Continuous monocropping highly affect the composition and diversity of microbial communities in peanut (Arachis hypogaea L.)
DOI:
https://doi.org/10.15835/nbha49412532Keywords:
Archaea population structure, continuous monocropping, microbial responses, peanut (Arachis hypogaea L.), pathogen fungi, rhizosphere bacterial communityAbstract
Continuous cropping systems are the leading cause of decreased soil biological environments in terms of unstable microbial population and diversity index. Nonetheless, their responses to consecutive peanut monocropping cycles have not been thoroughly investigated. In this study, the structure and abundance of microbial communities were characterized using pyrosequencing-based approach in peanut monocropping cycles for three consecutive years. The results showed that continuous peanut cultivation led to a substantial decrease in soil microbial abundance and diversity from initial cropping cycle (T1) to later cropping cycle (T3). Peanut rhizosphere soil had Actinobacteria, Protobacteria, and Gemmatimonadetes as the major bacterial phyla. Ascomycota, Basidiomycota were the major fungal phylum, while Crenarchaeota and Euryarchaeota were the most dominant phyla of archaea. Several bacterial, fungal and archaeal taxa were significantly changed in abundance under continuous peanut cultivation. Bacterial orders, Actinomycetales, Rhodospirillales and Sphingomonadales showed decreasing trends from T1>T2>T3. While, pathogenic fungi Phoma was increased and beneficial fungal taxa Glomeraceae decreased under continuous monocropping. Moreover, Archaeal order Nitrososphaerales observed less abundant in first two cycles (T1&T2), however, it increased in third cycle (T3), whereas, Thermoplasmata exhibit decreased trends throughout consecutive monocropping. Taken together, we have shown the taxonomic profiles of peanut rhizosphere communities that were affected by continuous peanut monocropping. The results obtained from this study pave ways towards a better understanding of the peanut rhizosphere soil microbial communities in response to continuous cropping cycles, which could be used as bioindicator to monitor soil quality, plant health and land management practices.
References
Arafat Y, Tayyab M, Khan MU, Chen T, Amjad H, Awais S, … Lin S (2019). Long-term monoculture negatively regulates fungal community composition and abundance of tea orchards. Agronomy 9:466. https://doi.org/10.3390/agronomy9080466
Arafat Y, Wei X, Jiang Y, Chen T, Saqib HSA, Lin S, Lin W (2017). Spatial distribution patterns of root-associated bacterial communities mediated by root exudates in different aged ratooning tea monoculture systems. International Journal of Molecular Science 18. https://doi.org/10.3390/ijms18081727
Ball AS (2005). Soil health-a new challenge for microbiologists and chemists. International Microbiology 8:13-21. https://doi.org/10.2436/IM.V8I1.9493
Bardou P, Mariette J, Escudié F, Djemiel C, Klopp C (2014). jvenn: an interactive Venn diagram viewer. BMC bioinformatics 15:1-7. https://doi.org/10.1186/1471-2105-15-293
Bloem J, Hopkins DW, Benedetti A (2005). Microbiological methods for assessing soil quality. CABI. https://doi.org/10.1079/9780851990989.0000
Canarini A, Kaiser C, Merchant A, Richter A, Wanek W (2019). Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Frontiers in Plant Science 10:157. https://doi.org/10.3389/fpls.2019.00157
Chen M, Chi X, Pan L, Chen N, Wang T, Wang M, Yang Z, Yu S (2016). Research progress of soil microenvironment and peanut continuous cropping obstacle mechanism. Journal Anhui Agricultural Science 44:33-35. https://doi.org/10.13989/j.cnki.0517-6611
