Microbial community variation in rhizosphere and non-rhizosphere soils of Castanopsis hystrix plantations across stand ages

Abstract

Soil microbial communities play a crucial role in forest ecological processes, but the differences between rhizosphere and non-rhizosphere soils, as well as their variations with stand ages remain unclear. We collected rhizosphere and non-rhizosphere soils in Castanopsis hystrix plantations at ages (6, 10, 15, 25, 30 and 34 years) in the southern subtropics and analyzed soil microbial communities using the phospholipid fatty acid (PLFA) method. There were significant differences in microbial communities between the two. Rhizosphere soils had higher total PLFAs and fungal to bacterial (F:B) ratios, and lower arbuscular mycorrhizal fungi to ectomycorrhizal fungi (AMF:EMF) ratios in the 34-year-old stand but microbial communities in non-rhizosphere soils showed no changes with stand age. Rhizosphere soils had higher total PLFAs and F:B ratios but lower AMF:EMF ratios. Further analysis revealed a strong correlation between fine root nutrients and rhizosphere soil PLFAs, indicating a closer interaction between root exudates and microbial communities. In contrast, non-rhizosphere soil PLFAs appeared to be more influenced by soil nitrogen availability. Overall, soil microbial communities exhibited significant differences between rhizosphere and non-rhizosphere soils over various stand ages. A strong correlation was observed between rhizosphere soil PLFAs and fine root nutrients, which may improve our understanding of forest management strategies.

Keywords

Total PLFAs / Soil microbial communities / Plant nutrients / Rhizosphere soil

References

[1] AiC, LiangGQ, SunJW, WangXB, ZhouW. Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil. Geoderma, 2012, 173: 330-338

[2] AvisTJ, GravelV, AntounH, TweddellRJ. Multifaceted beneficial effects of rhizosphere microorganisms on plant health and productivity. Soil Biol Biochem, 2008, 40(7): 1733-1740

[3] BergB. Litter decomposition and organic matter turnover in northern forest soils. For Ecol Manag, 2000, 133(1–2): 13-22

[4] BiBY, WangY, WangK, ZhangH, FeiHY, PanRP, HanFP. Changes in microbial metabolic C- and N- limitations in the rhizosphere and bulk soils along afforestation chronosequence in desertified ecosystems. J Environ Manag, 2022, 303, ArticleID: 114215

[5] BossioDA, ScowKM, GunapalaN, GrahamKJ. Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol, 1998, 36(1): 1-12

[6] BrantJB, MyroldDD, SulzmanEW. Root controls on soil microbial community structure in forest soils. Oecologia, 2006, 148(4): 650-659

[7] CamenzindT, HättenschwilerS, TresederKK, LehmannA, RilligMC. Nutrient limitation of soil microbial processes in tropical forests. Ecol Monogr, 2018, 88(1): 4-21

[8] CamenzindT, Mason-JonesK, MansourI, MatthiasCR, JohannesL. Formation of necromass-derived soil organic carbon determined by microbial death pathways. Nat Geosci, 2023, 16: 115-122

[9] ChaparroJM, SheflinAM, ManterDK, VivancoJM. Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils, 2012, 48(5): 489-499

[10] ChenYQ, ZhangYJ, CaoJB, FuSL, HuSJ, WuJP, ZhaoJ, LiuZF. Stand age and species traits alter the effects of understory removal on litter decomposition and nutrient dynamics in subtropical Eucalyptus plantations. Glob Ecol Conserv, 2019, 20, ArticleID: e00693

[11] CuiYX, BingHJ, FangLC, WuYH, YuJL, ShenGT, JiangM, WangX, ZhangXC. Diversity patterns of the rhizosphere and bulk soil microbial communities along an altitudinal gradient in an alpine ecosystem of the eastern Tibetan Plateau. Geoderma, 2019, 338: 118-127

[12] DangP, YuX, LeH, LiuJL, ShenZ, ZhaoZ. Effects of stand age and soil properties on soil bacterial and fungal community composition in Chinese pine plantations on the Loess Plateau. PLoS one, 2017, 12(10) e0186501

[13] FrostegårdA, BååthE. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils, 1996, 22 1): 59-65

[14] FrostegårdÅ, TunlidA, BååthE. Use and misuse of PLFA measurements in soils. Soil Biol Biochem, 2011, 43(8): 1621-1625

[15] GarciaC, RoldanA, HernandezT. Ability of different plant species to promote microbiological processes in semiarid soil. Geoderma, 2005, 124(1–2): 193-202

