Impact of Maize–Mushroom Intercropping on the Soil Bacterial Community Composition in Northeast China
Abstract
:1. Introduction
2. Materials and Methods
2.1. Site Description and Experimental Design
2.2. Soil Sampling
2.3. Soil Chemical Assays
2.4. DNA Extraction and MiSeq Sequencing
2.5. Data Analysis
3. Results
3.1. Soil Chemical Properties
3.2. Soil Bacterial Community Diversity
3.3. Soil Bacterial Community Structure
3.4. Comparative Analysis of Soil Bacterial Community
3.5. Metabolism of Soil Microbial Community
4. Discussion
4.1. Soil Physicochemical Properties
4.2. Bacterial Community Diversity
4.3. Bacterial Community Structure
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- NBSC (National Bureau of Statistics of China). National Statistical Yearbook; China Statistics Press: Beijing, China, 2017. [Google Scholar]
- Zhu, X.; Sun, L.; Song, F.; Liu, S.; Liu, F.; Li, X. Soil microbial community and activity are affected by integrated agricultural practices in China. Eur. J. Soil Sci. 2018, 69, 924–935. [Google Scholar] [CrossRef]
- Zaeem, M.; Nadeem, M.; Pham, T.H.; Ashiq, W.; Ali, W.; Gilani, S.S.M.; Elavarthi, S.; Kavanagh, V.; Cheema, M.; Galagedara, L.; et al. The potential of corn-soybean intercropping to improve the soil health status and biomass production in cool climate boreal ecosystems. Sci. Rep. 2019, 9, 13148. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fu, Z.; Zhou, L.; Chen, P.; Du, Q.; Pang, T.; Song, C.; Wang, X.; Liu, W.; Yang, W.; Yong, T. Effects of maize-soybean relay intercropping on crop nutrient uptake and soil bacterial community. J. Integr. Agr. 2019, 18, 2006–2018. [Google Scholar] [CrossRef]
- De Freitas, M.A.M.; Silva, D.V.; Guimaraes, F.R.; Leal, P.L.; Moreira, F.M.D.; da Silva, A.A.; Souza, M.D. Biological attributes of soil cultivated with corn intercropped with Urochloa brizantha in different plant arrangements with and without herbicide application. Agr. Ecosyst. Environ. 2018, 254, 35–40. [Google Scholar] [CrossRef]
- Nyawade, S.O.; Karanja, N.N.; Gachene, C.K.K.; Gitari, H.I.; Schulte-Geldermann, E.; Parker, M.L. Short-term dynamics of soil organic matter fractions and microbial activity in smallholder potato-legume intercropping systems. Appl. Soil Ecol. 2019, 142, 123–135. [Google Scholar] [CrossRef]
- Bünemann, E.K.; Bongiorno, G.; Bai, Z.; Creamer, R.E.; De Deyn, G.; de Goede, R.; Fleskens, L.; Geissen, V.; Kuyper, T.W.; Mäder, P.; et al. Soil quality—A critical review. Soil Biol. Biochem. 2018, 120, 105–125. [Google Scholar] [CrossRef]
- Jonathan, S.; Oyetunji, O.; Asemoloye, M.J.N. Asemoloye, Influence of spent mushroom compost (SMC) of Pleurotus ostreatus on the yield and nutrient compositions of Telfairia occidentalis Hook.F.A. (Pumpkin), a Nigerian leafy vegetable. Nat. Sci. 2012, 10, 149–156. [Google Scholar]
- Wang, B. New mushroom cultivation technology between field crop maize rows. J. Shanxi Agric. Sci. 2009, 37, 91–92. [Google Scholar]
- Griffiths, B.S.; Philippot, L. Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol. Rev. 2013, 37, 112–129. [Google Scholar] [CrossRef] [Green Version]
- Zheng, W.; Gong, Q.; Zhao, Z.; Liu, J.; Zhai, B.; Wang, Z.; Li, Z. Changes in the soil bacterial community structure and enzyme activities after intercrop mulch with cover crop for eight years in an orchard. Eur. J. Soil Biol. 2018, 86, 34–41. [Google Scholar] [CrossRef]
