Abstract
Purpose
Uncovering the diversity of abundant and rare bacterial subcommunities in different years of continuous monocropping are essential to predict microbial community changes and understand soil functions in the cut chrysanthemum cropping system.
Methods
The Illumina MiSeq high-throughput sequencing platform was employed to analyze the composition, structure, and diversity of rare and abundant bacterial subcommunities in three different continuous monocropping years of cut chrysanthemum, namely, 1 year (Y1), 6 years (Y6), and 12 years (Y12)
Results
The short- (Y6) and long-term (Y12) monocropping significantly enhanced the alpha diversity (e.g., Shannon index) of the abundant bacterial subcommunity (P < 0.05), but Y6 and Y12 treatments had a completely opposite impact on the rare bacterial subcommunity, with a remarkable decline in the Y12 and an increase in the Y6. Both Y6 and Y12 significantly reshaped the subcommunity structure of rare and abundant bacteria; Y12 significantly enriched the Acidobacteria in both rare and abundant taxa and decreased the abundant taxa Proteobacteria, while Y6 mainly increased the relative abundance of Gemmatimonadetes in the abundant phylum. The imbalance of soil nutrients including carbon, nitrogen, and phosphorus drove alterations of abundant and rare subcommunities.
Conclusion
The monocropping obstacle of cut chrysanthemum may be attributed to the decrease in the rare bacterial diversity.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Ainsworth TD, Krause L, Bridge T, Torda G, Raina JB, Zakrzewski M, Gates RD, Padilla-Gamino JL, Spalding HL, Smith C, Woolsey ES, Bourne DG, Bongaerts P, Leggat H-G, W, (2015) The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J 9:2261–2274. https://doi.org/10.1038/ismej.2015.39
Asaf S, Numan M, Khan AL, Al-Harrasi A (2020) Sphingomonas: from diversity and genomics to functional role in environmental remediation and plant growth. Crit Rev Biotechnol 40:138–152. https://doi.org/10.1080/07388551.2019.1709793
Bao SD (2000) Soil Agricultural Chemical Analysis, 3rd edn. Agriculture Press, Beijing (in Chinese)
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. P Natl Acad Sci USA 108:4516–4522. https://doi.org/10.1073/pnas.1000080107
Caron DA, Countway PD (2009) Hypotheses on the role of the protistan rare biosphere in a changing world. Aquat Microb Ecol 57:227–238. https://doi.org/10.3354/ame01352
Chen MN, Li X, Yang QL, Chi XY, Pan LJ, Chen N, Yang Z, Wang T, Wang MA, Yu SL (2014) Dynamic succession of soil bacterial community during continuous cropping of peanut (Arachis hypogaea L). PLoS One 9:e101355. https://doi.org/10.1371/journal.pone.0101355
Chen P, Wang YZ, Liu QZ, Zhang YT, Li XY, Li HQ, Li WH (2020a) Phase changes of continuous cropping obstacles in strawberry (Fragaria x ananassa Duch) production. Appl Soil Ecol 155:103626. https://doi.org/10.1016/j.apsoil.2020.103626
Chen QL, Ding J, Zhu D, Hu HW, Delgado-Baquerizo M, Ma YB, He JZ, Zhu YG (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
China Ministry of Agriculture (2016) Available online at: http://zdscxx.moa.gov. cn:8080/nyb/pc/search.jsp
Cookson WR, Abaye DA, Marschner P, Murphy DV, Stockdale EA, Goulding KW (2005) The contribution of soil organic matter fractions to carbon and nitrogen mineralization and microbial community size and structure. Soil Biol Biochem 37:1726–1737. https://doi.org/10.1016/j.soilbio.2005.02.007
Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, Berdugo M, Campbell CD, Singh BK (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541. https://doi.org/10.1038/ncomms10541
Egbe CC, Oyetibo GO, Ilori MO (2021) Ecological impact of organochlorine pesticides consortium on autochthonous microbial community in agricultural soil. Ecotox Environ Safe 207:111319. https://doi.org/10.1016/j.ecoenv.2020.111319
Eichorst SA, Trojan D, Roux S, Herbold C, Rattei T, Woebken D (2018) Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments. Environ Microbiol 20:1041–1063. https://doi.org/10.1111/1462-2920.14043
Epskamp S, Epskamp MS, MplusAutomation S (2019) Package ‘semPlot’. R Package Version 1.1.2. https://cran.r-project.org/package=semPlot.