[16] GeXG, WangCG, WangLL, ZhouBZ, CaoYH, XiaoWF, LiMH. Drought changes litter quantity and quality, and soil microbial activities to affect soil nutrients in moso bamboo forest. Sci Total Environ, 2022, 838(Pt 3) 156351

[17] Gómez-BrandónM, HerbónC, ProbstM, FornasierF, BarralMT, ParadeloR. Influence of land use on the microbiological properties of urban soils. Appl Soil Ecol, 2022, 175, ArticleID: 104452

[18] GuiH, HydeK, XuJC, MortimerP. Arbuscular mycorrhiza enhance the rate of litter decomposition while inhibiting soil microbial community development. Sci Rep, 2017, 7: 42184

[19] GuillaumeT, DamrisM, KuzyakovY. Losses of soil carbon by converting tropical forest to plantations: erosion and decomposition estimated by δ(13) C. Glob Chang Biol, 2015, 21 9): 3548-3560

[20] HeLM, ChenJM, PanYD, BirdseyR, KattgeJ. Relationships between net primary productivity and forest stand age in U.S. forests. Glob Biogeochem Cycles, 2012, 26(3): GB3009

[21] JiaGM, ZhangBL, NiuJT, WangLM, ChenFQ. Soil labile organic carbon fractions in rhizosphere soil in Citrus plantations in the three gorges reservoir area. Agrofor Syst, 2015, 89(6): 1097-1105

[22] KroppenstedtRM Fatty acid and menaquinon analysis of actinomycetes and related organisms, 1985 London Academic Press

[23] LangeM, EisenhauerN, SierraCA, BesslerH, EngelsC, GriffithsRI, Mellado-VázquezPG, MalikAA, RoyJ, ScheuS, SteinbeissS, ThomsonBC, TrumboreSE, GleixnerG. Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun, 2015, 6: 6707

[24] LauberCL, StricklandMS, BradfordMA, FiererN. The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem, 2008, 40(9): 2407-2415

[25] LiYB, BezemerTM, YangJJ, LüXT, LiXY, LiangWJ, HanXG, LiQ. Changes in litter quality induced by N deposition alter soil microbial communities. Soil Biol Biochem, 2019, 130: 33-42

[26] LiN, YangYM, XuF, ChenXY, WeiRY, LiZY, PanW, ZhangWH. Genetic diversity and population structure analysis of Castanopsis hystrix and construction of a core collection using phenotypic traits and molecular markers. Genes, 2022, 13(12): 2383

[27] LiJJ, HuangYM, ChenLH, GaoS, ZhangJ, ZhangDJ. Understory plant diversity and phenolic allelochemicals across a range of Eucalyptus grandis plantation ages. J for Res, 2023, 34(5): 1577-1590

[28] LiX, AguilaLCR, LuoJC, LiuY, WuT, LieZY, LiuXJ, ChengY, JiangF, LiuJX. Carbon storage capacity of Castanopsis hystrix plantations at different stand-ages in South China. Sci Total Environ, 2023, 894, 164974

[29] LiX, LiuY, WuGP, LieZY, ShengH, AguilaLCR, KhanMS, LiuXJ, ZhouS, WuT, XuWF, LiuJX. Mixed plantations do not necessarily provide higher ecosystem multifunctionality than monoculture plantations. Sci Total Environ, 2024, 914, 170156

[30] LiX, WuT, WuGP, AguilaLCR, LiuXJ, LiuY, ChengY, JiangF, LieZY, LiuJX. Increasing stand age increases N deficiency but alleviates relative P limitations in Castanopsis hystrix plantations in Southern China. Land Degrad Dev, 2024, 35(6): 2173-2183

[31] LiangC, SchimelJP, JastrowJD. The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol, 2017, 2: 17105

[32] LiuXB, BurslemDFRP, TaylorJD, TaylorAFS, KhooE, Majalap-LeeN, HelgasonT, JohnsonD. Partitioning of soil phosphorus among arbuscular and ectomycorrhizal trees in tropical and subtropical forests. Ecol Lett, 2018, 21(5): 713-723

[33] LiuXJ, LieZY, ReichPB, ZhouGY, YanJH, HuangWJ, WangYP, PeñuelasJ, TissueDT, ZhaoMD, WuT, WuDH, XuWF, LiYL, TangXL, ZhouS, MengZ, LiuSZ, ChuGW, ZhangDQ, ZhangQM, HeXH, LiuJX. Long-term warming increased carbon sequestration capacity in a humid subtropical forest. Glob Chang Biol, 2024, 30(1) ArticleID: e17072