- Gong, X.; Liu, C.; Li, J.; Luo, Y.; Yang, Q.; Zhang, W.; Yang, P.; Feng, B. Responses of rhizosphere soil properties, enzyme activities and microbial diversity to intercropping patterns on the Loess Plateau of China. Soil Till. Res. 2019, 195, 104355. [Google Scholar] [CrossRef]
- Monneveux, P.; Quillerou, E.; Sanchez, C.; Lopez-Cesati, J. Effect of zero tillage and residues conservation on continuous maize cropping in a subtropical environment (Mexico). Plant Soil 2006, 279, 95–105. [Google Scholar] [CrossRef]
- She, S.; Niu, J.; Zhang, C.; Xiao, Y.; Chen, W.; Dai, L.; Liu, X.; Yin, H.J.A.o.M. Significant relationship between soil bacterial community structure and incidence of bacterial wilt disease under continuous cropping system. Arch. Microbiol. 2017, 199, 267–275. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.; Hou, D.; Wu, W.; Sun, W.; Qiu, L. Influence of interplanting Pleurotus ostreatus on soil biological activity and fruit quality in pear orchard. J. Fruit Sci. 2012, 29, 583–588. [Google Scholar]
- Mohamed, M.F.; Nassef, D.M.T.; Waly, E.A.; Kotb, A.M. Production of oyster mushroom (Pleurotus spp.) intercropped with field grown faba bean (Vicia faba L.). Asian. J. Crop Sci. 2014, 6, 27–37. [Google Scholar] [CrossRef] [Green Version]
- Yang, X.; Wang, Y.; Qi, X.; Sun, L.; Zhang, M.; Song, F.; Liu, S.; Li, X.; Zhu, X. Effects of maize/mushroom intercropping on photosynthetic characteristics of maize ear leaf under high photosynthetic efficiency planting pattern. Soil Crops 2020, 9, 166–177. [Google Scholar]
- Sun, L.; Song, F.; Liu, S.; Cao, Q.; Liu, F.; Zhu, X. Integrated agricultural management practice improves soil quality in Northeast China. Arch. Agron. Soil Sci. 2018, 64, 1932–1943. [Google Scholar] [CrossRef]
- Zhu, X.; Yang, W.; Song, F.; Li, X. Diversity and composition of arbuscular mycorrhizal fungal communities in the cropland black soils of China. Glob. Ecol. Conserv. 2020, 22, e00964. [Google Scholar] [CrossRef]
- Gu, Z.; Li, G.; Du, Y.; Li, J.; Cai, F.; Wang, H. Investigation on parameters affecting the determination of organic matter in forest soil by potassium dichromate heating oxidation-volumetric method. Hubei For. Sci. Technol. 2014, 43, 24–26. [Google Scholar]
- Lei, Y.; Xiao, Y.; Li, L.; Jiang, C.; Zu, C.; Li, T.; Cao, H. Impact of tillage practices on soil bacterial diversity and composition under the tobacco-rice rotation in China. J. Microbiol. 2017, 55, 349–356. [Google Scholar] [CrossRef]
- Magoč, T.; Salzberg, S.L. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 2011, 27, 2957–2963. [Google Scholar] [CrossRef] [PubMed]
- Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Peña, A.G.; Goodrich, J.K.; Gordon, J.I.J.N.M. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7, 335–336. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Edgar, R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26, 2460–2461. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bokulich, N.A.; Subramanian, S.; Faith, J.J.; Gevers, D.; Gordon, J.I.; Knight, R.; Mills, D.A.; Caporaso, J.G. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 2013, 10, 57. [Google Scholar] [CrossRef]
- DeSantis, T.Z.; Hugenholtz, P.; Larsen, N.; Rojas, M.; Brodie, E.L.; Keller, K.; Huber, T.; Dalevi, D.; Hu, P.; Andersen, G.L. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 2006, 72, 5069–5072. [Google Scholar] [CrossRef] [Green Version]
- Segata, N.; Izard, J.; Waldron, L.; Gevers, D.; Miropolsky, L.; Garrett, W.S.; Huttenhower, C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011, 12, R60. [Google Scholar] [CrossRef] [Green Version]
