|Green manuring facilitates bacterial community dispersal across different compartments of subsequent tobacco
LIANG Hai1*, FU Li-bo2*, CHEN Hua2, ZHOU Guo-peng3, GAO Song-juan1#, CAO Wei-dong3#
1 College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, P.R.China
2 Institute of Agricultural Environment and Resources, Yunnan Academy of Agricultural Sciences, Kunming 650205, P.R.China
3 Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture and Rural Affairs/Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
绿肥-作物轮作作为一项可持续农艺措施，具有增强作物抗病、提升作物产量的效果。 然而，绿肥施用对作物相关微生物群落构建的调控机制尚不清楚。 本研究通过烟草与紫云英、黑麦草、肥田萝卜和冬闲（不施绿肥）四种轮作方式的田间试验，研究烟草不同区室（非根际土、根际土、根表及根内）细菌群落水平构建过程。 结果表明：与冬闲处理相比，绿肥各处理相邻区室构建的共现网络具有更多的边，表明其土壤-根界面存在显著的微生物相互作用。绿肥施用提高了土壤各区室间的扩散-生态位连续指数，促进了微生物的水平扩散。 对于不同的绿肥处理，中性群落模型对细菌出现频率的解释为24.6-27.6%，且每种处理至少有一个区室的归一化随机率高于50%边界，表明确定性和随机过程共同塑造了烟草微生物群落。综上所述，绿肥施用促进了不同区室间细菌群落的扩散，增强了相邻区室潜在的相互作用。本研究为了解绿肥-作物轮作条件下微生物群落的构建过程提供了经验依据。
Green manure–crop rotation is a sustainable approach to protect crops against diseases and improve yield. However, the mechanism by which green manuring manipulates the crop-associated microbial community remains to be elucidated. In this study, we explored the horizontal processes of bacterial communities in different compartments of the soil–root interface (bulk soil, rhizosphere soil, rhizoplane and endosphere) of tobacco by performing a field experiment including four rotation practices, namely, tobacco rotated with smooth vetch, ryegrass, radish, and winter fallow (without green manure). Results showed that the co-occurrence networks constructed by adjacent compartments of the soil–root interface with green manuring had more edges than without green manuring, indicating dramatic microbial interactions. Green manuring increased the dispersal-niche continuum index between bulk soil and other compartments, indicating that it facilitated the horizontal dispersal of microbes. For the different green manuring practices, the neutral community model explained 24.6–27.6% of detection frequency for bacteria, and at least one compartment under each practice had a normalized stochasticity ratio higher than the 50% boundary point, suggesting that the deterministic and stochastic processes jointly shaped the tobacco microbiome. In conclusion, green manuring generally facilitates bacterial community dispersal across different compartments and enhances potential interactions among adjacent compartments. This study provides empirical evidence for understanding the microbiome assembly under green manure–crop rotation.
Received: 28 April 2022
Accepted: 13 June 2022
|Fund: This work was supported financially by the National Key Research and Development Program of China (2021YFD1700200) and the China Agriculture Research System of MOF and MARA (CARS-22).
|About author: LIANG Hai, E-mail: firstname.lastname@example.org; FU Li-bo, E-mail: email@example.com; #Correspondence GAO Song-juan, E-mail: firstname.lastname@example.org; CAO Wei-dong, E-mail: email@example.com
* These authors contributed equally to this study
Cite this article:
LIANG Hai, FU Li-bo, CHEN Hua, ZHOU Guo-peng, GAO Song-juan, CAO Wei-dong.
Green manuring facilitates bacterial community dispersal across different compartments of subsequent tobacco. Journal of Integrative Agriculture, 22(4): 1199-1215.
| Bahram M, Kohout P, Anslan S, Harend H, Abarenkov K, Tedersoo L. 2016. Stochastic distribution of small soil eukaryotes resulting from high dispersal and drift in a local environment. ISME Journal, 10, 885–896.
Bai Y, Müller D B, Srinivas G, Garrido-Oter R, Potthoff E, Rott M, Dombrowski N, Münch P C, Spaepen S, Remus-Emsermann M, Hüttel B, McHardy A C, Vorholt J A, Schulze-Lefert P. 2015. Functional overlap of the Arabidopsis leaf and root microbiota. Nature, 528, 364–369.
Bais H P, Loyola-Vargas V M, Flores H E, Vivanco J M. 2001. Root-specific metabolism: The biology and biochemistry of underground organs. In Vitro Cellular and Developmental Biology (Plant), 37, 730–741.
Bais H P, Weir T L, Perry L G, Gilroy S, Vivanco J M. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology, 57, 233–266.
Bansept F, Obeng N, Schulenburg H, Traulsen A. 2021. Modeling host-associating microbes under selection. ISME Journal, 15, 3648–3656.
