Soil microbiome mediated nutrients decline during forest degradation process
Yangying Liu, Shang Wang, Zhujun Wang, Zhaojing Zhang, Huayu Qin, Ziyan Wei, Kai Feng, Shuzhen Li, Yueni Wu, Huaqun Yin, Hui Li, Ye Deng
Soil microbiome mediated nutrients decline during forest degradation process
Degradation succession in forests is an important and serious land use/cover change problem in ecology, and during these processes soil microbial communities mediate the recycling of most important nutrients. To reveal the effect of degradation succession processes on soil microbial community diversity, structure, and species interrelationships, we collected abundant samples (21 per vegetation type) in broad-leaved forest, coniferous forest, and meadow to observe the microbial community dynamics. The results showed that diversity and structure of soil prokaryotic and fungal communities responded differently to different forest degradation processes, diversity of soil microbial communities increased during degradation processes. Soil microbial communities abundance changes may indicate that prokaryotic communities showed a living strategies change as an ecological adaption to harsh conditions during forest degradation process. While for fungal communities, their abundance changes may indicate that environmental selection pressure and plant selectivity during forest degradation process. Changes in soil prokaryotic communities and fungal communities were both correlated with soil carbon and nitrogen loss. The soil microbial interaction network analysis indicated more complex species interrelationships formed due to the loss of soil nutrients during degradation succession processes, suggesting soil microbial communities might form more complex and stable networks to resist the external disturbance of soil nutrient loss. All results suggested soil microorganisms, including bacteria, archaea and fungi, all involved in the soil nutrient decline during the forest degradation process.
microbial communities / degradation succession / soil nutrients / high-throughput sequencing / molecular ecological networks
[1] |
Anderson, I.C., Genney, D.R., Alexander, I.J., 2014. Fine-scale diversity and distribution of ectomycorrhizal fungal mycelium in a Scots pine forest. New Phytologist 201, 1423–1430
CrossRef
Pubmed
Google scholar
|
[2] |
Avis, P.G., 2012. Ectomycorrhizal iconoclasts: the ITS rDNA diversity and nitrophilic tendencies of fetid Russula. Mycologia 104, 998–1007
CrossRef
Pubmed
Google scholar
|
[3] |
Avis, P.G., Charvat, I., 2005. The response of ectomycorrhizal fungal inoculum to long-term increases in nitrogen supply. Mycologia 97, 329–337
CrossRef
Pubmed
Google scholar
|
[4] |
Baldrian, P., 2017. Forest microbiome: diversity, complexity and dynamics. FEMS Microbiology Reviews 41, 109–130.
Pubmed
|
[5] |
Baldrian, P., Merhautova, V., Cajthaml, T., Petrankova, M., Snajdr, J., 2010. Small-scale distribution of extracellular enzymes, fungal, and bacterial biomass in Quercus petraea forest topsoil. Biology and Fertility of Soils 46, 717–726
CrossRef
Google scholar
|
[6] |
Bastida, F., Garcia, C., von Bergen, M., Moreno, J.L., Richnow, H.H., Jehmlich, N., 2015. Deforestation fosters bacterial diversity and the cyanobacterial community responsible for carbon fixation processes under semiarid climate: a metaproteomics study. Applied Soil Ecology 93, 65–67
CrossRef
Google scholar
|
[7] |
Bird, S.B., Herrick, J.E., Wander, M.M., Wright, S.F., 2002. Spatial heterogeneity of aggregate stability and soil carbon in semi-arid rangeland. Environmental Pollution 116, 445–455
CrossRef
Pubmed
Google scholar
|
[8] |
Borneman, J., Triplett, E.W., 1997. Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. Applied and Environmental Microbiology 63, 2647–2653.
Pubmed
|
[9] |
Cao, S.X., 2011. Impact of China’s Large-Scale Ecological Restoration Program on the Environment and Society in Arid and Semiarid Areas of China: Achievements, Problems, Synthesis, and Applications. Critical Reviews in Environmental Science and Technology 41, 317–335
CrossRef
Google scholar
|
[10] |
Cashore, B., Gale, F., Meidinger, E., Newsom, D., 2006. Confronting sustainability: forest certification in developing and transitioning countries. Yale University Faculty of Environmental Studies Publication Series.
