011.06.022

Jombart, 2008, adegenet: a R package for the multivariate analysis of genetic markers, Bioinformatics, 24, 1403, 10.1093/bioinformatics/btn129

Jousset, 2017, Where less may be more: how the rare biosphere pulls ecosystems strings, ISME Journal, 11, 853, 10.1038/ismej.2016.174

Khamzina, 2016, Above- and belowground litter stocks and decay at a multi-species afforestation site on arid, saline soil, Nutrient Cycling in Agroecosystems, 104, 187, 10.1007/s10705-016-9766-1

Klein, 1995, Saprophytic fungal-bacterial biomass variations in successional communities of a semi-arid steppe ecosystem, Biology and Fertility of Soils, 19, 253, 10.1007/BF00336168

Konneke, 2005, Isolation of an autotrophic ammonia-oxidizing marine archaeon, Nature, 437, 543, 10.1038/nature03911

Krakau, 2013, Scots Pine (Pinus sylvestris L.), Forest tree breeding in europe: current state-of-the-art and perspectives, 267, 10.1007/978-94-007-6146-9_6

Lafleur, 2015, Organic carbon accumulation in topsoil following afforestation with willow: emphasis on leaf litter decomposition and soil organic matter quality, Forests, 6, 769, 10.3390/f6030769

Lange, 2014, Biotic and abiotic properties mediating plant diversity effects on soil microbial communities in an experimental grassland, PLOS ONE, 9, e96182, 10.1371/journal.pone.0096182

Langille, 2013, Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences, Nature Biotechnology, 31, 814, 10.1038/nbt.2676

Lauber, 2009, Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale, Applied and Environmental Microbiology, 75, 5111, 10.1128/aem.00335-09

Li, 2004, Microbial biomass and bacterial functional diversity in forest soils: effects of organic matter removal, compaction, and vegetation control, Soil Biology and Biochemistry, 36, 571, 10.1016/j.soilbio.2003.12.001

Li, 2016, Potential and actual impacts of deforestation and afforestation on land surface temperature, Journal of Geophysical Research: Atmospheres, 121, 14,372, 10.1002/2016JD024969

Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biology, 15, 10.1186/s13059-014-0550-8

Lu, 2017, Plant–soil interaction affects the mineralization of soil organic carbon: evidence from 73-year-old plantations with three coniferous tree species in subtropical Australia, Journal of Soils and Sediments, 17, 985, 10.1007/s11368-016-1602-3

Ma, 2013, Impacts of vegetation change on the regional surface climate: a scenario-based analysis of afforestation in Jiangxi Province, China, Advances in Meteorology, 2013, 10.1155/2013/796163

Márquez, 2015, Stream macroinvertebrate communities change with grassland afforestation in central Argentina, Limnologica—Ecology and Management of Inland Waters, 53, 17, 10.1016/j.limno.2015.05.002

McGill, 2007, Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework, Ecology Letters, 10, 995, 10.1111/j.1461-0248.2007.01094.x

Mendes, 2014, Taxonomical and functional microbial community selection in soybean rhizosphere, ISME Journal, 8, 1577, 10.1038/ismej.2014.17

Mizrahi-Man, 2013, Taxonomic classification of bacterial 16S rRNA genes using short sequencing reads: evaluation of effective study designs, PLOS ONE, 8, e53608, 10.1371/journal.pone.0053608

Narisawa, 2008, Coexistence of antibiotic-producing and antibiotic-sensitive bacteria in biofilms is mediated by resistant bacteria, Applied and Environmental Microbiology, 74, 3887, 10.1128/AEM.02497-07

Nosetto, 2008, Regional patterns and controls of ecosystem salinization with grassland afforestation along a rainfall gradient, Global Biogeochemical Cycles, 22, 10.1029/2007GB003000

Oleksyn, 2003, Nutrient conservation increases with latitude of origin in European Pinus sylvestris populations, Oecologia, 136, 220, 10.1007/s00442-003-1265-9

Pedley, 2014, Commercial spruce plantations support a limited canopy fauna: evidence from a multi taxa comparison of native and plantation forests, Forest Ecology and Management, 314, 172, 10.1016/j.foreco.2013.12.010