Chen M, Li X, Yang Q, Chi X, Pan L, Chen N, … Yu S (2012). Soil eukaryotic microorganism succession as affected by continuous cropping of peanut-pathogenic and beneficial fungi were selected. PLoS One 7:e40659. https://doi.org/10.1371/journal.pone.0040659
Chen M, Li X, Yang Q, Chi X, Pan L, Chen N, … Yu S (2014a). 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 M, Zhang J, Liu H, Wang M, Pan L, Chen N, … Du B (2020). Long-term continuously monocropped peanut significantly disturbed the balance of soil fungal communities. Journal of Microbiology 58:563-573. https://doi.org/10.7717/peerj.9024
Chong J, Liu P, Zhou G, Xia J (2020). Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nature Protocols 15:799-821. https://doi.org/10.1038/s41596-019-0264-1
Coskun D, Britto DT, Shi W, Kronzucker HJ (2017). How plant root exudates shape the nitrogen cycle. Trends in Plant Science 22:661-673. https://doi.org/10.1016/j.tplants.2017.05.004
Dai L, Zhang G, Yu Z, Ding H, Xu Y, Zhang Z (2019). Effect of drought stress and developmental stages on microbial community structure and diversity in peanut rhizosphere soil. International Journal of Molecular Sciences 20:2265. https://doi.org/10.3390/ijms20092265
Eisenhauer N, Lanoue A, Strecker T, Scheu S, Steinauer K, Thakur MP, Mommer L (2017). Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Scientific Reports 7:44641. https://doi.org/10.1038/srep44641
Fabra A, Castro S, Taurian T, Angelini J, Ibañez F, Dardanelli M, … Valetti L (2010). Interaction among Arachis hypogaea L. (peanut) and beneficial soil microorganisms: how much is it known? Critical Reviews in Microbiology 36:179-194. https://doi.org/10.3109/10408410903584863
Fisher RA (1936). The use of multiple measurements in taxonomic problems. Annals of Eugenics 7:179-188. https://doi.org/10.1111/j.1469-1809.1936.tb02137.x
Fournier B, Dos Santos SP, Gustavsen JA, Imfeld G, Lamy F, Mitchell EA, … Heger TJ (2020). Impact of a synthetic fungicide (fosetyl-Al and propamocarb-hydrochloride) and a biopesticide (Clonostachys rosea) on soil bacterial, fungal, and protist communities. Science of The Total Environment 738:139635. https://doi.org/10.1016/j.scitotenv.2020.139635
Harrison KA, Bardgett RD (2010). Influence of plant species and soil conditions on plant–soil feedback in mixed grassland communities. Journal of Ecology 98:384-395. https://doi.org/10.1111/j.1365-2745.2009.01614.x
Hartmann A, Rothballer M, Schmid M (2008). Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant and Soil 312:7-14. https://doi.org/10.1007/s11104-007-9514-z
Hu W, Pan J, Wang B, Guo J, Li M, Xu M (2020). Metagenomic insights into the metabolism and evolution of a new Thermoplasmata order (Candidatus gimiplasmatales). Environmental Microbiology. https://doi.org/10.1111/1462-2920.15349
Huang L-F, Song L-X, Xia X-J, Mao W-H, Shi K, Zhou Y-H, Yu J-Q (2013). Plant-soil feedbacks and soil sickness: from mechanisms to application in agriculture. Journal of Chemical Ecology 39:232-242. https://doi.org/10.1007/s10886-013-0244-9
Huang W, Sun D, Fu J, Zhao H, Wang R, An Y (2019). Effects of continuous sugar beet cropping on rhizospheric microbial communities. Genes (Basel) 11. https://doi.org/10.3390/genes11010013
Huang Y, Han L, Tao T, Yao Y, Yang J, Liang C, Xie J, Han X (2017). Bacterial community in peanut soils in various cropping systems. Allelopathy Journal 42:93-107. https://doi.org/10.26651/2017-42-1-1108
Jiang H, Shao H, Xiang Q, Gu Y, Li B, Gu H, Guan Y, Zhang Y (2020). Continuous Cropping and natural fallow practices affect tobacco fitness and soil microbiomes. Authorea Preprints. https://doi.org/10.22541/au.160279755.50286859/v1
Kaeberlein T, Lewis K, Epstein SS (2002). Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296:1127-1129. https://doi.org/10.1126/science.1070633