|
[11] |
Celentano, D., Rousseau, G.X., Engel, V.L., Zelarayan, M., Oliveira, E.C., Araujo, A.C.M., de Moura, E.G., 2017. Degradation of Riparian Forest Affects Soil Properties and Ecosystem Services Provision in Eastern Amazon of Brazil. Land Degradation & Development 28, 482–493
CrossRef
Google scholar
|
[12] |
Cox, F., Barsoum, N., Lilleskov, E.A., Bidartondo, M.I., 2010. Nitrogen availability is a primary determinant of conifer mycorrhizas across complex environmental gradients. Ecology Letters 13, 1103–1113
CrossRef
Pubmed
Google scholar
|
[13] |
Crowther, T.W., Maynard, D.S., Leff, J.W., Oldfield, E.E., McCulley, R.L., Fierer, N., Bradford, M.A., 2014. Predicting the responsiveness of soil biodiversity to deforestation: a cross-biome study. Global Change Biology 20, 2983–2994
CrossRef
Pubmed
Google scholar
|
[14] |
de Vries, F.T., Liiri, M.E., Bjornlund, L., Bowker, M.A., Christensen, S., Setala, H.M., Bardgett, R.D., 2012. Land use alters the resistance and resilience of soil food webs to drought. Nature Climate Change 2, 276–280
CrossRef
Google scholar
|
[15] |
Deng, Y., Jiang, Y.H., Yang, Y., He, Z., Luo, F., Zhou, J., 2012. Molecular ecological network analyses. BMC Bioinformatics 13, 113
CrossRef
Pubmed
Google scholar
|
[16] |
Dighton, J., Jones, H.E., Robinson, C.H., Beckett, J., 1997. The role of abiotic factors, cultivation practices and soil fauna in the dispersal of genetically modified microorganisms in soils. Applied Soil Ecology 5, 109–131
CrossRef
Google scholar
|
[17] |
Edgar, R.C., 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996–998
CrossRef
Pubmed
Google scholar
|
[18] |
Falkowski, P.G., Fenchel, T., Delong, E.F., 2008. The microbial engines that drive Earth’s biogeochemical cycles. Science 320, 1034–1039
CrossRef
Pubmed
Google scholar
|
[19] |
Faust, K., Raes, J., 2012. Microbial interactions: from networks to models. Nature Reviews. Microbiology 10, 538–550
CrossRef
Pubmed
Google scholar
|
[20] |
Feng, C., Ma, Y., Fu, S.L., Chen, H.Y.H., 2017a. Soil Carbon and Nutrient Dynamics Following Cessation of Anthropogenic Disturbances in Degraded Subtropical Forests. Land Degradation & Development 28, 2457–2467
CrossRef
Google scholar
|
[21] |
Feng, K., Zhang, Z., Cai, W., Liu, W., Xu, M., Yin, H., Wang, A., He, Z., Deng, Y., 2017b. Biodiversity and species competition regulate the resilience of microbial biofilm community. Molecular Ecology 26, 6170–6182
CrossRef
Pubmed
Google scholar
|
[22] |
Fierer, N., 2017. Embracing the unknown: disentangling the complexities of the soil microbiome. Nature Reviews. Microbiology 15, 579–590
CrossRef
Pubmed
Google scholar
|
[23] |
Fierer, N., Jackson, R.B., 2006. The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America 103, 626–631
CrossRef
Pubmed
Google scholar
|
[24] |
Frąc, M., Hannula, S.E., Bełka, M., Jędryczka, M., 2018. Fungal Biodiversity and Their Role in Soil Health. Frontiers in Microbiology 9, 707
CrossRef
Pubmed
Google scholar
|
[25] |
Ghazoul, J., Burivalova, Z., Garcia-Ulloa, J., King, L.A., 2015. Conceptualizing Forest Degradation. Trends in Ecology & Evolution 30, 622–632
CrossRef
Pubmed
Google scholar
|
[26] |
Grundmann, G.L., Debouzie, D., 2000. Geostatistical analysis of the distribution of NH(4)(+) and NO(2)(-)-oxidizing bacteria and serotypes at the millimeter scale along a soil transect. FEMS Microbiology Ecology 34, 57–62.
Pubmed
|
[27] |
Guo, L.B., Gifford, R.M., 2002. Soil carbon stocks and land use change: a meta analysis. Global Change Biology 8, 345–360
CrossRef
Google scholar
|
[28] |
Heijnen, C.E., Chenu, C., Robert, M., 1993. Micro-morphological studies on clay-amended and unamended Loamy Sand, relating survival of introduced bacteria and soil structure. Geoderma 56, 195–207
CrossRef
Google scholar
|
[29] |
Kaiser, K., Wemheuer, B., Korolkow, V., Wemheuer, F., Nacke, H., Schöning, I., Schrumpf, M., Daniel, R., 2016. Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests. Scientific Reports 6, 33696.
