Abstract
Aims
The positive soil biodiversity and multifunctionality relationship has been widely recognized, however in agricultural ecosystems, this relationship is context dependent and could be altered by land use intensity (LUI). Understanding how LUI affects soil microbial community and multifunctionality (SMF) is instructive for optimizing external inputs and managements.
Methods
We sampled soils from three cropping systems (cotton, wheat-maize and vegetable) with different LUI, sequenced both bacterial and fungal communities, and quantified the multifunctionality by averaging carbon, nitrogen and phosphorus cycling functions. The relationship between soil microbial diversity and SMF was further explored.
Results
The results showed that the positive effects of soil microbial diversity on SMF was significantly affected by LUI. In general, LUI decreased SMF and both bacterial and fungal diversity. Cotton and wheat-maize rotation systems with relatively lower LUI showed higher microbial diversity and SMF compared with the vegetable system, which had the highest LUI and the lowest SMF. Moreover, bacterial but not fungal diversity drove this positive relationship between microbial diversity and SMF in both cotton and wheat-maize systems but not in the vegetable system, indicating a larger bacterial effect in lower LUI system. Random forest and structural equation modeling further confirmed bacterial diversity and composition contributed to SMF mainly via promoting carbon and phosphorus cycling.
Conclusions
Our findings highlight the importance of LUI in influencing the relationships of biodiversity-SMF and further demonstrate that soil microbial diversity conservation with less anthropogenic disturbances is important for supporting soil functioning in agroecosystems.
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Abbreviations
- SMF:
-
Soil multifunctionality
- LUI:
-
Land use intensity
- C:
-
Carbon
- N:
-
Nitrogen
- P:
-
Phosphorus
- ANOVA:
-
Analysis of variance
- PERMANOVA:
-
Permutational multivariate ANOVA
- PCoA:
-
Principal co-ordinates analysis
- ASVs:
-
Amplicon Sequence Variants
References
Abramovitch RB, Martin GB (2004) Strategies used by bacterial pathogens to suppress plant defenses. Curr Opin Plant Biol 7:356–364. https://doi.org/10.1016/j.pbi.2004.05.002
Allison SD, Martiny JB (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci 105:11512–11519. https://doi.org/10.1073/pnas.0801925105
Babin D, Deubel A, Jacquiod S et al (2019) Impact of long-term agricultural management practices on soil prokaryotic communities. Soil Biol Biochem 129:17–28. https://doi.org/10.1016/j.soilbio.2018.11.002
Bai Z, Caspari T, Gonzalez MR et al (2018) Effects of agricultural management practices on soil quality: a review of long-term experiments for Europe and China. Agric Ecosyst Environ 265:1–7. https://doi.org/10.1016/j.agee.2018.05.028
Bender SF, Wagg C, van der Heijden MGA (2016) An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol Evol 31:440–452. https://doi.org/10.1016/j.tree.2016.02.016
Bi QF, Li KJ, Zheng BX et al (2020) Partial replacement of inorganic phosphorus (P) by organic manure reshapes phosphate mobilizing bacterial community and promotes P bioavailability in a paddy soil. Sci Total Environ 134977. https://doi.org/10.1016/j.scitotenv.2019.134977
Bonanomi G, De Filippis F, Cesarano G et al (2016) Organic farming induces changes in soil microbiota that affect agro-ecosystem functions. Soil Biol Biochem 103:327–336. https://doi.org/10.1016/j.soilbio.2016.09.005
Byrnes JE, Gamfeldt L, Isbell F et al (2014) Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions. Methods Ecol Evol 5:111–124. https://doi.org/10.1111/2041-210X.12143
Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583
