Conservation of beneficial microbes between the rhizosphere and the cyanosphere

Zheng, Qing; Hu, Yuntao; Kosina, Suzanne M.; Van Goethem, Marc W.; Tringe, Susannah G.; Bowen, Benjamin P.; Northen, Trent R.

doi:10.1111/nph.19225

Title: Conservation of beneficial microbes between the rhizosphere and the cyanosphere

Journal Article · 04 September 2023 · New Phytologist

DOI: https://doi.org/10.1111/nph.19225 · OSTI ID:1998204

^[1];

^[2];

^[2]

Environmental Genomics and Systems Biology Division Lawrence Berkeley National Laboratory Berkeley CA 94720 USA
Environmental Genomics and Systems Biology Division Lawrence Berkeley National Laboratory Berkeley CA 94720 USA, Joint Genome Institute Berkeley CA 94720 USA

Summary Biocrusts are phototroph‐driven communities inhabiting arid soil surfaces. Like plants, most photoautotrophs (largely cyanobacteria) in biocrusts are thought to exchange fixed carbon for essential nutrients like nitrogen with cyanosphere bacteria. Here, we aim to compare beneficial interactions in rhizosphere and cyanosphere environments, including finding growth‐promoting strains for hosts from both environments. To examine this, we performed a retrospective analysis of 16S rRNA gene sequencing datasets, host–microbe co‐culture experiments between biocrust communities/biocrust isolates and a model grass ( Brachypodium distachyon ) or a dominant biocrust cyanobacterium ( Microcoleus vaginatus ), and metabolomic analysis. All 18 microbial phyla in the cyanosphere were also present in the rhizosphere, with additional 17 phyla uniquely found in the rhizosphere. The biocrust microbes promoted the growth of the model grass, and three biocrust isolates ( Bosea sp._L1B56, Pseudarthrobacter sp. _ L1D14 and Pseudarthrobacter picheli_ L1D33) significantly promoted the growth of both hosts. Moreover, pantothenic acid was produced by Pseudarthrobacter sp._L1D14 when grown on B . distachyon exudates, and supplementation of plant growth medium with this metabolite increased B . distachyon biomass by over 60%. These findings suggest that cyanobacteria and other diverse photoautotrophic hosts can be a source for new plant growth‐promoting microbes and metabolites.

View Journal Article

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Montana State University, Bozeman, MT (United States)

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

Grant/Contract Number:: AC02-05CH11231; SC0021369

OSTI ID:: 1998204

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 3 Vol. 240; ISSN 0028-646X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (64)