Kirk JL, Beaudette LA, Hart M, Moutoglis P, Klironomos JN, Lee H, Trevors JT (2004). Methods of studying soil microbial diversity. Journal of Microbiological Methods 58:169-188. https://doi.org/10.1016/j.mimet.2004.04.006
Larkin RP (2003). Characterization of soil microbial communities under different potato cropping systems by microbial population dynamics, substrate utilization, and fatty acid profiles. Soil Biology and Biochemistry 35:1451-1466. https://doi.org/10.1016/S0038-0717(03)00240-2
Li C, Li X, Kong W, Wu Y, Wang J (2010). Effect of monoculture soybean on soil microbial community in the Northeast China. Plant and Soil 330:423-433. https://doi.org/10.1007/s11104-009-0216-6
Li F, Hou B, Chen L, Yao Z, Hong G (2008). In vitro observation of the molecular interaction between NodD and its inducer naringenin as monitored by fluorescence resonance energy transfer. Acta Biochimica et Biophysica Sinica 40:783-789. https://doi.org/10.1111/J.1745-7270.2008.00462.X
Li H, Wang J, Liu Q, Zhou Z, Chen F, Xiang D (2019a). Effects of consecutive monoculture of sweet potato on soil bacterial community as determined by pyrosequencing. Journal of Basic Microbiology 59:181-191. https://doi.org/10.1002/jobm.201800304
Li P, Dai C, Wang X, Zhang T, Chen Y (2012). Variation of soil enzyme activities and microbial community structure in peanut monocropping system in subtropical China. African Journal of Agricultural Research 7:1870-1879. https://doi.org/10.5897/AJAR11.1713
Li P, Liu J, Jiang C, Wu M, Liu M, Wei S, … Li Z (2020a). Trade-off between potential phytopathogenic and non-phytopathogenic fungi in the peanut monoculture cultivation system. Applied Soil Ecology 148:103508. https://doi.org/10.1016/j.apsoil.2020.103508
Li X, Jousset A, De Boer W, Carrión VJ, Zhang T, Wang X, Kuramae EE (2019b). Legacy of land use history determines reprogramming of plant physiology by soil microbiome. The ISME Journal 13:738-751. https://doi.org/10.1038/s41396-018-0300-0
Li X, Panke-Buisse K, Yao X, Coleman-Derr D, Ding C, Wang X, Ruan H (2020b). Peanut plant growth was altered by monocropping-associated microbial enrichment of rhizosphere microbiome. Plant and Soil 446:655-669. https://doi.org/10.1007/s11104-019-04379-1
Li X-G, Ding C-F, Hua K, Zhang T-L, Zhang Y-N, Zhao L, Yang Y-R, Liu J-G, Wang X-X (2014a). Soil sickness of peanuts is attributable to modifications in soil microbes induced by peanut root exudates rather than to direct allelopathy. Soil Biology and Biochemistry 78:149-159. Htpps://doi.org/10.7717/peerj.9024
Li X-G, Ding C-F, Zhang T-L, Wang X-X (2014b). Fungal pathogen accumulation at the expense of plant-beneficial fungi as a consequence of consecutive peanut monoculturing. Soil Biology and Biochemistry 72:11-18. https://doi.org/10.1016/j.soilbio.2014.01.019
Li X-G, Zhang T-L, Wang X-X, Hua K, Zhao L, Han Z-M (2013). The composition of root exudates from two different resistant peanut cultivars and their effects on the growth of soil-borne pathogen. International Journal of Biological Sciences 9:164. https://doi.org/10.7150/ijbs.5579
Liao J, Xu Q, Xu H, Huang D (2019). Natural farming improves soil quality and alters microbial diversity in a cabbage field in Japan. Sustainability 11:3131. https://doi.org/10.3390/su11113131
Liechty Z, Santos-Medellin C, Edwards J, Nguyen B, Mikhail D, Eason S, … Sundaresan V (2020). Comparative analysis of root microbiomes of rice cultivars with high and low methane emissions reveals differences in abundance of methanogenic Archaea and putative upstream fermenters. mSystems 5. https://doi.org/10.1128/mSystems.00897-19
Liu J, Yao Q, Li Y, Zhang W, Mi G, Chen X, Yu Z, Wang G (2019a). Continuous cropping of soybean alters the bulk and rhizospheric soil fungal communities in a Mollisol of Northeast PR China. Land Degradation and Development 30:1725-1738. https://doi.org/10.1002/saj2.20069