Barel J M, Kuyper T W, de Boer W, Douma J C, de Deyn G B. 2018. Legacy effects of diversity in space and time driven by winter cover crop biomass and nitrogen concentration. Journal of Applied Ecology, 55, 299–310.
Barnes C J, van der Gast C J, Burns C A, McNamara N P, Bending G D. 2016. Temporally variable geographical distance effects contribute to the assembly of root-associated fungal communities. Frontiers in Microbiology, 7, 196.
Beckers B, de Beeck M, Thijs S, Truyens S, Weyens N, Boerjan W, Vangronsveld J. 2016. Performance of 16s rDNA primer pairs in the study of rhizosphere and endosphere bacterial microbiomes in metabarcoding studies. Frontiers in Microbiology, 7, 650.
Beckers B, de Beeck M O, Weyens N, Boerjan W, Vangronsveld J. 2017. Structural variability and niche differentiation in the rhizosphere and endosphere bacterial microbiome of field-grown poplar trees. Microbiome, 5, 25.
Berendsen R L, Pieterse C M J, Bakker P A H M. 2012. The rhizosphere microbiome and plant health. Trends in Plant Science, 17, 478–486.
Bulgarelli D, Garrido-Oter R, Münch P C, Weiman A, Dröge J, Pan Y, McHardy A C, Schulze-Lefert P. 2015. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host and Microbe, 17, 392–403.
Bulgarelli D, Rott M, Schlaeppi K, ver Themaat E V L, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner F O, Amann R, Eickhorst T, Schulze-Lefert P. 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature, 488, 91–95.
Burns A R, Stephens, W Z, Stagaman K, Wong S, Rawls J F, Guillemin K, Bohannan B J M, 2016. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME Journal, 10, 655–664.
Callahan B J, McMurdie P J, Rosen M J, Han A W, Johnson A J A, Holmes S P. 2016. DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13, 581–583.
Chase J M. 2007. Drought mediates the importance of stochastic community assembly. Proceedings of the National Academy of Sciences of the United States of America, 104, 17430–17434.
Chen W, Ren K, Isabwe A, Chen H, Liu M, Yang J. 2019. Stochastic processes shape microeukaryotic community assembly in a subtropical river across wet and dry seasons. Microbiome, 7, 1.
Chen W, Pan Y, Yu L, Yang J, Zhang W. 2017. Patterns and processes in marine microeukaryotic community biogeography from Xiamen coastal waters and intertidal sediments, southeast China. Frontiers in Microbiology, 8, 1912.
Cordovez V, Dini-Andreote F, Carrión V J, Raaijmakers J M. 2019. Ecology and evolution of plant microbiomes. Annual Review of Microbiology, 73, 69–88.
Dahlstrom K M, McRose D L, Newman D K. 2020. Keystone metabolites of crop rhizosphere microbiomes. Current Biology, 30, R1131–R1137.
Du X, Deng Y, Li S, Escalas A, Feng K, He Q, Wang Z, Wu Y, Wang D, Peng X, Wang S. 2021. Steeper spatial scaling patterns of subsoil microbiota are shaped by deterministic assembly process. Molecular Ecology, 30, 1072–1085.
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty N K, Bhatnagar S, Eisen J A, Sundaresan V, Jeffery L D. 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. Proceedings of the National Academy of Sciences of the United States of America, 112, E911-E920.
Emmett B D, Buckley D H, Drinkwater L E. 2020. Plant growth rate and nitrogen uptake shape rhizosphere bacterial community composition and activity in an agricultural field. New Phytologist, 225, 960–973.
Faith D P. 1992. Conservation evaluation and phylogenetic diversity. Biological Conservation, 61, 1–10.
Gao S, Cao W, Zhou G, Res R M. 2021. Bacterial communities in paddy soils changed by milk vetch as green manure: A study conducted across six provinces in South China. Pedosphere, 31, 521–530.
Gao S, Zhou G, Rees R M, Cao W. 2020. Green manuring inhibits nitrification in a typical paddy soil by changing the contributions of ammonia-oxidizing archaea and bacteria. Applied Soil Ecology, 156, 10369.
Gibert C, Escarguel G. 2019. PER-SIMPER - A new tool for inferring community assembly processes from taxon occurrences. Global Ecology and Biogeography, 28, 374–385.
Gravel D, Canham C D, Beaudet M, Messier C. 2006. Reconciling niche and neutrality: The continuum hypothesis. Ecology Letters, 9, 399–409.
Guttman D S, McHardy A C, Schulze-Lefert P. 2014. Microbial genome-enabled insights into plant-microorganism interactions. Nature Reviews Genetics, 15, 797–813.
