Host-specific and tissue-dependent orchestration of microbiome community structure in traditional rice paddy ecosystems

Huang, Weijuan; Gilbert, Sarah; Poulev, Alexander; Acosta, Kenneth; Lebeis, Sarah; Long, Chunlin; Lam, Eric

doi:10.1007/s11104-020-04568-3

Host-specific and tissue-dependent orchestration of microbiome community structure in traditional rice paddy ecosystems

Journal Article · Tue Jun 02 04:00:00 EDT 2020 · Plant and Soil

DOI:https://doi.org/10.1007/s11104-020-04568-3· OSTI ID:1803329

Huang, Weijuan ^[1]; Gilbert, Sarah; Poulev, Alexander; Acosta, Kenneth; Lebeis, Sarah; Long, Chunlin;

OSTI

Abstract Background and aim

Rice and duckweed are two monocotyledonous plants that naturally coexist in paddy fields. While the presence of duckweed in paddy fields significantly improves rice productivity, the interplay between soil microbes and the two plant hosts in this agroecosystem remains unexplored.

Methods

We compared the bacterial community structure between duckweed, rice and soil from multiple rice paddies. We also isolated bacteria from these communities and characterized their modes of bacterial colonization and plant growth-promotion using model plants.

Results

Our data indicate that host-specific and tissue-dependent factors reproducibly orchestrate the bacterial community structure associated with their plant hosts. This is corroborated by results from culture-dependent approaches in which the dominant genusPantoeaisolated from rice aerial tissues can strongly attach and colonize gnotobiotic duckweed in spite of the low representation of this bacterial genus in the natural duckweed microbiome. Our study identified a core of 254 bacterial taxa that are consistently found in all rice and duckweed tissue samples from rice paddy fields. Furthermore, characterizing auxin-producing bacteria isolates from both plant species identified potential plant growth-promoting bacteria that may improve growth for both duckweed and rice in paddy fields.

Conclusions

Results from this work provide evidence for the importance of the host tissue and species context in determining plant colonization by microbes in the paddy field system. The resources generated in this study could facilitate the agronomic deployment of microbes for more sustainable rice production.

Research Organization:: Cold Spring Harbor Laboratory Cold Spring Harbor, NY (United States); Univ. of California, Oakland, CA (United States); Battelle Memorial Institute, Columbus, OH (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: SC0018244; AC02-05CH11231; AC05-76RL01830

OSTI ID:: 1803329

Journal Information:: Plant and Soil, Journal Name: Plant and Soil Journal Issue: 1-2 Vol. 452; ISSN 0032-079X

Publisher:: Springer

Country of Publication:: United States

Language:: English

References (42)