Biocrusts positively affect the soil water balance in semiarid ecosystems: The Role of Biocrusts in the Local Water Balance Chamizo, Sonia; Cantón, Yolanda; Rodríguez-Caballero, Emilio Ecohydrology, Vol. 9, Issue 7 https://doi.org/10.1002/eco.1719	journal	January 2016
The potential roles of biological soil crusts in dryland hydrologic cycles Belnap, Jayne Hydrological Processes, Vol. 20, Issue 15 https://doi.org/10.1002/hyp.6325	journal	January 2006
Biological Soil Crusts as an Organizing Principle in Drylands Belnap, Jayne; Weber, Bettina; Büdel, Burkhard Biological Soil Crusts: An Organizing Principle in Drylands https://doi.org/10.1007/978-3-319-30214-0_1	book	January 2016
High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3 Vogel, John; Hill, Theresa Plant Cell Reports, Vol. 27, Issue 3 https://doi.org/10.1007/s00299-007-0472-y	journal	November 2007
Production of B-group vitamins by plant growth-promoting Pseudomonas fluorescens strain 267 and the importance of vitamins in the colonization and nodulation of red clover Marek-Kozaczuk, Monika; Skorupska, A. Biology and Fertility of Soils, Vol. 33, Issue 2 https://doi.org/10.1007/s003740000304	journal	February 2001
Nitrogen cycling in desert biological soil crusts across biogeographic regions in the Southwestern United States Strauss, Sarah L.; Day, Thomas A.; Garcia-Pichel, Ferran Biogeochemistry, Vol. 108, Issue 1-3 https://doi.org/10.1007/s10533-011-9587-x	journal	March 2011
The concurrent use of novel soil surface microclimate measurements to evaluate CO2 pulses in biocrusted interspaces in a cool desert ecosystem Tucker, Colin L.; McHugh, Theresa A.; Howell, Armin Biogeochemistry, Vol. 135, Issue 3 https://doi.org/10.1007/s10533-017-0372-3	journal	September 2017
Plant species-specificity and effects of bioinoculants and fertilization on plant performance for nickel phytomining Ghasemi, Zahra; Ghaderian, Seyed Majid; Rodríguez-Garrido, Beatriz Plant and Soil, Vol. 425, Issue 1-2 https://doi.org/10.1007/s11104-017-3553-x	journal	February 2018
Consistent Sets of Spectrophotometric Chlorophyll Equations for Acetone, Methanol and Ethanol Solvents Ritchie, Raymond J. Photosynthesis Research, Vol. 89, Issue 1 https://doi.org/10.1007/s11120-006-9065-9	journal	June 2006
Optimization of Fermentation Medium for Indole Acetic Acid Production by Pseudarthrobacter sp. NIBRBAC000502770 Ham, Seunghee; Yoon, Hyeokjun; Park, Jeong-Mi Applied Biochemistry and Biotechnology, Vol. 193, Issue 8 https://doi.org/10.1007/s12010-021-03558-0	journal	March 2021
Microbiota and Host Nutrition across Plant and Animal Kingdoms Hacquard, Stéphane; Garrido-Oter, Ruben; González, Antonio Cell Host & Microbe, Vol. 17, Issue 5 https://doi.org/10.1016/j.chom.2015.04.009	journal	May 2015
Dealing with the unknown: Metabolomics and Metabolite Atlases Bowen, Benjamin P.; Northen, Trent R. Journal of the American Society for Mass Spectrometry, Vol. 21, Issue 9 https://doi.org/10.1016/j.jasms.2010.04.003	journal	September 2010
Soil inoculation method determines the strength of plant–soil interactions van de Voorde, Tess F. J.; van der Putten, Wim H.; Bezemer, T. Martijn Soil Biology and Biochemistry, Vol. 55 https://doi.org/10.1016/j.soilbio.2012.05.020	journal	December 2012
Biological soil crusts greatly contribute to small-scale soil heterogeneity along a grazing gradient Concostrina-Zubiri, L.; Huber-Sannwald, E.; Martínez, I. Soil Biology and Biochemistry, Vol. 64 https://doi.org/10.1016/j.soilbio.2013.03.029	journal	September 2013
Growth explains microbial carbon use efficiency across soils differing in land use and geology Zheng, Qing; Hu, Yuntao; Zhang, Shasha Soil Biology and Biochemistry, Vol. 128 https://doi.org/10.1016/j.soilbio.2018.10.006	journal	January 2019
Let the Core Microbiota Be Functional Lemanceau, Philippe; Blouin, Manuel; Muller, Daniel Trends in Plant Science, Vol. 22, Issue 7 https://doi.org/10.1016/j.tplants.2017.04.008	journal	July 2017
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome? Sasse, Joelle; Martinoia, Enrico; Northen, Trent Trends in Plant Science, Vol. 23, Issue 1 https://doi.org/10.1016/j.tplants.2017.09.003	journal	January 2018
“Pantothenic Acid,” A Growth Determinant of Universal Biological Occurrence Williams, Roger J.; Lyman, Carl M.; Goodyear, George H. Journal of the American Chemical Society, Vol. 55, Issue 7 https://doi.org/10.1021/ja01334a049	journal	July 1933
Physiological variation among native and exotic winter annual plants associated with microbiotic crusts in the Mojave Desert DeFalco, Lesley A.; Detling, James K.; Tracy, C. Richard Plant and Soil, Vol. 234, Issue 1, p. 1-14 https://doi.org/10.1023/A:1010323001006	journal	July 2001
Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots Bressan, Mélanie; Roncato, Marie-Anne; Bellvert, Floriant The ISME Journal, Vol. 3, Issue 11 https://doi.org/10.1038/ismej.2009.68	journal	June 2009
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Drought and host selection influence bacterial community dynamics in the grass root microbiome Naylor, Dan; DeGraaf, Stephanie; Purdom, Elizabeth The ISME Journal, Vol. 11, Issue 12 https://doi.org/10.1038/ismej.2017.118	journal	July 2017
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
Exometabolite niche partitioning among sympatric soil bacteria Baran, Richard; Brodie, Eoin L.; Mayberry-Lewis, Jazmine Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9289	journal	September 2015