Hamonts K, Trivedi P, Garg A, Janitz C, Grinyer J, Holford P, Botha F C, Anderson I C, Singh B K. 2018. Field study reveals core plant microbiota and relative importance of their drivers. Environmental Microbiology, 20, 124–140.
Hassani M A, Durán P, Hacquard S. 2018. Microbial interactions within the plant holobiont. Microbiome, 6, 58.
Kaiser C, Kilburn M R, Clode P L, Fuchslueger L, Koranda M, Cliff J B, Solaiman Z M, Murphy D V. 2015. Exploring the transfer of recent plant photosynthates to soil microbes: Mycorrhizal pathway vs direct root exudation. New Phytologist, 205, 1537–1551.
Kaur P, Kumar A, Arora V. 2020. Plant growth promoting rhizobacteria. Plant Cell Biotechnology and Molecular Biology, 21, 63–64.
Kembel S W, O’Connor T K, Arnold H K, Hubbell S P, Wright S J, Green J L. 2014. Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proceedings of the National Academy of Sciences of the United States of America, 111, 13715–13720.
Kim J Y, Whon T W, Lim M Y, Kim Y B, Kim N, Kwon M S, Kim J, Lee S H, Choi H J, Nam I H, Chung W H, Kim J H, Bae J W, Roh S W, Nam Y D. 2020. The human gut archaeome: Identification of diverse haloarchaea in Korean subjects. Microbiome, 8, 114.
Kim N, Zabaloy M C, Guan K, Villamil M B. 2020. Do cover crops benefit soil microbiome? A meta-analysis of current research. Soil Biology and Biochemistry, 142, 107701.
Knights D, Kuczynski J, Charlson E S, Zaneveld J, Mozer M C, Collman R G, Bushman F D, Knight R, Kelley S T. 2011. Bayesian community-wide culture-independent microbial source tracking. Nature Methods, 8, 761–765.
Leibold M A, Holyoak M, Mouquet N, Amarasekare P, Chase J M, Hoopes M F, Holt R D, Shurin J B, Law R, Tilman D, Loreau M, Gonzalez A. 2004. The metacommunity concept: A framework for multi-scale community ecology. Ecology Letters, 7, 601–613.
Levins R. 1968. Evolution in changing environments: Some theoretical explorations. Monographs in Population Biology.
Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F, Chaffron S, Ignacio-Espinosa J C, Roux S, Vincent F, Bittner L, Darzi Y, Wang J, Audic S, Berline L, Bontempi G, Cabello A M, Coppola L, Cornejo-Castillo F M, D’Ovidio F, et al. 2015. Determinants of community structure in the global plankton interactome. Science, 348, 874–875.
Liu L, Yang J, Yu Z, Wilkinson D M. 2015. The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. ISME Journal, 9, 2068–2077.
Liu X, Hannula S E, Li X, Hundscheid M P J,Gunnewiek P J A K, Clocchiatti A, Ding W, de Boer W. 2021. Decomposing cover crops modify root-associated microbiome composition and disease tolerance of cash crop seedlings. Soil Biology and Biochemistry, 160,108343.
Louca S, Parfrey L W, Doebeli M. 2016. Decoupling function and taxonomy in the global ocean microbiome. Science, 353, 1272–1277.
Lupwayi N Z, May W E, Kanashiro D A, Petri R M. 2018. Soil bacterial community responses to black medic cover crop and fertilizer N under no-till. Applied Soil Ecology, 124, 95–103.
Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider J H M, Piceno Y M, DeSantis T Z, Andersen G L, Bakker P A H M, Raaijmakers J M. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science, 332, 1097–1100.
Müller D B, Vogel C, Bai Y, Vorholt J A. 2016. The plant microbiota: Systems-level insights and perspectives. Annual Review of Genetics, 50, 211–234.
Nevins C J, Nakatsu C, Armstrong S. 2018. Characterization of microbial community response to cover crop residue decomposition. Soil Biology and Biochemistry, 127, 39–49.
Ning D, Deng Y, Tiedje J M, Zhou J. 2019. A general framework for quantitatively assessing ecological stochasticity. Proceedings of the National Academy of Sciences of the United States of America, 116, 16892–16898.
Pandit S N, Kolasa J, Cottenie K. 2009. Contrasts between habitat generalists and specialists: An empirical extension to the basic metacommunity framework. Ecology, 90, 2253–2262.
Perry L G, Weir T L, Prithiviraj B, Paschke M W, Vivanco J M. 2006. Root exudation and rhizosphere biology: multiple functions of a plant secondary metabolite. In: Baluska F, Mancuso S, Volkmann D, eds., Communication in Plants. Springer-Verlag, Berlin/Heidelberg. pp. 403–420.