The plant microbiome explored: implications for experimental botany Berg, Gabriele; Rybakova, Daria; Grube, Martin Journal of Experimental Botany, Vol. 67, Issue 4 https://doi.org/10.1093/jxb/erv466	journal	November 2015
Surprisingly extensive mixed phylogenetic and ecological signals among bacterial Operational Taxonomic Units Koeppel, Alexander F.; Wu, Martin Nucleic Acids Research, Vol. 41, Issue 10 https://doi.org/10.1093/nar/gkt241	journal	April 2013
Functional overlap of the Arabidopsis leaf and root microbiota Bai, Yang; Müller, Daniel B.; Srinivas, Girish Nature, Vol. 528, Issue 7582 https://doi.org/10.1038/nature16192	journal	December 2015
Reduction of Ammonia Volatilization from Urea by a Floating Duckweed in Flooded Rice Fields Li, Hua; Liang, Xinqiang; Lian, Yanfeng Soil Science Society of America Journal, Vol. 73, Issue 6 https://doi.org/10.2136/sssaj2008.0230	journal	November 2009
Bacterial Production of Indole Related Compounds Reveals Their Role in Association Between Duckweeds and Endophytes Gilbert, Sarah; Xu, Jenny; Acosta, Kenneth Frontiers in Chemistry, Vol. 6 https://doi.org/10.3389/fchem.2018.00265	journal	July 2018
Tomato root microbiota and Phytophthora parasitica-associated disease Larousse, Marie; Rancurel, Corinne; Syska, Camille Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0273-7	journal	May 2017
AdapterRemoval: Easy Cleaning of Next Generation Sequencing Reads Lindgreen, Stinus BMC Research Notes, Vol. 5, Issue 1 https://doi.org/10.1186/1756-0500-5-337	journal	January 2012
Ensiling of cattle waste and wheat straw with or without green maize Kamra, D. N.; Jakhmola, R. C.; Singh, Rameshwar Agricultural Wastes, Vol. 9, Issue 4 https://doi.org/10.1016/0141-4607(84)90089-1	journal	January 1984
Modulation of the Root Microbiome by Plant Molecules: The Basis for Targeted Disease Suppression and Plant Growth Promotion Pascale, Alberto; Proietti, Silvia; Pantelides, Iakovos S. Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01741	journal	January 2020
Integrated reactive nitrogen budgets and future trends in China Gu, Baojing; Ju, Xiaotang; Chang, Jie Proceedings of the National Academy of Sciences, Vol. 112, Issue 28 https://doi.org/10.1073/pnas.1510211112	journal	June 2015
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Nutrient removal ability and economical benefit of a rice-fish co-culture system in aquaculture pond Feng, Jinfei; Li, Fengbo; Zhou, Xiyue Ecological Engineering, Vol. 94 https://doi.org/10.1016/j.ecoleng.2016.06.002	journal	September 2016
Assessment, validation and deployment strategy of a two-barcode protocol for facile genotyping of duckweed species Borisjuk, N.; Chu, P.; Gutierrez, R. Plant Biology, Vol. 17 https://doi.org/10.1111/plb.12229	journal	August 2014
A buried Neolithic paddy soil reveals loss of microbial functional diversity after modern rice cultivation Zhu, Yong-Guan; Su, Jian-Qiang; Cao, Zhihong Science Bulletin, Vol. 61, Issue 13 https://doi.org/10.1007/s11434-016-1112-0	journal	July 2016
Large-scale replicated field study of maize rhizosphere identifies heritable microbes Walters, William A.; Jin, Zhao; Youngblut, Nicholas Proceedings of the National Academy of Sciences, Vol. 115, Issue 28 https://doi.org/10.1073/pnas.1800918115	journal	June 2018
Duckweed ( Spirodela polyrhiza ) as green manure for increasing yield and reducing nitrogen loss in rice production Yao, Yuanlin; Zhang, Min; Tian, Yuhua Field Crops Research, Vol. 214 https://doi.org/10.1016/j.fcr.2017.09.021	journal	December 2017
Microbial small molecules – weapons of plant subversion Stringlis, Ioannis A.; Zhang, Hao; Pieterse, Corné M. J. Natural Product Reports, Vol. 35, Issue 5 https://doi.org/10.1039/C7NP00062F	journal	January 2018
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/aem.00062-07	journal	June 2007
The Split-Apply-Combine Strategy for Data Analysis Wickham, Hadley Journal of Statistical Software, Vol. 40, Issue 1 https://doi.org/10.18637/jss.v040.i01	journal	January 2011
Understanding and exploiting plant beneficial microbes Finkel, Omri M.; Castrillo, Gabriel; Herrera Paredes, Sur Current Opinion in Plant Biology, Vol. 38 https://doi.org/10.1016/j.pbi.2017.04.018	journal	August 2017
Farmland biodiversity: is habitat heterogeneity the key? Benton, Tim G.; Vickery, Juliet A.; Wilson, Jeremy D. Trends in Ecology & Evolution, Vol. 18, Issue 4 https://doi.org/10.1016/s0169-5347(03)00011-9	journal	April 2003