[34] MeenaM, YadavG, SonigraP, NagdaA, MehtaT, SwapnilP, HarishMA, KumarS. Multifarious responses of forest soil microbial community toward climate change. Microb Ecol, 2023, 86 1): 49-74

[35] MuruganR, BeggiF, KumarS. Belowground carbon allocation by trees, understory vegetation and soil type alter microbial community composition and nutrient cycling in tropical Eucalyptus plantations. Soil Biol Biochem, 2014, 76: 257-267

[36] NayloA, AlmeidaPSI, BenidireL, KhalilEH, CastroPM, OuvrardS, SchwartzC, BoularbahA. Trace and major element contents, microbial communities, and enzymatic activities of urban soils of Marrakech city along an anthropization gradient. J Soil Sediment, 2019, 19: 2153-2165

[37] NiYY, YangT, MaYY, ZhangKP, SoltisPS, SoltisDE, GilbertJA, ZhaoYP, FuCX, ChuHY. Soil pH determines bacterial distribution and assembly processes in natural mountain forests of Eastern China. Glob Ecol Biogeogr, 2021, 30(11): 2164-2177

[38] RenCJ, ZhouZH, GuoYX, YangGH, ZhaoFZ, WeiGH, HanXH, FengL, FengYZ, RenGX. Contrasting patterns of microbial community and enzyme activity between rhizosphere and bulk soil along an elevation gradient. CATENA, 2021, 196, ArticleID: 104921

[39] SaleemM, LawAD, SahibMR, PervaizZH, ZhangQM. Impact of root system architecture on rhizosphere and root microbiome. Rhizosphere, 2018, 6: 47-51

[40] SandnesA, EldhusetTD, WollebækG. Organic acids in root exudates and soil solution of Norway spruce and silver birch. Soil Biol Biochem, 2005, 37(2): 259-269

[41] SchimelJP, SchaefferSM. Microbial control over carbon cycling in soil. Front Microbiol, 2012, 3: 348

[42] ShenLL, DengHY, ZhangGL, MaAQ, MoXY. Effect of climate change on the potentially suitable distribution pattern of Castanopsis hystrix miq. China Plants, 2023, 12(4): 717

[43] ShiXZ, WangJQ, Lucas-BorjaME, WangZY, LiX, HuangZQ. Microbial diversity regulates ecosystem multifunctionality during natural secondary succession. J Appl Ecol, 2021, 58(12): 2833-2842

[44] ShiXZ, EisenhauerN, PeñuelasJ, FuYR, WangJQ, ChenYX, LiuSG, HeLL, Lucas-BorjaME, WangLY, HuangZQ. Trophic interactions in soil micro-food webs drive ecosystem multifunctionality along tree species richness. Glob Change Biol, 2024, 30(3) ArticleID: e17234

[45] SinghJS, GuptaVK. Soil microbial biomass: a key soil driver in management of ecosystem functioning. Sci Total Environ, 2018, 634: 497-500

[46] SinsabaughRL, HillBH, FollstadSJJ. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature, 2009, 462 7274): 795-798

[47] de Souza JP, de Carvalho Gonçalves JF, Jaquetti RK, da Costa KCP, de Lima RMB, Fearnside PM, da Rocha Nina Junior A (2023) Silvicultural interventions and agroforestry systems increase the economic and ecological value of Bertholletia excelsa plantations in the Amazon. Agrofor Syst 97(2): 197–207. https://doi.org/10.1007/s10457-022-00798-9

[48] SunD, ZhangWX, LinYB, LiuZF, ShenWJ, ZhouLX, RaoXQ, LiuSP, CaiX, HeD, FuSL. Soil erosion and water retention varies with plantation type and age. For Ecol Manag, 2018, 422: 1-10

[49] TianP, RazaviBS, ZhangXC, WangQK, BlagodatskayaE. Microbial growth and enzyme kinetics in rhizosphere hotspots are modulated by soil organics and nutrient availability. Soil Biol Biochem, 2020, 141, ArticleID: 107662

[50] TrogischS, HeJS, HectorA, Scherer-LorenzenM. Impact of species diversity, stand age and environmental factors on leaf litter decomposition in subtropical forests in China. Plant Soil, 2016, 400(1): 337-350

[51] TurnerJ, LambertMJ. Nutrient cycling in age sequences of two Eucalyptus plantation species. For Ecol Manag, 2008, 255(5–6): 1701-1712

