The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages

Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J.; He, Zhili; Zhou, Jizhong; Firestone, Mary K.

doi:10.1111/ele.12630

Title: The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages

Journal Article · Mon Jun 06 00:00:00 EDT 2016 · Ecology Letters

DOI:https://doi.org/10.1111/ele.12630· OSTI ID:1467800

Shi, Shengjing ^[1];

^[2]; Shi, Zhou J. ^[3]; He, Zhili ^[3]; Zhou, Jizhong ^[4]; Firestone, Mary K. ^[5]

Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy and Management; Univ. of Oklahoma, Norman, OK (United States). Dept. of Botony and Microbiology and Inst. of Environmental Genomics
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Nuclear and Chemical Sciences Division; Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy and Management
Univ. of Oklahoma, Norman, OK (United States). Dept. of Botony and Microbiology and Inst. of Environmental Genomics
Univ. of Oklahoma, Norman, OK (United States). Dept. of Botony and Microbiology and Inst. of Environmental Genomics; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division; Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control and School of Environment
Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy and Management; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division

While interactions between roots and microorganisms have been intensively studied, we know little about interactions among root-associated microbes. We used random matrix theory-based network analysis of 16S rRNA genes to identify bacterial networks associated with wild oat (Avena fatua) over two seasons in greenhouse microcosms. Rhizosphere networks were substantially more complex than those in surrounding soils, indicating the rhizosphere has a greater potential for interactions and niche-sharing. Network complexity increased as plants grew, even as diversity decreased, highlighting that community organisation is not captured by univariate diversity. Covariations were predominantly positive (> 80%), suggesting that extensive mutualistic interactions may occur among rhizosphere bacteria; we identified quorum-based signalling as one potential strategy. Putative keystone taxa often had low relative abundances, suggesting low-abundance taxa may significantly contribute to rhizosphere function. Network complexity, a previously undescribed property of the rhizosphere microbiome, appears to be a defining characteristic of this habitat.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC52-07NA27344; AC02-05CH11231; SC0004730; SC0010570; SCW1421; 00008322

OSTI ID:: 1467800

Alternate ID(s):: OSTI ID: 1401210; OSTI ID: 1474903

Report Number(s):: LLNL-JRNL-679806; 803848

Journal Information:: Ecology Letters, Vol. 19, Issue 8; ISSN 1461-023X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 624 works