Peng, 2014, Afforestation in China cools local land surface temperature, Proceedings of the National Academy of Sciences of the United States of America, 111, 2915, 10.1073/pnas.1315126111

R Core Team, 2013, R: a language and environment for statistical computing

Ren, 2016, Responsiveness of soil nitrogen fractions and bacterial communities to afforestation in the Loess Hilly Region (LHR) of China, Scientific Reports, 6, 28469, 10.1038/srep28469

Rodŕıguez, 1999, Phosphate solubilizing bacteria and their role in plant growth promotion, Biotechnology Advances, 17, 319, 10.1016/S0734-9750(99)00014-2

Savolainen, 2004, Genetic variation in cessation of growth and frost hardiness and consequences for adaptation of Pinus sylvestris to climatic changes, Forest Ecology and Management, 197, 79, 10.1016/j.foreco.2004.05.006

Schloss, 2009, Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities, Applied and Environmental Microbiology, 75, 7537, 10.1128/AEM.01541-09

Schluter, 2015, Adhesion as a weapon in microbial competition, ISME Journal, 9, 139, 10.1038/ismej.2014.174

Sharma, 1998, Oxidation of ammonia by ferrate(vi), Journal of Environmental Science and Health, Part A, 33, 635, 10.1080/10934529809376752

Shen, 2011, Phosphorus dynamics: from soil to plant, Plant Physiology, 156, 997, 10.1104/pp.111.175232

Shen, 2008, Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam, Environmental Microbiology, 10, 1601, 10.1111/j.1462-2920.2008.01578.x

Šnajdr, 2013, Dominant trees affect microbial community composition and activity in post-mining afforested soils, Soil Biology and Biochemistry, 56, 105, 10.1016/j.soilbio.2012.05.004

Song, 2008, Dynamics and relationships of Ca, Mg, Fe in litter, soil fauna and soil in Pinus koraiensis-broadleaf mixed forest, Chinese Geographical Science, 18, 284, 10.1007/s11769-008-0284-1

Spallek, 2009, How microbes utilize host ubiquitination, Cellular Microbiology, 11, 1425, 10.1111/j.1462-5822.2009.01346.x

State Forestry Administration of China, 2011, China National Progress report to the UNFF Secretariat on the implementation of NLBI and other relevant resolutions

Stieglmeier, 2014, The phylum Thaumarchaeota, The Prokaryotes: other major lineages of bacteria and the archaea, 347, 10.1007/978-3-642-38954-2_338

Stutter, 2012, Relationships between soil physicochemical, microbiological properties, and nutrient release in buffer soils compared to field soils, Journal of Environmental Quality, 41, 400, 10.2134/jeq2010.0456

Székely, 2014, The importance of species sorting differs between habitat generalists and specialists in bacterial communities, FEMS Microbiology Ecology, 87, 102, 10.1111/1574-6941.12195

Verberk, 2011, Explaining general patterns in species abundance and distributions, Nature Education Knowledge, 3

Wang, 2016, Changes of soil C stocks and stability after 70-year afforestation in the Northeast USA, Plant and Soil, 401, 319, 10.1007/s11104-015-2755-3

Wen, 2002, Relationships between bird communities and vegetation structure in Honghua’erji, northern inner Mongolia, Journal of Forestry Research, 13, 294, 10.1007/BF02860095

Wu, 2018, The Aboveground vegetation type and underground soil property mediate the divergence of soil microbiomes and the biological interactions, Microbial Ecology, 75, 434, 10.1007/s00248-017-1050-7

Xiao, 2017, Changes in microbial communities and respiration following the revegetation of eroded soil, Agriculture, Ecosystems & Environment, 246, 30, 10.1016/j.agee.2017.05.026

Zechmeister-Boltenstern, 2015, The application of ecological stoichiometry to plant–microbial–soil organic matter transformations, Ecological Monographs, 85, 133, 10.1890/14-0777.1

Zheng, 2017, A long-term hybrid poplar plantation on cropland reduces soil organic carbon mineralization and shifts microbial community abundance and composition, Applied Soil Ecology, 111, 94, 10.1016/j.apsoil.2016.11.017