Chen X, Jiang N, Condron LM et al (2019) Soil alkaline phosphatase activity and bacterial phoD gene abundance and diversity under long-term nitrogen and manure inputs. Geoderma 349:36–44. https://doi.org/10.1016/j.geoderma.2019.04.039
Chen H, Dai Z, Veach AM et al (2020a) Global meta-analyses show that conservation tillage practices promote soil fungal and bacterial biomass. Agric Ecosyst Environ 293:106841. https://doi.org/10.1016/j.agee.2020.106841
Chen Q, Ding J, Zhu D et al (2020b) Rare microbial taxa as the major drivers of ecosystem multifunctionality in long-term fertilized soils. Soil Biol Biochem 141:107686. https://doi.org/10.1016/j.soilbio.2019.107686
Chen L, He Z, Zhao W et al (2020c) Soil structure and nutrient supply drive changes in soil microbial communities during conversion of virgin desert soil to irrigated cropland. Eur J Soil Sci 71:768–781. https://doi.org/10.1111/ejss.12901
Chen H, Yin C, Fan X et al (2021) Effect of P availability on straw-induced priming effect was mainly regulated by fungi in croplands. Appl Microbiol Biotechnol 105:9403–9418. https://doi.org/10.1007/s00253-021-11691-3
D’Acunto L, Andrade JF, Poggio SL et al (2018) Diversifying crop rotation increased metabolic soil diversity and activity of the microbial community. Agric Ecosyst Environ 257:159–164. https://doi.org/10.1016/j.agee.2018.02.011
Dai Z, Liu G, Chen H et al (2020) Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems. ISME J 14:757–770
Dalrymple D (1971) Survey of multiple cropping in less developed nations. Econ. Res. Serv. U.S. Department of Agriculture, Washington, D.C., pp 3–120
Delgado-Baquerizo M, Maestre FT, Reich PB et al (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541. https://doi.org/10.1038/ncomms10541
Delgado-Baquerizo M, Trivedi P, Trivedi C et al (2017) Microbial richness and composition independently drive soil multifunctionality. Funct Ecol 31:2330–2343. https://doi.org/10.1111/1365-2435.12924
Dighton J (2007) 16 nutrient cycling by saprotrophic fungi in terrestrial habitats. Environ Microb Relat 4:287
Dumbrell AJ, Nelson M, Helgason T et al (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Edwards CA (1987) The concept of integrated systems in lower input/sustainable agriculture. Am J Altern Agric 2(4):148–152
Eisenhauer N, Klier M, Partsch S et al (2009) No interactive effects of pesticides and plant diversity on soil microbial biomass and respiration. Appl Soil Ecol 42:31–36. https://doi.org/10.1016/j.apsoil.2009.01.005
Gao J, Feng J, Zhang X et al (2016) Drying-rewetting cycles alter carbon and nitrogen mineralization in litter-amended alpine wetland soil. Catena 145:285–290
Han S, Tan S, Chen W et al (2022a) Bacterial rather than fungal diversity and community assembly drive soil multifunctionality in a subtropical forest ecosystem. Environ Microbiol Rep 14:85–95
Han L, Xu M, Kong X et al (2022b) Deciphering the diversity, composition, function, and network complexity of the soil microbial community after repeated exposure to a fungicide boscalid. Environ Pollut 312:120060
Herzog F, Steiner B, Bailey D et al (2006) Assessing the intensity of temperate European agriculture at the landscape scale. Eur J Agron 24:165–181. https://doi.org/10.1016/j.eja.2005.07.006
Huang B, Yan D, Ouyang C et al (2020) Chloropicrin fumigation alters the soil phosphorus and the composition of the encoding alkaline phosphatase PhoD gene microbial community. Sci Total Environ 711:135080. https://doi.org/10.1016/j.scitotenv.2019.135080
Jacobsen CS, Hjelmsø MH (2014) Agricultural soils, pesticides and microbial diversity. Curr Opin Biotechnol 27:15–20. https://doi.org/10.1016/j.copbio.2013.09.003
Jangid K, Williams MA, Franzluebbers AJ et al (2008) Relative impacts of land-use, management intensity and fertilization upon soil microbial community structure in agricultural systems. Soil Biol Biochem 40:2843–2853. https://doi.org/10.1016/j.soilbio.2008.07.030