- Langille, M.G.I.; Zaneveld, J.; Caporaso, J.G.; McDonald, D.; Knights, D.; Reyes, J.A.; Clemente, J.C.; Burkepile, D.E.; Vega Thurber, R.L.; Knight, R.; et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 2013, 31, 814–821. [Google Scholar] [CrossRef]
- Fuentes, M.; Govaerts, B.; De León, F.; Hidalgo, C.; Dendooven, L.; Sayre, K.D.; Etchevers, J. Fourteen years of applying zero and conventional tillage, crop rotation and residue management systems and its effect on physical and chemical soil quality. Eur. J. Agron. 2009, 30, 228–237. [Google Scholar] [CrossRef]
- Li, Q.; Chen, J.; Wu, L.; Luo, X.; Li, N.; Arafat, Y.; Lin, S.; Wang, X. Belowground interactions impact the soil bacterial community, soil fertility, and crop yield in maize/peanut intercropping systems. Int. J. Mol. Sci. 2018, 19, 622. [Google Scholar] [CrossRef] [Green Version]
- Sun, Y.; Zhang, N.; Wang, E.; Yuan, H.; Yang, J.; Chen, W. Influence of intercropping and intercropping plus rhizobial inoculation on microbial activity and community composition in rhizosphere of alfalfa (Medicago sativa L.) and Siberian wild rye (Elymus sibiricus L.). FEMS Microbiol. Ecol. 2010, 70, 62–70. [Google Scholar]
- Du, B.; Pang, J.; Hu, B.; Allen, D.E.; Bell, T.L.; Pfautsch, S.; Netzer, F.; Dannenmann, M.; Zhang, S.; Rennenberg, H. N2-fixing black locust intercropping improves ecosystem nutrition at the vulnerable semi-arid Loess Plateau region, China. Sci. Total Environ. 2019, 688, 333–345. [Google Scholar] [CrossRef] [PubMed]
- de Oliveira, A.B.; Cantarel, A.A.M.; Seiller, M.; Florio, A.; Bérard, A.; Hinsinger, P.; Cadre, E.L. Short-term plant legacy alters the resistance and resilience of soil microbial communities exposed to heat disturbance in a Mediterranean calcareous soil. Ecol. Indic. 2020, 108, 105740. [Google Scholar] [CrossRef]
- Kebeney, S.J.; Semoka, J.M.R.; Msanya, B.M.; Ng’Etich, W.K.; Chemei, D.K. Effects of nitrogen fertilizer rates and soybean residue management on nitrate nitrogen in sorghum-soybean intercropping system. Int. J. Plant Soil Sci. 2014, 4, 212–229. [Google Scholar] [CrossRef]
- Phiri, A.T.; Weil, R.R.; Yobe, G.; Msaky, J.J.; Mrema, J.; Grossman, J.; Harawa, R. Insitu assessment of soil nitrate-nitrogen in the pigeon pea-groundnut intercropping-maize rotation system: Implications on nitrogen management for increased maize productivity. Int. Res. J. Agric. Sci. Soil Sci. 2014, 2, 13–29. [Google Scholar]
- Vieira, F.R.; Pecchia, J.A.; Segato, F.; Polikarpov, I. Exploring oyster mushroom (Pleurotus ostreatus) substrate preparation by varying phase I composting time: Changes in bacterial communities and physicochemical composition of biomass impacting mushroom yields. J. Appl. Microbiol. 2019, 126, 931–944. [Google Scholar] [CrossRef]
- Kim, D.G. Estimation of net gain of soil carbon in a nitrogen-fixing tree and crop intercropping system in sub-Saharan Africa: Results from re-examining a study. Agroforest Syst. 2012, 86, 175–184. [Google Scholar] [CrossRef]
- Dos Santos Soares, D.; Ramos, M.L.G.; Marchão, R.L.; Maciel, G.A.; de Oliveira, A.D.; Malaquias, J.V.; de Carvalho, A.M. How diversity of crop residues in long-term no-tillage systems affect chemical and microbiological soil properties. Soil Tillage Res. 2019, 194, 104316. [Google Scholar] [CrossRef]