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. https://doi.org/10.1890/05-1839
Fiorini A, Remelli S, Boselli R, Mantovi P, Ardenti F, Trevisan M, Menta C, Tabaglio V (2022) Driving crop yield, soil organic C pools, and soil biodiversity with selected winter cover crops under no-till. Soil till Res 217:105283. https://doi.org/10.1016/j.still.2021.105283
Franke-Whittle IH, Manici LM, Insam H, Stres B (2015) Rhizosphere bacteria and fungi associated with plant growth in soils of three replanted apple orchards. Plant Soil 395:317–333. https://doi.org/10.1007/s11104-015-2562-x
García-Delgado C, Barba-Vicente V, Marin-Benito JM, Igual JM, Sanchez-Martin MJ, Rodriguez-Cruz MS (2019) Influence of different agricultural management practices on soil microbial community over dissipation time of two herbicides. Sci Total Environ 646:1478–1488. https://doi.org/10.1016/j.scitotenv.2018.07.395
Hei JY, Wang S, He XH (2023) Effects of exogenous organic acids on the growth, edaphic factors, soil extracellular enzymes, and microbiomes predict continuous cropping obstacles of Panax notoginseng from the forest understorey. Plant Soil: 1–18. https://doi.org/10.1007/s11104 -023–06044–0.
Hunt HW, Wall DH (2002) Modelling the effects of loss of soil biodiversity on ecosystem function. Global Change Biol 8:33–50. https://doi.org/10.1046/j.1365-2486.2002.00425.x
Hutchins DA, Jansson JK, Remais JV, Rich VI, Singh BK, Trivedi P (2019) Climate change microbiology—problems and perspectives. Nat Rev Microbiol 17:391–396. https://doi.org/10.1038/s41579-019-0178-5
Jiao S, Lu YH (2020a) Abundant fungi adapt to broader environmental gradients than rare fungi in agricultural fields. Global Change Biol 26:4506–4520. https://doi.org/10.1111/gcb.15130
Jiao S, Lu YH (2020b) Soil pH and temperature regulate assembly processes of abundant and rare bacterial communities in agricultural ecosystems. Environ Microbiol 22:1052–1065. https://doi.org/10.1111/1462-2920.14815
Jiao S, Chen WM, Wei GH (2017) Biogeography and ecological diversity patterns of rare and abundant bacteria in oil-contaminated soils. Mol Ecol 26:5305–5317. https://doi.org/10.1111/mec.14218
Jiao S, Wang JM, Wei GH, Chen WM, Lu YH (2019) Dominant role of abundant rather than rare bacterial taxa in maintaining agro-soil microbiomes under environmental disturbances. Chemosphere 235:248–259. https://doi.org/10.1016/j.chemosphere.2019.06.174
Kolde R (2015) Pheatmap: pretty heatmaps. http://cran.r-project.org/web/packages/pheatmap/index.html
Kumawat KC, Singh I, Nagpal S, Sharma P, Gupta RK, Sirari A (2022) Co-inoculation of indigenous Pseudomonas oryzihabitans and Bradyrhizobium sp. modulates the growth, symbiotic efficacy, nutrient acquisition, and grain yield of soybean. Pedosphere 32:438–451. https://doi.org/10.1016/S1002-0160(21)60085-1
Li H, Wang J, Liu Q, Zhou Z, Chen F, Xiang D (2019) Effects of consecutive monoculture of sweet potato on soil bacterial community as determined by pyrosequencing. J Basic Microb 59:181–191. https://doi.org/10.1002/jobm.201800304
Li J, Cheng X, Chu G, Hu B, Tao R (2023) Continuous cropping of cut chrysanthemum reduces rhizospheric soil bacterial community diversity and co-occurrence network complexity. Appl Soil Ecol 185:104801. https://doi.org/10.1016/j.apsoil.2022.104801
Liang YT, Xiao X, Nuccio EE, Yuan MT, Zhang N, Xue K, Cohan FM, Zhou JZ, Sun B (2020) Differentiation strategies of soil rare and abundant microbial taxa in response to changing climatic regimes. Environ Microbiol 22:1327–1340. https://doi.org/10.1111/1462-2920.14945
Liu LM, Yang J, Yu Z, Wilkinson DM (2015) The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. ISME J 9:2068–2077. https://doi.org/10.1038/ismej.2015.29
Liu X, Wang YZ, Liu YH, Chen H, Hu YL (2020) Response of bacterial and fungal soil communities to Chinese fir (Cunninghamia lanceolate) long-term monoculture plantations. Front Microbiol 11:181. https://doi.org/10.3389/fmicb.2020.00181
Liu C, Xia R, Tang M, Chen X, Zhong B, Liu XY, Bian RJ, Yang L, Zheng JF, Cheng K, Zhang XH, Drosos M, Li LQ, Shan SD, Joseph S, Pan GX (2022a) Improved ginseng production under continuous cropping through soil health reinforcement and rhizosphere microbial manipulation with biochar: a field study of Panax ginseng from Northeast China. Hortic Res 9: uhac108. https://doi.org/10.1093/hr/uhac108.