Pielou C. 1966. The measurement of diversity in different types of biological collections. Journal of Theoretical Biology, 13, 131–144.
Pimm S L. 1984. The complexity and stability of ecosystems. Nature, 307, 321–326.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner F. 2013. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41, 590–596.
Rayment G E, Lyons D J. 2011. Soil Chemical Methods. CSIRO Publishing, Australasia.
Rudrappa T, Czymmek K J, Paré P W, Bais H P. 2008. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiology, 148, 1547–1556.
Sasse J, Martinoia E, Northen T. 2018. Feed your friends: Do plant exudates shape the root microbiome? Trends in Plant Science, 23, 25–41.
Schlaeppi K, Dombrowski N, Oter R G, ver Themaat E V L, Schulze-Lefert P. 2014. Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proceedings of the National Academy of Sciences of the United States of America, 111, 585–592.
Shannon C E. 1948. A mathematical theory of communication. The Bell System Technical Journal, 27, 379–423.
Sloan W T, Lunn M, Woodcock S, Head I M, Nee S, Curtis T P. 2006. Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environmental Microbiology, 8, 732–740.
Tkacz A, Bestion E, Bo Z, Hortala M, Poole P S. 2020. Influence of plant fraction, soil, and plant species on microbiota: A multikingdom comparison. MBIO, 11, e02785-19.
Tringe S G, von Mering C, Kobayashi A, Salamov A A, Chen K, Chang H W, Podar M, Short J M, Mathur E J, Detter J C, Bork P, Hugenholtz P, Rubin E M. 2005. Comparative metagenomics of microbial communities. Science, 308, 554–557.
Vandenkoornhuyse P, Quaiser A, Duhamel M, le Van A, Dufresne A. 2015. The importance of the microbiome of the plant holobiont. New Phytologist, 206, 1196–1206.
Vanwonterghem I, Jensen P D, Dennis P G, Hugenholtz P, Rabaey K, Tyson G W. 2014. Deterministic processes guide long-term synchronised population dynamics in replicate anaerobic digesters. ISME Journal, 8, 2015–2028.
Vilmi A, Gibert C, Escarguel G, Happonen K, Heino J, Jamoneau A, Passy S I, Picazo F, Soininen J, Tison-Rosebery J, Wang J. 2021. Dispersal-niche continuum index: A new quantitative metric for assessing the relative importance of dispersal versus niche processes in community assembly. Ecography, 44, 370–379.
Walters W A, Jin Z, Youngblut N, Wallace J G, Sutter J, Zhang W, González-Peña A, Peiffer J, Koren O, Shi Q, Knight R, del Rio T G, Tringe S G, Buckler E S, Dangl J L, Ley R E. 2018. Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proceedings of the National Academy of Sciences of the United States of America, 115, 7368–7373.
Wang L, Lin H, Dong Y, Li B, He Y. 2020. Effects of endophytes inoculation on rhizosphere and endosphere microecology of Indian mustard (Brassica juncea) grown in vanadium-contaminated soil and its enhancement on phytoremediation. Chemosphere, 240, 124891.
Wei G, Li M, Li F, Li H, Gao Z. 2016. Distinct distribution patterns of prokaryotes between sediment and water in the Yellow River estuary. Applied Microbiology and Biotechnology, 100, 9683–9697.
Wilson B, Haye L A C. 2015. Distinguishing relative specialist and generalist species in the fossil record. Marine Micropaleontology, 119, 7–16.
Wu W, Logares R, Huang B, Hsieh C H. 2017. Abundant and rare picoeukaryotic sub-communities present contrasting patterns in the epipelagic waters of marginal seas in the northwestern Pacific Ocean. Environmental Microbiology, 19, 287–300.
Xiong C, Zhu Y G, Wang J T, Singh B, Han L L, Shen J P, Li P P, Wang G B, Wu C F, Ge A H, Zhang L M, He J Z. 2021. Host selection shapes crop microbiome assembly and network complexity. New Phytologist, 229, 1091–1104.
Zhang J, Zhang B, Liu Y, Guo Y, Shi P, Wei G. 2018. Distinct large-scale biogeographic patterns of fungal communities in bulk soil and soybean rhizosphere in China. Science of the Total Environment, 644, 791–800.
Zhou G, Gao S, Lu Y, Liao Y, Nie J, Cao W. 2020a. Co-incorporation of green manure and rice straw improves rice production, soil chemical, biochemical and microbiological properties in a typical paddy field in southern China. Soil and Tillage Research, 197, 104499.
Zhou G, Gao S, Xu C, Dou F, Shimizu K Y, Cao W. 2020b. Rational utilization of leguminous green manure to mitigate methane emissions by influencing methanogenic and methanotrophic communities. Geoderma, 361, 114071.
|No Suggested Reading articles found!