- Trivedi, P.; Delgadobaquerizo, M.; Anderson, I.C.; Singh, B.K. Response of soil properties and microbial communities to agriculture: Implications for primary productivity and soil health indicators. Front. Plant Sci. 2016, 7, 990. [Google Scholar] [CrossRef] [Green Version]
- Yang, G.; Ma, K.; Lu, F.; Wei, C.; Dai, X. Effect of continuous cropping of potato on allelochemicals and soil microbial community. J. Ecol. Rural Environ. 2015, 31, 711–717. [Google Scholar]
- Qin, X.; Zheng, Y.; Tang, L.; Long, G. Effects of maize and potato intercropping on rhizosphere microbial community structure and diversity. Acta Agron. Sin. 2015, 41, 919–928. [Google Scholar] [CrossRef]
- Acosta-Martínez, V.; Acosta-Mercado, D.; Sotomayor-Ramírez, D.; Cruz-Rodríguez, L. Microbial communities and enzymatic activities under different management in semiarid soils. Appl. Soil Ecol. 2008, 38, 249–260. [Google Scholar] [CrossRef]
- Zhang, M.; Wang, N.; Hu, Y.; Sun, G. Changes in soil physicochemical properties and soil bacterial community in mulberry (Morus alba L.)/alfalfa (Medicago sativa L.) intercropping system. Microbiol. Open 2018, 7, e00555. [Google Scholar] [CrossRef] [PubMed]
- Lupwayi, N.Z.; May, W.E.; Kanashiro, D.A.; Petri, R.M. Soil bacterial community responses to black medic cover crop and fertilizer N under no-till. Appl. Soil Ecol. 2018, 124, 95–103. [Google Scholar] [CrossRef]
- Yu, H.; Chen, S.; Zhang, X.; Zhou, X.; Wu, F. Rhizosphere bacterial community in watermelon-wheat intercropping was more stable than in watermelon monoculture system under Fusarium oxysporum f. sp. niveum invasion. Plant Soil 2019, 445, 369–381. [Google Scholar] [CrossRef]
- Hugenholtz, P.; Goebel, B.M.; Pace, N.R. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 1998, 180, 4765–4774. [Google Scholar] [CrossRef] [Green Version]
- Thiel, V.; Fukushima, S.I.; Kanno, N.; Hanada, S. Chloroflexi. In Encyclopedia of Microbiology, 4th ed.; Schmidt, T.M., Ed.; Academic Press: Cambridge, MA, USA, 2019; pp. 651–662. [Google Scholar]
- Chistoserdova, L.; Jenkins, C.; Kalyuzhnaya, M.G.; Marx, C.J.; Lapidus, A.; Vorholt, J.A.; Staley, J.T.; Lidstrom, M.E. The enigmatic planctomycetes may hold a key to the origins of methanogenesis and methylotrophy. Mol. Biol. Evol. 2004, 21, 1234. [Google Scholar] [CrossRef] [Green Version]
- Kindaichi, T.; Yamaoka, S.; Uehara, R.; Ozaki, N.; Ohashi, A.; Albertsen, M.; Nielsen, P.H.; Nielsen, J.L. Phylogenetic diversity and ecophysiology of candidate phylum Saccharibacteria in activated sludge. FEMS Microbiol. Ecol. 2016, 92, fiw078. [Google Scholar] [CrossRef] [Green Version]
- Ahn, J.H.; Lee, S.A.; Kim, J.M.; Kim, M.S.; Song, J.; Weon, H.Y. Dynamics of bacterial communities in rice field soils as affected by different long-term fertilization practices. J. Microbiol. 2016, 54, 724–731. [Google Scholar] [CrossRef]
- Wackett, L.P. Pseudomonas putida-a versatile biocatalyst. Nat. Biotechnol. 2003, 21, 136–138. [Google Scholar] [CrossRef]
- Bever, J.D.; Dickie, I.A.; Facelli, E.; Facelli, J.M.; Klironomos, J.; Moora, M.; Rillig, M.C.; Stock, W.D.; Tibbett, M.; Zobel, M. Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 2010, 25, 468–478. [Google Scholar] [CrossRef] [Green Version]
- Lladó, S.; Žifčáková, L.; Větrovský, T.; Eichlerová, I.; Baldrian, P. Functional screening of abundant bacteria from acidic forest soil indicates the metabolic potential of Acidobacteria subdivision 1 for polysaccharide decomposition. Biol. Fertil. Soils 2016, 52, 251–260. [Google Scholar] [CrossRef]