Liu XP, Wang HT, Wu YJ, Bi QF, Ding K, Lin XY (2022b) Manure application effects on subsoils: Abundant taxa initiate the diversity reduction of rare bacteria and community functional alterations. Soil Biol Biochem 174:108816. https://doi.org/10.1016/j.soilbio.2022.108816
Luo JP, Liao GC, Banerjee S, Gu SH, Liang JB, Guo XY, Zhao HP, Liang YC, Li TQ (2023) Long-term organic fertilization promotes the resilience of soil multifunctionality driven by bacterial communities. Soil Biol Biochem 177:108922. https://doi.org/10.1016/j.soilbio.2022.108922
Lynch MDJ, Neufeld JD (2015) Ecology and exploration of the rare biosphere. Nat Rev Microbiol 13:217–229. https://doi.org/10.1038/nrmicro3400
Mo YY, Zhang WJ, Yang J, Lin YS, Yu Z, Lin SJ (2018) Biogeographic patterns of abundant and rare bacterioplankton in three subtropical bays resulting from selective and neutral processes. ISME J 12:2198–2210. https://doi.org/10.1038/s41396-018-0153-6
Obalum SE, Chibuike GU, Peth S, Ouyang Y (2017) Soil organic matter as sole indicator of soil degradation. Environ Monit Assess 189:1–19. https://doi.org/10.1007/s10661-017-5881-y
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R (2015) Vegan: community ecology package. R package version 22-1
Philippot L, Spor A, Henault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron PA (2013) Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7:1609–1619. https://doi.org/10.1038/ismej.2013.34
Postma A, Slabbert E, Postma F, Jacobs K (2016) Soil bacterial communities associated with natural and commercial Cyclopia spp. FEMS Microbiol Ecol 92: fiw016. https://doi.org/10.1093/femsec/fiw016.
Prommer J, Walker TWN, Wanek W, Braun J, Zezula D, Hu YT, Hofhansl F, Richter A (2020) Increased microbial growth, biomass, and turnover drive soil organic carbon accumulation at higher plant diversity. Global Change Biol 26:669–681. https://doi.org/10.1111/gcb.14777
Qin ZR, Zhao ZH, Xia LL, Wang SY, Yu GW, Miao AH (2022) Responses of abundant and rare prokaryotic taxa in a controlled organic contaminated site subjected to vertical pollution-induced disturbances. Sci Total Environ 853:158625. https://doi.org/10.1016/j.scitotenv.2022.158625
Santhanam R, Luu VT, Weinhold A, Goldberg J, Oh Y, Baldwin IT (2015) Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. P Natl Acad Sci USA 112:E5013–E5020. https://doi.org/10.1073/pnas.1505765112
Tan Y, Cui Y, Li H, Kuang A, Li X, Wei Y, Ji X (2017) Rhizospheric soil and root endogenous fungal diversity and composition in response to continuous Panax notoginseng cropping practices. Microbiol Res 194:10–19. https://doi.org/10.1016/j.micres.2016.09.009
Wan WJ, Gadd GM, Yang YY, Yuan WK, Gu JD, Ye LP, Liu WZ (2021) Environmental adaptation is stronger for abundant rather than rare microorganisms in wetland soils from the Qinghai-Tibet Plateau. Mol Ecol 30:2390–2403. https://doi.org/10.1111/mec.15882
Wang T, Yang KX, Ma QY, Jiang X, Zhou YQ, Kong DL, Wang ZY, Parales RE, Li L, Zhao X, Ruan ZY (2022) Rhizosphere microbial community diversity and function analysis of cut Chrysanthemum during continuous monocropping. Front Microbiol 13:801546. https://doi.org/10.3389/fmicb.2022.801546
Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Vaenables B (2013) gplots: Various R programming tools for plotting data. R package version 2.12.1. http://CRAN.Rproject.org/package=gplots.