Jansson JK, Hofmockel KS (2020) Soil microbiomes and climate change. Nat Rev Microbiol 18(1):35–46. https://doi.org/10.1038/s41579-019-0265-7
Jing X, Sanders NJ, Shi Y et al (2015) The links between ecosystem multifunctionality and above-and belowground biodiversity are mediated by climate. Nat Commun 6:8159. https://doi.org/10.1038/ncomms9159
Koutika LS, Epron D, Bouillet J et al (2014) Changes in N and C concentrations, soil acidity and P availability in tropical mixed acacia and eucalypt plantations on a nutrient-poor sandy soil. Plant Soil 379:205–216. https://doi.org/10.1007/s11104-014-2047-3
Kuypers MM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263–276. https://doi.org/10.1038/nrmicro.2018.9
Li J, Delgado-Baquerizo M, Wang J et al (2019a) Fungal richness contributes to multifunctionality in boreal forest soil. Soil Biol Biochem 136:107526. https://doi.org/10.1016/j.soilbio.2019.107526
Li X, He H, Zhang X et al (2019b) Distinct responses of soil fungal and bacterial nitrate immobilization to land conversion from forest to agriculture. Soil Biol Biochem 134:81–89. https://doi.org/10.1016/j.soilbio.2019.03.023
Li Y, Ge Y, Wang J et al (2021a) Functional redundancy and specific taxa modulate the contribution of prokaryotic diversity and composition to multifunctionality. Mol Biol 30:2915–2930. https://doi.org/10.1111/mec.15935
Li M, Guo J, Ren T et al (2021b) Crop rotation history constrains soil biodiversity and multifunctionality relationships. Agric Ecosyst Environ 319:107550. https://doi.org/10.1016/j.agee.2021.107550
Li K, Zhang H, Li X et al (2021c) Field management practices drive ecosystem multifunctionality in a smallholder-dominated agricultural system. Agric Ecosyst Environ 313:107389
Lian T, Yu Z, Liu J et al (2018) Rhizobacterial community structure in response to nitrogen addition varied between two Mollisols differing in soil organic carbon. Sci Rep 8:1–8. https://doi.org/10.1038/s41598-018-30769-z
Liu J, Yu Z, Yao Q et al (2017) Distinct soil bacterial communities in response to the cropping system in a Mollisol of Northeast China. Appl Soil Ecol 119:407–416. https://doi.org/10.1016/j.apsoil.2017.07.013
Liu J, Ma Q, Hui X et al (2020) Long-term high-P fertilizer input decreased the total bacterial diversity but not phoD-harboring bacteria in wheat rhizosphere soil with available-P deficiency. Soil Biol Biochem 149:107918
Locey K J, Lennon J T (2016) Reply to Willis: Powerful predictions of biodiversity from ecological models and scaling laws. Proc Natl Acad Sci 113: E5097–E5097
Luo G, Rensing C, Chen H et al (2018) Deciphering the associations between soil microbial diversity and ecosystem multifunctionality driven by long-term fertilization management. Funct Ecol 32:1103–1116
Maestre FT, Castillo-Monroy AP, Bowker MA et al (2012) Species richness effects on ecosystem multifunctionality depend on evenness, composition and spatial pattern. J Ecol 100:317–330. https://doi.org/10.1111/j.1365-2745.2011.01918.x
Magoˇc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963
Maier S, Kratz AM, Weber J et al (2022) Water-driven microbial nitrogen transformations in biological soil crusts causing atmospheric nitrous acid and nitric oxide emissions. ISME J 16:1012–1024
Mangalassery S, Mooney SJ, Sparkes DL et al (2015) Impacts of zero tillage on soil enzyme activities, microbial characteristics and organic matter functional chemistry in temperate soils. Eur J Soil Biol 68:9–17. https://doi.org/10.1016/j.ejsobi.2015.03.001
Manning P, van der Plas F, Soliveres S et al (2018) Redefining ecosystem multifunctionality. Nat Ecol Evol 2:427–436. https://doi.org/10.1038/s41559-018-0660-x
Mori AS, Isbell F, Fujii S et al (2016) Low multifunctional redundancy of soil fungal diversity at multiple scales. Ecol Lett 19:249–259. https://doi.org/10.1111/ele.12560
National Bureau of Statistics of China (2015) Handan statistical yearbook. China Statistics Press, Beijing