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Bacterial Succession Decreases Network Complexity During Plant Material Decomposition in Mangroves Moitinho, Marta A.; Bononi, Laura; Souza, Danilo T. Microbial Ecology, Vol. 76, Issue 4 https://doi.org/10.1007/s00248-018-1190-4	journal	April 2018
Mangrove Sediment Microbiome: Adaptive Microbial Assemblages and Their Routed Biogeochemical Processes in Yunxiao Mangrove National Nature Reserve, China Lin, Xiaolan; Hetharua, Buce; Lin, Lian Microbial Ecology, Vol. 78, Issue 1 https://doi.org/10.1007/s00248-018-1261-6	journal	October 2018
Alterations in soil fungal community composition and network assemblage structure by different long-term fertilization regimes are correlated to the soil ionome Xue, Chao; Ryan Penton, C.; Zhu, Chen Biology and Fertility of Soils, Vol. 54, Issue 1 https://doi.org/10.1007/s00374-017-1241-x	journal	September 2017
Unique bacterial assembly, composition, and interactions in a parasitic plant and its host Fitzpatrick, Connor R.; Schneider, Adam C. Journal of Experimental Botany, Vol. 71, Issue 6 https://doi.org/10.1093/jxb/erz572	journal	January 2020
Microbial Network and Soil Properties Are Changed in Bacterial Wilt-Susceptible Soil Qi, Gaofu; Ma, Gaoqiang; Chen, Shu Applied and Environmental Microbiology, Vol. 85, Issue 13 https://doi.org/10.1128/aem.00162-19	journal	April 2019
Rhizosphere protists are key determinants of plant health Xiong, Wu; Song, Yuqi; Yang, Keming Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00799-9	journal	March 2020
Microbiome Selection Could Spur Next-Generation Plant Breeding Strategies Gopal, Murali; Gupta, Alka Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01971	journal	December 2016
Diversity and Co-occurrence Patterns of Soil Bacterial and Fungal Communities in Seven Intercropping Systems Li, Sen; Wu, Fengzhi Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01521	journal	July 2018
A New Method to Correct for Habitat Filtering in Microbial Correlation Networks Brisson, Vanessa; Schmidt, Jennifer; Northen, Trent R. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00585	journal	March 2019
Ecological networks reveal contrasting patterns of bacterial and fungal communities in glacier-fed streams in Central Asia Ren, Ze; Gao, Hongkai PeerJ Preprints https://doi.org/10.7287/peerj.preprints.27887	posted_content	August 2019
Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning Wagg, Cameron; Schlaeppi, Klaus; Banerjee, Samiran Nature Publishing Group https://doi.org/10.7892/boris.134558	text	January 2019
Linking microbial co-occurrences to soil ecological processes across a woodland-grassland ecotone Banerjee, Samiran; Thrall, Peter H.; Bissett, Andrew Wiley Open Access https://doi.org/10.5167/uzh-168387	text	January 2018
Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning Wagg, Cameron; Schlaeppi, Klaus; Banerjee, Samiran Nature Publishing Group https://doi.org/10.5167/uzh-182853	text	January 2019
Ecological networks reveal contrasting patterns of bacterial and fungal communities in glacier-fed streams in Central Asia Ren, Ze; Gao, Hongkai PeerJ Preprints https://doi.org/10.7287/peerj.preprints.27887v1	posted_content	August 2019
Keystone taxa as drivers of microbiome structure and functioning Banerjee, Samiran; Schlaeppi, Klaus; Van Der Heijden, Marcel G. A. Springer Nature https://doi.org/10.7892/boris.117151	text	January 2018
The xylella fastidiosa-resistant olive cultivar “leccino” has stable endophytic microbiota during the olive quick decline syndrome (OQDS) Vergine, Marzia; Meyer, Joana B.; Cardinale, Massimiliano ETH Zurich https://doi.org/10.3929/ethz-b-000395840	text	January 2020
Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots Banerjee, Samiran; Walder, Florian; Büchi, Lucie Nature Publishing Group https://doi.org/10.5167/uzh-182854	text	January 2019
Ecological networks reveal contrasting patterns of bacterial and fungal communities in glacier-fed streams in Central Asia Ren, Ze; Gao, Hongkai PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7715	journal	January 2019
Ecological diversity and co-occurrence patterns of bacterial community through soil profile in response to long-term switchgrass cultivation He, Shubin; Guo, Lixiang; Niu, Mengying Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-03778-7	journal	June 2017
Mainland and island populations of Mussaenda kwangtungensis differ in their phyllosphere fungal community composition and network structure Qian, Xin; Li, Shengchun; Wu, Binwei Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-57622-6	journal	January 2020
Seasonal Changes in a Maize-Based Polyculture of Central Mexico Reshape the Co-occurrence Networks of Soil Bacterial Communities Rebollar, Eria A.; Sandoval-Castellanos, Edson; Roessler, Kyria Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02478	journal	December 2017
Traits-Based Integration of Multi-Species Inoculants Facilitates Shifts of Indigenous Soil Bacterial Community Wang, Jingjing; Li, Qingqing; Xu, Song Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01692	journal	July 2018
Succession of Composition and Function of Soil Bacterial Communities During Key Rice Growth Stages Wang, Wenhui; Luo, Xue; Chen, Yang Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00421	journal	March 2019
Leaf and Root Endospheres Harbor Lower Fungal Diversity and Less Complex Fungal Co-occurrence Patterns Than Rhizosphere Qian, Xin; Li, Hanzhou; Wang, Yonglong Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01015	journal	May 2019
Soil Bacterial and Fungal Communities Exhibit Distinct Long-Term Responses to Disturbance in Temperate Forests Osburn, Ernest D.; McBride, Steven G.; Aylward, Frank O. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02872	journal	December 2019
Featured Gut Microbiomes Associated With the Progression of Chronic Hepatitis B Disease Chen, Zhangran; Xie, Yurou; Zhou, Fei Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00383	journal	March 2020
Diazotroph Diversity and Nitrogen Fixation in Summer Active Perennial Grasses in a Mediterranean Region Agricultural Soil Gupta, Vadakattu V. S. R.; Zhang, Bangzhou; Penton, Christopher Ryan Frontiers in Molecular Biosciences, Vol. 6 https://doi.org/10.3389/fmolb.2019.00115	journal	November 2019

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