Wu HM, Wu LK, Zhu Q, Wang JY, Qin XJ, Xu JH, Kong LF, Chen J, Lin S, Khan MU, Amjad H, Lin WX (2017) The role of organic acids on microbial deterioration in the Radix pseudostellariae rhizosphere under continuous monoculture regimes. Sci Rep 7:3497. https://doi.org/10.1038/s41598-017-03793-8
Xiong W, Zhao QY, Zhao J, Xun WB, Li R, Zhang RF, Wu HS, Shen QR (2015) Different continuous cropping spans significantly affect microbial community membership and structure in a vanilla-grown soil as revealed by deep pyrosequencing. Microb Ecol 70:209–218. https://doi.org/10.1007/s00248-014-0516-0
Xiong C, He JZ, Singh BK, Zhu YG, Wang JT, Li PP, Zhang QB, Han LL, Shen JP, Ge AH, Wu CF, Zhang LM (2021) Rare taxa maintain the stability of crop mycobiomes and ecosystem functions. Environ Microbiol 23:1907–1924. https://doi.org/10.1111/1462-2920.15262
Xue MD, Guo ZY, Gu XY, Gao HL, Weng SM, Zhou J, Gu DG, Lu HX, Zhou XQ (2020) Rare rather than abundant microbial communities drive the effects of long-term greenhouse cultivation on ecosystem functions in subtropical agricultural soils. Sci Total Environ 706:136004. https://doi.org/10.1016/j.scitotenv.2019.136004
Yilmaz B, Portugal S, Tran TM, Gozzelino R, Ramos S, Gomes J, Regalado A, Cowan PJ, d’Apice AJF, Chong AS, Doumbo OK, Traore B, Crompton PD, Silveira H, Soares MP (2014) Gut microbiota elicits a protective immune response against malaria transmission. Cell 159:1277–1289. https://doi.org/10.1016/j.cell.2014.10.053
Zhang M, Zhang T, Zhou L, Lou W, Zeng W, Liu T, Yin H, Liu H, Liu X, Mathivanan K, Praburaman L, Meng D (2022) Soil microbial community assembly model in response to heavy metal pollution. Environ Res 213:113576. https://doi.org/10.1016/j.envres.2022.113576
Zhao ZY, Ma YT, Feng TY, Kong X, Wang ZH, Zheng W, Zhai BN (2022) Assembly processes of abundant and rare microbial communities in orchard soil under a cover crop at different periods. Geoderma 406:115543. https://doi.org/10.1016/j.geoderma.2021.115543
Zheng W, Zhao ZY, Lv FL, Wang RZ, Wang ZH, Zhao ZY, Li ZY, Zhai BN (2021) Assembly of abundant and rare bacterial and fungal sub-communities in different soil aggregate sizes in an apple orchard treated with cover crop and fertilizer. Soil Biol Biochem 156:108222. https://doi.org/10.1016/j.soilbio.2021.108222
Acknowledgements
This work was jointly supported by grants from National Natural Science Foundation of China (Grant No. 42207367), Zhejiang Provincial Natural Science Foundation of China (Grant No. LGN20C150003; LGN22C150010), China Postdoctoral Science Foundation funded project (Grant No. 2022M711655), and Ningbo Public Welfare Science and Technology Plan Project (2022S190).
Funding
National Natural Science Foundation of China,42207367,Rui Tao,Natural Science Foundation of Zhejiang Province,LGN20C150003,Rui Tao,LGN22C150010,Maibo Jiang,Postdoctoral Research Foundation of China,2022M711655,Rui Tao
Author information
Authors and Affiliations
Contributions
J Li, F Meng, and Mb Jiang contributed to the methodology. Mb Jiang and Nn Chen performed data curation. Data visualization was performed by R Tao. Funding acquisition was by R Tao and Mb Jiang. The first draft of the manuscript was written by J Li. Writing—review & editing were performed by R Tao and Gx Chu.
Corresponding author
Ethics declarations
Conflict of interest
We declare that we have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, J., Meng, F., Chen, N. et al. Loss in the rare bacterial diversity drives the monocropping obstacle of cut chrysanthemum. J Soil Sci Plant Nutr (2024). https://doi.org/10.1007/s42729-024-01701-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s42729-024-01701-4