[52] WangZT, LiT, WenXX, LiuY, HanJ, LiaoYC, DeBruynJM. Fungal communities in rhizosphere soil under conservation tillage shift in response to plant growth. Front Microbiol, 2017, 8: 1301

[53] WangDY, FeliceML, ScowKM. Impacts and interactions of biochar and biosolids on agricultural soil microbial communities during dry and wet-dry cycles. Appl Soil Ecol, 2020, 152, ArticleID: 103570

[54] WangY, LiuXS, ChenFF, HuangRL, DengXJ, JiangY. Seasonal dynamics of soil microbial biomass C and N of Keteleeria fortunei var. cyclolepis forests with different ages. J For Res, 2020, 31(6): 2377-2384

[55] WangJ, LiaoLR, YeZC, LiuHF, ZhangC, ZhangL, LiuGB, WangGL. Different bacterial co-occurrence patterns and community assembly between rhizosphere and bulk soils under N addition in the plant–soil system. Plant Soil, 2022, 471(1): 697-713

[56] WangY, DongLG, ZhangM, CuiYX, BaiXX, SongB, ZhangJW, YuX. Dynamic microbial community composition, co-occurrence pattern and assembly in rhizosphere and bulk soils along a coniferous plantation chronosequence. Catena, 2023, 223, ArticleID: 106914

[57] WenL, LeiPF, XiangWH, YanWD, LiuSG. Soil microbial biomass carbon and nitrogen in pure and mixed stands of Pinus massoniana and Cinnamomum camphora differing in stand age. For Ecol Manag, 2014, 328: 150-158

[58] WenZH, WhitePJ, ShenJB, LambersH. Linking root exudation to belowground economic traits for resource acquisition. New Phytol, 2022, 233(4): 1620-1635

[59] WuGP, SuYG, WangJJ, LinSN, HuangZY, HuangG. Elevational patterns of microbial carbon use efficiency in a subtropical mountain forest. Biol Fertil Soils, 2024, 60(1): 5-15

[60] XiaoYS, PengFT, DangZQ, JiangXM, ZhangJH, ZhangYF, ShuHR. Influence of rhizosphere ventilation on soil nutrient status, root architecture and the growth of young peach trees. Soil Sci Plant Nutr, 2015, 61(5): 775-787

[61] XuJ, LiuB, QuZL, MaY, SunH. Age and species of Eucalyptus plantations affect soil microbial biomass and enzymatic activities. Microorganisms, 2020, 8(6): 811

[62] YesilonisI, SzlaveczK, PouyatR, WhighamD, XiaL. Historical land use and stand age effects on forest soil properties in the Mid-Atlantic US. For Ecol Manag, 2016, 370: 83-92

[63] YouYM, HuangXM, ZhuHG, LiuSR, LiangHW, WenYG, WangH, CaiDX, YeD. Positive interactions between Pinus massoniana and Castanopsis hystrix species in the uneven-aged mixed plantations can produce more ecosystem carbon in subtropical China. For Ecol Manag, 2018, 410: 193-200

[64] ZarafsharM, BazotS, MatinizadehM, BordbarSK, RoustaMJ, KoochY, EnayatiK, AbbasiA, NegahdarsaberM. Do tree plantations or cultivated fields have the same ability to maintain soil quality as natural forests?. Appl Soil Ecol, 2020, 151, ArticleID: 103536

[65] ZhangN, NunanN, HirschPR, SunB, ZhouJZ, LiangYT. Theory of microbial coexistence in promoting soil–plant ecosystem health. Biol Fertil Soils, 2021, 57(7): 897-911

[66] ZhangXX, WangLJ, ZhouWX, HuW, HuJW, HuM. Changes in litter traits induced by vegetation restoration accelerate litter decomposition in Robinia pseudoacacia plantations. Land Degrad Dev, 2022, 33(1): 179-192

[67] ZhaoML, ZhaoJ, YuanJ, HaleL, WenT, HuangQW, VivancoJM, ZhouJZ, KowalchukGA, ShenQR. Root exudates drive soil-microbe-nutrient feedbacks in response to plant growth. Plant Cell Environ, 2021, 44(2): 613-628

[68] ZhouSYD, LieZY, LiuXJ, ZhuYG, PeñuelasJ, NeilsonR, SuXX, LiuZF, ChuGW, MengZ, YanJH, LiuJX. Distinct patterns of soil bacterial and fungal community assemblages in subtropical forest ecosystems under warming. Glob Chang Biol, 2023, 29(6): 1501-1513

RIGHTS & PERMISSIONS

Northeast Forestry University