Liu X, Zhang Y, Ren X, Chen B, Shen C, Wang F (2019b). Long-term greenhouse vegetable cultivation alters the community structures of soil ammonia oxidizers. Journal of Soils and Sediments 19:883-902. https://doi.org/10.1007/s11368-018-2089-x
Lopes LD, Hao J, Schachtman DP (2021). Alkaline soil pH affects bulk soil, rhizosphere and root endosphere microbiomes of plants growing in a Sandhills ecosystem. FEMS Microbiology Ecology 97. https://doi.org/10.1093/femsec/fiab028
Lynn TM, Liu Q, Hu Y, Yuan H, Wu X, Khai AA, Wu J, Ge T (2017). Influence of land use on bacterial and archaeal diversity and community structures in three natural ecosystems and one agricultural soil. Archives of Microbiology 199:711-721. https://doi.org/10.1007/s00203-017-1347-4
Mazzola M (2004). Assessment and management of soil microbial community structure for disease suppression 1. Annual Review of Phytopathology 42:35-59. https://doi.org/10.1146/annurev.phyto.42.040803.140408
Meier IC, Finzi AC, Phillips RP (2017). Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools. Soil Biology and Biochemistry 106:119-128. https://doi.org/10.1016/j.soilbio.2016.12.004
Mocali S, Benedetti A (2010). Exploring research frontiers in microbiology: the challenge of metagenomics in soil microbiology. Research in Microbiology 161:497-505. https://doi.org/10.1016/j.resmic.2010.04.010
Mommer L, Kirkegaard J, Van Ruijven J (2016). Root-root interactions: towards a rhizosphere framework. Trends in Plant Science 21:209-217. https://doi.org/10.1016/j.tplants.2016.01.009
Nannipieri P, Ascher J, Ceccherini M, Landi L, Pietramellara G, Renella G (2003). Microbial diversity and soil functions. European Journal of Soil Science 54:655-670. https://doi.org/10.1046/j.1351-0754.2003.0556.x
Pan J, Wang Q, Guo X, Jiang X, Cheng Q, Fu L, Liu W, Zhang L (2021). Local patterns of arbuscular mycorrhizal fungal diversity and community structure in a natural Toona ciliata var. pubescens forest in South Central China. PeerJ 9:e11331. https://doi.org/10.7717/peerj.11331
Pieterse CMJ, De Jonge R, Berendsen RL (2016). The soil-borne supremacy. Trends in Plant Science 21:171-173. https://doi.org/10.1016/j.tplants.2016.01.018
Raaijmakers JM, Mazzola M (2012). Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annual Review of Phytopathology 50:403-424. https://doi.org/10.1146/annurev-phyto-081211-172908
Rampelotto P, De Siqueira Ferreira A, Barboza A, Roesch L (2013). Changes in diversity, abundance, and structure of soil bacterial communities in Brazilian Savanna under different land use systems. Microbial Ecology 66:593-607. https://doi.org/10.1007/s00248-013-0235-y
Rincon-Florez VA, Carvalhais LC, Dang YP, Crawford MH, Schenk PM, Dennis PG (2020). Significant effects on soil microbial communities were not detected after strategic tillage following 44 years of conventional or no-tillage management. Pedobiologia 80:150640. https://doi.org/10.1016/j.pedobi.2020.150640
Schardl C, Craven K (2003). Interspecific hybridization in plant‐associated fungi and oomycetes: a review. Molecular Ecology 12:2861-2873. https://doi.org/10.1046/j.1365-294x.2003.01965.x
Schink B (1992). Syntrophism among prokaryotes. The Prokaryotes. https://doi.org/10.1007/0-387-30742-7_11
Sharma SK, Ramesh A, Sharma MP, Joshi OP, Govaerts B, Steenwerth KL, Karlen DL (2010). Microbial community structure and diversity as indicators for evaluating soil quality. Biodiversity, Biofuels, Agroforestry and Conservation Agriculture 317-358. https://doi.org/10.1007/978-90-481-9513-8_11
Song ZQ, Wang FP, Zhi XY, Chen JQ, Zhou EM, Liang F, … Li WJ (2013). Bacterial and archaeal diversities in Yunnan and Tibetan hot springs, China. Environmental Microbiology 15:1160-1175. https://doi.org/10.1111/1462-2920.12025