CrossRef
Pubmed
Google scholar
|
[30] |
Kang, S., Mills, A.L., 2006. The effect of sample size in studies of soil microbial community structure. Journal of Microbiological Methods 66, 242–250
CrossRef
Pubmed
Google scholar
|
[31] |
Kong, Y., 2011. Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies. Genomics 98, 152–153
CrossRef
Pubmed
Google scholar
|
[32] |
Kranabetter, J.M., Friesen, J., Gamiet, S., Kroeger, P., 2009. Epigeous fruiting bodies of ectomycorrhizal fungi as indicators of soil fertility and associated nitrogen status of boreal forests. Mycorrhiza 19, 535–548
CrossRef
Pubmed
Google scholar
|
[33] |
Lang, C., Seven, J., Polle, A., 2011. Host preferences and differential contributions of deciduous tree species shape mycorrhizal species richness in a mixed Central European forest. Mycorrhiza 21, 297–308
CrossRef
Pubmed
Google scholar
|
[34] |
Lauber, C.L., Strickland, M.S., Bradford, M.A., Fierer, N., 2008. The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biology & Biochemistry 40, 2407–2415
CrossRef
Google scholar
|
[35] |
Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G.W., Prosser, J.I., Schuster, S.C., Schleper, C., 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809
CrossRef
Pubmed
Google scholar
|
[36] |
Li, L.L., Jiang, W.J., Du, L.H., Liu, G.L., Wu, J.G., 2008. Biodiversity and Protection Strategies of Songshan Nature Reserve. Sichuan Forestry Exploration and Design 4, 004.
|
[37] |
Lin, Y.T., Whitman, W.B., Coleman, D.C., Chih-Yu, C., 2011. Molecular characterization of soil bacterial community in a perhumid, low mountain forest. Microbes and Environments 26, 325–331
CrossRef
Pubmed
Google scholar
|
[38] |
Luo, F., Yang, Y., Zhong, J., Gao, H., Khan, L., Thompson, D.K., Zhou, J., 2007. Constructing gene co-expression networks and predicting functions of unknown genes by random matrix theory. BMC Bioinformatics 8, 299
CrossRef
Pubmed
Google scholar
|
[39] |
Magoč, T., Salzberg, S.L., 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics (Oxford, England) 27, 2957–2963
CrossRef
Pubmed
Google scholar
|
[40] |
Marin-Spiotta, E., Silver, W.L., Swanston, C.W., Ostertag, R., 2009. Soil organic matter dynamics during 80 years of reforestation of tropical pastures. Global Change Biology 15, 1584–1597
CrossRef
Google scholar
|
[41] |
Mueller, R.C., Paula, F.S., Mirza, B.S., Rodrigues, J.L.M., Nüsslein, K., Bohannan, B.J.M., 2014. Links between plant and fungal communities across a deforestation chronosequence in the Amazon rainforest. ISME Journal 8, 1548–1550
CrossRef
Pubmed
Google scholar
|
[42] |
Navarrete, A.A., Tsai, S.M., Mendes, L.W., Faust, K., de Hollander, M., Cassman, N.A., Raes, J., van Veen, J.A., Kuramae, E.E., 2015. Soil microbiome responses to the short-term effects of Amazonian deforestation. Molecular Ecology 24, 2433–2448
CrossRef
Pubmed
Google scholar
|
[43] |
Öpik, M., Zobel, M., Cantero, J.J., Davison, J., Facelli, J.M., Hiiesalu, I., Jairus, T., Kalwij, J.M., Koorem, K., Leal, M.E., Liira, J., Metsis, M., Neshataeva, V., Paal, J., Phosri, C., Põlme, S., Reier, Ü., Saks, Ü., Schimann, H., Thiéry, O., Vasar, M., Moora, M., 2013. Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23, 411–430
CrossRef
Pubmed
Google scholar
|
[44] |
Osono, T., 2006. Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter. Canadian Journal of Microbiology 52, 701–716
CrossRef
Pubmed
Google scholar
|
[45] |
Osono, T., Hirose, D., Fujimaki, R., 2006. Fungal colonization as affected by litter depth and decomposition stage of needle litter. Soil Biology & Biochemistry 38, 2743–2752
CrossRef
Google scholar
|
[46] |
Pinzari, F., Reverberi, M., Pinar, G., Maggi, O., Persiani, A.M., 2014. Metabolic profiling of Minimedusa polyspora (Hotson) Weresub & P.M. LeClair, a cellulolytic fungus isolated from Mediterranean maquis, in southern Italy. Plant Biosystems 148, 333–341