- Rashad, F.M.; Fathy, H.M.; El-Zayat, A.S.; Elghonaimy, A.M. Isolation and characterization of multifunctional Streptomyces species with antimicrobial, nematicidal and phytohormone activities from marine environments in Egypt. Microbiol. Res. 2015, 175, 34–47. [Google Scholar] [CrossRef] [PubMed]
- Binnie, C.; Cossar, J.D.; Stewart, D.I.H. Heterologous biopharmaceutical protein expression in Streptomyces. Trends Biotechnol. 1997, 15, 315–320. [Google Scholar] [CrossRef]
- Tao, T.; Yue, Y.; Chen, W.; Chen, W. Proposal of Nakamurella gen. nov. as a substitute for the bacterial genus Microsphaera Yoshimi et al. 1996 and Nakamurellaceae fam. nov. as a substitute for the illegitimate bacterial family Microsphaeraceae Rainey et al. 1997. Int. J. Syst. Evol. Microbiol. 2004, 54, 999–1000. [Google Scholar] [CrossRef] [PubMed]
- Subhashini, D. Growth promotion and increased potassium uptake of tobacco by potassium-mobilizing bacterium Frateuria aurantia grown at different potassium levels in vertisols. Commun. Soil Sci. Plant Anal. 2015, 46, 210–220. [Google Scholar] [CrossRef]
- Li, F.; Chen, L.; Zhang, J.; Yin, J.; Huang, S. Bacterial community structure after long-term organic and inorganic fertilization reveals important associations between soil nutrients and specific taxa involved in nutrient transformations. Front. Microbiol. 2017, 8, 187. [Google Scholar] [CrossRef] [Green Version]
- Kojima, M.; Kimura, N.; Miura, R. Regulation of primary metabolic pathways in oyster mushroom mycelia induced by blue light stimulation: Accumulation of shikimic acid. Sci. Rep. 2015, 5, 8630. [Google Scholar] [CrossRef]
- Ngwene, B.; Neugart, S.; Baldermann, S.; Ravi, B.; Schreiner, M. Intercropping induces changes in specific secondary metabolite concentration in Ethiopian Kale (Brassica carinata) and African Nightshade (Solanum scabrum) under controlled conditions. Front. Plant Sci. 2017, 8, 1700. [Google Scholar] [CrossRef]
- Zhang, X.; Gao, G.; Wu, Z.; Wen, X.; Zhong, H.; Zhong, Z.; Bian, F.; Gai, X. Agroforestry alters the rhizosphere soil bacterial and fungal communities of moso bamboo plantations in subtropical China. Appl. Soil Ecol. 2019, 143, 192–200. [Google Scholar] [CrossRef]
Planting Pattern | pH | TN (g kg−1) | AN (mg kg−1) | NO3−-N (mg kg−1) | NH4+-N (mg kg−1) | SOM% |
---|---|---|---|---|---|---|
Maize | 6.37 ± 0.10 b | 1.28 ± 1.49 a | 257 ± 33.6 a | 191 ± 58 a | 51.3 ± 15.3 a | 3.12 ± 0.15 b |
Mushroom | 7.49 ± 0.05 a | 1.39 ± 0.60 a | 169 ± 10.4 b | 2.19 ± 0.27 b | 4.15 ± 0.46 b | 3.23 ± 0.05 ab |
Intercropping | 7.40 ± 0.04 a | 1.51 ± 1.05 a | 170 ± 8.65 b | 19.8 ± 3.39 b | 8.41 ± 0.69 b | 3.59 ± 0.10 a |
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Yang, X.; Wang, Y.; Sun, L.; Qi, X.; Song, F.; Zhu, X. Impact of Maize–Mushroom Intercropping on the Soil Bacterial Community Composition in Northeast China. Agronomy 2020, 10, 1526. https://doi.org/10.3390/agronomy10101526
Yang X, Wang Y, Sun L, Qi X, Song F, Zhu X. Impact of Maize–Mushroom Intercropping on the Soil Bacterial Community Composition in Northeast China. Agronomy. 2020; 10(10):1526. https://doi.org/10.3390/agronomy10101526
Chicago/Turabian StyleYang, Xiaoqin, Yang Wang, Luying Sun, Xiaoning Qi, Fengbin Song, and Xiancan Zhu. 2020. "Impact of Maize–Mushroom Intercropping on the Soil Bacterial Community Composition in Northeast China" Agronomy 10, no. 10: 1526. https://doi.org/10.3390/agronomy10101526