Sørensen J, Nicolaisen MH, Ron E, Simonet P (2009). Molecular tools in rhizosphere microbiology-from single-cell to whole-community analysis. Plant and Soil 321:483-512. https://doi.org/10.1007/s11104-009-9946-8
Steinauer K, Chatzinotas A, Eisenhauer N (2016). Root exudate cocktails: the link between plant diversity and soil microorganisms? Ecology and Evolution 6:7387-7396. https://doi.org/10.1002/ece3.2454
Streit WR, Schmitz RA (2004). Metagenomics–the key to the uncultured microbes. Current Opinion in Microbiology 7:492-498. https://doi.org/10.1016/j.mib.2004.08.002
Sui N, Wang Y, Liu S, Yang Z, Wang F, Wan S (2018). Transcriptomic and physiological evidence for the relationship between unsaturated fatty acid and salt stress in peanut. Frontiers in Plant Science 9:7. https://doi.org/10.3389/fpls.2018.00007
Taffner J, Bergna A, Cernava T, Berg G (2020). Tomato-associated archaea show a cultivar-specific rhizosphere effect but an unspecific transmission by seeds. Phytobiomes Journal 4:133-141. https://doi.org/10.1094/PBIOMES-01-20-0017-R
Taffner J, Cernava T, Erlacher A, Berg G (2019). Novel insights into plant-associated archaea and their functioning in arugula (Eruca sativa Mill.). Journal of Advanced Research 19:39-48. https://doi.org/10.1016/j.jare.2019.04.008
Tang X, Zhong R, Jiang J, He L, Huang Z, Shi G, … He L (2020). Cassava/peanut intercropping improves soil quality via rhizospheric microbes increased available nitrogen contents. BMC Biotechnology 20:13. https://doi.org/10.1186/s12896-020-00606-1
Tian L, Shi S, Ma L, Tran LP, Tian C (2020). Community structures of the rhizomicrobiomes of cultivated and wild soybeans in their continuous cropping. Microbiology Research 232:126390. https://doi.org/10.1016/j.micres.2019.126390
Tringe SG, Von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW, … Detter JC (2005). Comparative metagenomics of microbial communities. Science 308:554-557. https://doi.org/10.1126/science.1107851
Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van Der Putten WH, Wall DH (2004). Ecological linkages between aboveground and belowground biota. Science 304:1629-1633. https://doi.org/10.1126/science.1094875
Wehner J, Antunes PM, Powell JR, Mazukatow J, Rillig MC (2010). Plant pathogen protection by arbuscular mycorrhizas: a role for fungal diversity? Pedobiologia 53:197-201. https://doi.org/10.1016/j.pedobi.2009.10.002
Xie XG, Zhao YY, Yang Y, Lu F, Dai CC (2020). Endophytic fungus alleviates soil sickness in peanut crops by improving the carbon metabolism and rhizosphere bacterial diversity. Microbial Ecology 82:49-61. https://doi.org/10.1007/s00248-020-01555-0
Xu Y, Ge Y, Song J, Rensing C (2020). Assembly of root-associated microbial community of typical rice cultivars in different soil types. Biology and Fertility of Soils 56:249-260. https://doi.org/10.1007/s42832-020-0063-1
Zhao Q, Xiong W, Xing Y, Sun Y, Lin X, Dong Y (2018). Long-term coffee monoculture alters soil chemical properties and microbial communities. Scientific Reports 8:6116. https://doi.org/10.1038/s41598-018-24537-2
Zhao Y, Mao X, Zhang M, Yang W, Di HJ, Ma L, Liu W, Li B (2020). Response of soil microbial communities to continuously mono-cropped cucumber under greenhouse conditions in a calcareous soil of north China. Journal of Soils and Sediments 1-14. https://doi.org/10.1007/s11368-020-02603-5
Downloads
Additional Files
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Ali I. MALLANO, Xianli ZHAO, Yanling SUN, Guangpin JIANG, Huang CHAO
This work is licensed under a Creative Commons Attribution 4.0 International License.
License:
Open Access Journal:
The journal allows the author(s) to retain publishing rights without restriction. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author.