CrossRef
Google scholar
|
[47] |
Powers, J.S., Corre, M.D., Twine, T.E., Veldkamp, E., 2011. Geographic bias of field observations of soil carbon stocks with tropical land-use changes precludes spatial extrapolation. Proceedings of the National Academy of Sciences of the United States of America 108, 6318–6322
CrossRef
Pubmed
Google scholar
|
[48] |
Prescott, C.E., Grayston, S.J., 2013. Tree species influence on microbial communities in litter and soil: Current knowledge and research needs. Forest Ecology and Management 309, 19–27
CrossRef
Google scholar
|
[49] |
Ranjard, L., Richaume, A., 2001. Quantitative and qualitative microscale distribution of bacteria in soil. Research in Microbiology 152, 707–716
CrossRef
Pubmed
Google scholar
|
[50] |
Rodrigues, J.L.M., Pellizari, V.H., Mueller, R., Baek, K., Jesus, E.C., Paula, F.S., Mirza, B., Hamaoui, G.S. Jr, Tsai, S.M., Feigl, B., Tiedje, J.M., Bohannan, B.J.M., Nüsslein, K., 2013. Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America 110, 988–993
CrossRef
Pubmed
Google scholar
|
[51] |
Rousk, J., Bååth, E., Brookes, P.C., Lauber, C.L., Lozupone, C., Caporaso, J.G., Knight, R., Fierer, N., 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME Journal 4, 1340–1351
CrossRef
Pubmed
Google scholar
|
[52] |
Saetre, P., 1999. Spatial patterns of ground vegetation, soil microbial biomass and activity in a mixed spruce-birch stand. Ecography 22, 183–192
CrossRef
Google scholar
|
[53] |
Sahani, U., Behera, N., 2001. Impact of deforestation on soil physicochemical characteristics, microbial biomass and microbial activity of tropical soil. Land Degradation & Development 12, 93–105
CrossRef
Google scholar
|
[54] |
Sasaki, N., Putz, F.E., 2009. Critical need for new definitions of “forest” and “forest degradation” in global climate change agreements. Conservation Letters 2, 226–232
CrossRef
Google scholar
|
[55] |
Scupham, A.J., Presley, L.L., Wei, B., Bent, E., Griffith, N., McPherson, M., Zhu, F., Oluwadara, O., Rao, N., Braun, J., Borneman, J., 2006. Abundant and diverse fungal microbiota in the murine intestine. Applied and Environmental Microbiology 72, 793–801
CrossRef
Pubmed
Google scholar
|
[56] |
Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., Ideker, T., 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research 13, 2498–2504
CrossRef
Pubmed
Google scholar
|
[57] |
Sharma, G., Pandey, R.R., Singh, M.S., 2011. Microfungi associated with surface soil and decaying leaf litter of Quercus serrata in a subtropical natural oak forest and managed plantation in Northeastern India. African Journal of Microbiological Research 5, 777–787
CrossRef
Google scholar
|
[58] |
Shen, C.C., Ge, Y., Yang, T., Chu, H.Y., 2017. Verrucomicrobial elevational distribution was strongly influenced by soil pH and carbon/nitrogen ratio. Journal of Soils and Sediments 17, 2449–2456
CrossRef
Google scholar
|
[59] |
Stursova, M., Baldrian, P., 2011. Effects of soil properties and management on the activity of soil organic matter transforming enzymes and the quantification of soil-bound and free activity. Plant and Soil 338, 99–110
CrossRef
Google scholar
|
[60] |
Tedersoo, L., Bahram, M., Cajthaml, T., Põlme, S., Hiiesalu, I., Anslan, S., Harend, H., Buegger, F., Pritsch, K., Koricheva, J., Abarenkov, K., 2016. Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME Journal 10, 346–362
CrossRef
Pubmed
Google scholar
|
[61] |
Urbanova, M., Snajdr, J., Baldrian, P., 2015. Composition of fungal and bacterial communities in forest litter and soil is largely determined by dominant trees. Soil Biology & Biochemistry 84, 53–64
CrossRef
Google scholar
|
[62] |
van der Heijen, M.G.A., 2008. The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems (vol 11, pg 296, 2008). Ecology Letters 11, 651–651.