Regulating the reapers: activating metacaspases for programmed cell death Lam, Eric; Zhang, Yi Trends in Plant Science, Vol. 17, Issue 8 https://doi.org/10.1016/j.tplants.2012.05.003	journal	August 2012
Populations, Community Composition and Biomass of Aquatic Organisms in the Floodwater of Rice Fields and Effects of Field Management Kimura, Makoto Soil Science and Plant Nutrition, Vol. 51, Issue 2 https://doi.org/10.1111/j.1747-0765.2005.tb00021.x	journal	April 2005
Quality control and preprocessing of metagenomic datasets Schmieder, R.; Edwards, R. Bioinformatics, Vol. 27, Issue 6 https://doi.org/10.1093/bioinformatics/btr026	journal	January 2011
Drought Stress Results in a Compartment-Specific Restructuring of the Rice Root-Associated Microbiomes Santos-Medellín, Christian; Edwards, Joseph; Liechty, Zachary mBio, Vol. 8, Issue 4 https://doi.org/10.1128/mBio.00764-17	journal	July 2017
Structure, variation, and assembly of the root-associated microbiomes of rice Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1414592112	journal	January 2015
New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region Gurtler, V.; Stanisich, V. A. Microbiology, Vol. 142, Issue 1 https://doi.org/10.1099/13500872-142-1-3	journal	January 1996
Variations in nutrient and trace element composition of rice in an organic rice-frog coculture system Sha, Zhimin; Chu, Qingnan; Zhao, Zheng Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-15658-1	journal	November 2017
Colorimetric Estimation of Indoleacetic acid Gordon, Solon A.; Weber, Robert P. Plant Physiology, Vol. 26, Issue 1 https://doi.org/10.1104/pp.26.1.192	journal	January 1951
The effect of floating vegetation on CH4 and N2O emissions from subtropical paddy fields in China Wang, Chun; Li, Shouchun; Lai, Derrick Y. F. Paddy and Water Environment, Vol. 13, Issue 4 https://doi.org/10.1007/s10333-014-0459-6	journal	August 2014
Rice, fish, and the planet Lansing, J. S.; Kremer, J. N. Proceedings of the National Academy of Sciences, Vol. 108, Issue 50 https://doi.org/10.1073/pnas.1117707109	journal	November 2011
Performance of duckweed and effective microbes in reducing arsenic in paddy and paddy soil Ng, C. A.; Wong, L. Y.; Lo, P. K. GREEN AND SUSTAINABLE TECHNOLOGY: 2nd International Symposium (ISGST2017), AIP Conference Proceedings https://doi.org/10.1063/1.4979402	conference	January 2017
Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis: Tissue-specific Aux/IAA signaling in lateral root development Fukaki, Hidehiro; Nakao, Yoko; Okushima, Yoko The Plant Journal, Vol. 44, Issue 3 https://doi.org/10.1111/j.1365-313x.2005.02537.x	journal	October 2005
Microbial interactions within the plant holobiont Hassani, M. Amine; Durán, Paloma; Hacquard, Stéphane Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0445-0	journal	March 2018
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life Parks, Donovan H.; Chuvochina, Maria; Waite, David W. Nature Biotechnology, Vol. 36, Issue 10 https://doi.org/10.1038/nbt.4229	journal	August 2018
Defining the core Arabidopsis thaliana root microbiome Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11237	journal	August 2012
Rice-soft shell turtle coculture effects on yield and its environment Zhang, Jian; Hu, Liangliang; Ren, Weizheng Agriculture, Ecosystems & Environment, Vol. 224 https://doi.org/10.1016/j.agee.2016.03.045	journal	May 2016
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB DeSantis, T. Z.; Hugenholtz, P.; Larsen, N. Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072 https://doi.org/10.1128/AEM.03006-05	journal	July 2006
Rice-duck co-culture for reducing negative impacts of biogas slurry application in rice production systems Yang, Haishui; Yu, Degui; Zhou, Jiajia Journal of Environmental Management, Vol. 213 https://doi.org/10.1016/j.jenvman.2018.02.077	journal	May 2018
An Ordination of the Upland Forest Communities of Southern Wisconsin Bray, J. Roger; Curtis, J. T. Ecological Monographs, Vol. 27, Issue 4 https://doi.org/10.2307/1942268	journal	February 1957
Duckweed hosts a taxonomically similar bacterial assemblage as the terrestrial leaf microbiome Acosta, Kenneth; Xu, Jenny; Gilbert, Sarah PLOS ONE, Vol. 15, Issue 2 https://doi.org/10.1371/journal.pone.0228560	journal	February 2020
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory Nature Biotechnology, Vol. 31, Issue 9 https://doi.org/10.1038/nbt.2676	journal	August 2013

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