Pasari JR, Levi T, Zavaleta ES et al (2013) Several scales of biodiversity affect ecosystem multifunctionality. Proc Natl Acad Sci 110:10219–10222. https://doi.org/10.1073/pnas.1314558110
Rodríguez A, Duran J, Rey A et al (2019) Interactive effects of forest die-off and drying-rewetting cycles on C and N mineralization. Geoderma 333:81–89. https://doi.org/10.1016/j.geoderma.2018.07.003
Smithee S, Tracy S, Drescher KM et al (2014) A novel, broadly applicable approach to isolation of fungi in diverse growth media. J Microbiol Methods 105:155–161. https://doi.org/10.1016/j.mimet.2014.07.023
Sofo A, Zanella A, Ponge JF (2022) Soil quality and fertility in sustainable agriculture, with a contribution to the biological classification of agricultural soils. Soil Use Manag 38:1085–1112. https://doi.org/10.1111/sum.12702
Sorokin DY, Lücker S, Vejmelkova D et al (2012) Nitrification expanded: discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi. ISME J 6:2245–2256. https://doi.org/10.1038/ismej.2012.70
Strickland MS, Osburn E, Lauber C et al (2009) Litter quality is in the eye of the beholder: initial decomposition rates as a function of inoculum characteristics. Funct Ecol 23:627–636. https://doi.org/10.1111/j.1365-2435.2008.01515.x
Sun S, Li S, Avera BN et al (2017) Soil bacterial and fungal communities show distinct recovery patterns during forest ecosystem restoration. Appl Environ Microbiol 83:e00966–e00917. https://doi.org/10.1128/AEM.00966-17
Tan H, Barret M, Mooij MJ et al (2013) Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol Fertil Soils 49:661–672. https://doi.org/10.1007/s00374-012-0755-5
Wei X, Wu S, Nie X et al (2009) The effects of residual tetracycline on soil enzymatic activities and plant growth. J Environ Sci Heal B 44:461–471. https://doi.org/10.1080/03601230902935139
Wu X, Peng J, Liu P et al (2021) Metagenomic insights into nitrogen and phosphorus cycling at the soil aggregate scale driven by organic material amendments. Sci Total Environ 785:147329. https://doi.org/10.1016/j.scitotenv.2021.147329
Xie Y, Wang F, Wang K et al (2020) Responses of bacterial phoD gene abundance and diversity to crop rotation and feedbacks to phosphorus uptake in wheat. Appl Soil Ecol 154:103604
Zhang Q, Shamsi IH, Xu D et al (2012) Chemical fertilizer and organic manure inputs in soil exhibit a vice versa pattern of microbial community structure. Appl Soil Ecol 57:1–8. https://doi.org/10.1016/j.apsoil.2012.02.012
Zhang J, Li T, Jia J et al (2021a) Bacterial taxa and fungal diversity are the key factors determining soil multifunctionality in different cropping systems. Land Degrad Dev 32:5012–5022. https://doi.org/10.1002/ldr.4087
Zhang K, Maltais-Landry G, Liao H (2021b) How soil biota regulate C cycling and soil C pools in diversified crop rotations. Soil Biol Biochem 156:108219. https://doi.org/10.1016/j.soilbio.2021.108219
Acknowledgements
This study was supported by National Key R&D Program of China (2022YFD1901300); National Natural Science Foundation of China (No. 32201330); and China Scholarship Council (No.201913043). We acknowledge Prof. Rachel Creamer and Dr. Ron de Goede (Wageningen University & Research) for his insightful and constructive comments.
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JY Jia, JZ Zhang, GZ Wang and JL Zhang designed this study; JY Jia and JZ Zhang sampled soil from field, and JY Jia performed laboratory work; JY Jia, YZ Li, Mx Xie, GZ Wang and JL Zhang analyzed and interpreted the data; JY Jia, GZ Wang and JL Zhang wrote the manuscript.
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Jia, J., Zhang, J., Li, Y. et al. Land use intensity constrains the positive relationship between soil microbial diversity and multifunctionality. Plant Soil (2022). https://doi.org/10.1007/s11104-022-05853-z
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DOI: https://doi.org/10.1007/s11104-022-05853-z