|
[63] |
Voříšková, J., Brabcová, V., Cajthaml, T., Baldrian, P., 2014. Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytologist 201, 269–278
CrossRef
Pubmed
Google scholar
|
[64] |
Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R., 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 5261–5267
CrossRef
Pubmed
Google scholar
|
[65] |
Yan, J.Z., Zhang, Y.L., Bai, W.Q., Liu, Y.H., Bao, W.K., Liu, L.S., Zheng, D., 2005. Land cover changes based on plant successions: Deforestation, rehabilitation and degeneration of forest in the upper Dadu River watershed. Science in China. Series D, Earth Sciences 48, 2214–2230
CrossRef
Google scholar
|
[66] |
Yang, G.L., Hou, S.G., Le Baoge, R., Li, Z.G., Xu, H., Liu, Y.P., Du, W.T., Liu, Y.Q., 2016. Differences in bacterial diversity and communities between glacial snow and glacial soil on the Chongce Ice Cap, West Kunlun Mountains. Scientific Reports 6, 36548
CrossRef
Pubmed
Google scholar
|
[67] |
Yao, F., Yang, S., Wang, Z., Wang, X., Ye, J., Wang, X., DeBruyn, J.M., Feng, X., Jiang, Y., Li, H., 2017. Microbial Taxa distribution is associated with ecological trophic cascades along an elevation gradient. Frontiers in Microbiology 8, 2071
CrossRef
Pubmed
Google scholar
|
[68] |
Yue, Y.J., Yu, X.X., Li, G.T., Fan, D.X., Ye, J.D., 2009. Spatial structure of Quercus mongolica forest in Beijing Songshan Mountain Nature Reserve. Ying Yong Sheng Tai Xue Bao 20, 1811–1816.
Pubmed
|
[69] |
Zhang, K., Yu, Z., Li, X., Zhou, W., Zhang, D., 2007. Land use change and land degradation in China from 1991 to 2001. Land Degradation & Development 18, 209–219
CrossRef
Google scholar
|
[70] |
Zhang, Y., Guo, L.D., Liu, R.J., 2004. Survey of arbuscular mycorrhizal fungi in deforested and natural forest land in the subtropical region of Dujiangyan, southwest China. Plant and Soil 261, 257–263
CrossRef
Google scholar
|
[71] |
Zhang, Y., Liu, X., Cong, J., Lu, H., Sheng, Y., Wang, X., Li, D., Liu, X., Yin, H., Zhou, J., Deng, Y., 2017. The microbially mediated soil organic carbon loss under degenerative succession in an alpine meadow. Molecular Ecology 26, 3676–3686
CrossRef
Pubmed
Google scholar
|
[72] |
Zhao, M., Xue, K., Wang, F., Liu, S., Bai, S., Sun, B., Zhou, J., Yang, Y., 2014. Microbial mediation of biogeochemical cycles revealed by simulation of global changes with soil transplant and cropping. ISME Journal 8, 2045–2055
CrossRef
Pubmed
Google scholar
|
[73] |
Zhou, J., Deng, Y., Shen, L., Wen, C., Yan, Q., Ning, D., Qin, Y., Xue, K., Wu, L., He, Z., Voordeckers, J.W., Nostrand, J.D., Buzzard, V., Michaletz, S.T., Enquist, B.J., Weiser, M.D., Kaspari, M., Waide, R., Yang, Y., Brown, J.H., 2016. Temperature mediates continental-scale diversity of microbes in forest soils. Nature Communications 7, 12083
CrossRef
Pubmed
Google scholar
|
[74] |
Zhou, J., Deng, Y., Shen, L., Wen, C., Yan, Q., Ning, D., Qin, Y., Xue, K., Wu, L., He, Z., Voordeckers, J.W., Van Nostrand, J.D., Buzzard, V., Michaletz, S.T., Enquist, B.J., Weiser, M.D., Kaspari, M., Waide, R., Yang, Y., Brown, J.H., 2017. Correspondence: Reply to ‘Analytical flaws in a continental-scale forest soil microbial diversity study’. Nature Communications 8, 15583
CrossRef
Pubmed
Google scholar
|
/
〈 | 〉 |