Contribution of cryptogamic covers to the global cycles of carbon and nitrogen Elbert, Wolfgang; Weber, Bettina; Burrows, Susannah Nature Geoscience, Vol. 5, Issue 7 https://doi.org/10.1038/ngeo1486	journal	June 2012
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
A symbiotic nutrient exchange within the cyanosphere microbiome of the biocrust cyanobacterium, Microcoleus vaginatus Nelson, Corey; Giraldo-Silva, Ana; Garcia-Pichel, Ferran The ISME Journal, Vol. 15, Issue 1 https://doi.org/10.1038/s41396-020-00781-1	journal	September 2020
Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence Yeoh, Yun Kit; Dennis, Paul G.; Paungfoo-Lonhienne, Chanyarat Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00262-8	journal	August 2017
Linking soil biology and chemistry in biological soil crust using isolate exometabolomics Swenson, Tami L.; Karaoz, Ulas; Swenson, Joel M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02356-9	journal	January 2018
Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota Hu, Lingfei; Robert, Christelle A. M.; Cadot, Selma Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05122-7	journal	July 2018
The structure and function of the global citrus rhizosphere microbiome Xu, Jin; Zhang, Yunzeng; Zhang, Pengfan Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07343-2	journal	November 2018
Shared features and reciprocal complementation of the Chlamydomonas and Arabidopsis microbiota Durán, Paloma; Flores-Uribe, José; Wippel, Kathrin Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28055-8	journal	January 2022
Rhizosphere bacteriome structure and functions Ling, Ning; Wang, Tingting; Kuzyakov, Yakov Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28448-9	journal	February 2022
Dryland photoautotrophic soil surface communities endangered by global change Rodriguez-Caballero, Emilio; Belnap, Jayne; Büdel, Burkhard Nature Geoscience, Vol. 11, Issue 3 https://doi.org/10.1038/s41561-018-0072-1	journal	February 2018
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao Nature Microbiology, Vol. 3, Issue 4 https://doi.org/10.1038/s41564-018-0129-3	journal	March 2018
Genomic insights that advance the species definition for prokaryotes Konstantinidis, K. T.; Tiedje, J. M. Proceedings of the National Academy of Sciences, Vol. 102, Issue 7 https://doi.org/10.1073/pnas.0409727102	journal	February 2005
Assembly and ecological function of the root microbiome across angiosperm plant species Fitzpatrick, Connor R.; Copeland, Julia; Wang, Pauline W. Proceedings of the National Academy of Sciences, Vol. 115, Issue 6 https://doi.org/10.1073/pnas.1717617115	journal	January 2018
Ecological drivers of bacterial community assembly in synthetic phycospheres Fu, He; Uchimiya, Mario; Gore, Jeff Proceedings of the National Academy of Sciences, Vol. 117, Issue 7 https://doi.org/10.1073/pnas.1917265117	journal	February 2020
Panothenic Acid and the Nodule Bacteria-Legume Symbiosis McBurney, Charles H.; Bollen, Walter B.; Williams, Roger J. Proceedings of the National Academy of Sciences, Vol. 21, Issue 6 https://doi.org/10.1073/pnas.21.6.301	journal	June 1935
Multilocus sequence analysis of Bosea species and description of Bosea lupini sp. nov., Bosea lathyri sp. nov. and Bosea robiniae sp. nov., isolated from legumes De Meyer, Sofie E.; Willems, Anne International Journal of Systematic and Evolutionary Microbiology, Vol. 62, Issue 10 https://doi.org/10.1099/ijs.0.035477-0	journal	October 2012
Pantothenic acid as a Nutrilite for Green Plants Williams, Roger J.; Rohrman, Ewald Plant Physiology, Vol. 10, Issue 3 https://doi.org/10.1104/pp.10.3.559	journal	July 1935
Root Exudation and Rhizosphere Biology: Fig. 1. Walker, Travis S.; Bais, Harsh Pal; Grotewold, Erich Plant Physiology, Vol. 132, Issue 1 https://doi.org/10.1104/pp.102.019661	journal	May 2003
Mutually Exclusive Alterations in Secondary Metabolism Are Critical for the Uptake of Insoluble Iron Compounds by Arabidopsis and Medicago truncatula Rodriguez-Celma, J.; Lin, W. -D.; Fu, G. -M. PLANT PHYSIOLOGY, Vol. 162, Issue 3 https://doi.org/10.1104/pp.113.220426	journal	June 2013
Towards a predictive framework for biocrust mediation of plant performance: A meta‐analysis Havrilla, Caroline A.; Chaudhary, V. Bala; Ferrenberg, Scott Journal of Ecology, Vol. 107, Issue 6 https://doi.org/10.1111/1365-2745.13269	journal	May 2019
Evolution of bacterial communities in the wheat crop rhizosphere: Rhizosphere bacteria in field-grown intensive wheat crops Donn, Suzanne; Kirkegaard, John A.; Perera, Geetha Environmental Microbiology, Vol. 17, Issue 3 https://doi.org/10.1111/1462-2920.12452	journal	May 2014
Field study reveals core plant microbiota and relative importance of their drivers: Core microbiota of field-grown sugarcane and their drivers Hamonts, Kelly; Trivedi, Pankaj; Garg, Anshu Environmental Microbiology, Vol. 20, Issue 1 https://doi.org/10.1111/1462-2920.14031	journal	January 2018
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing Benjamini, Yoav; Hochberg, Yosef Journal of the Royal Statistical Society: Series B (Methodological), Vol. 57, Issue 1 https://doi.org/10.1111/j.2517-6161.1995.tb02031.x	journal	January 1995
Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species Coleman-Derr, Devin; Desgarennes, Damaris; Fonseca-Garcia, Citlali New Phytologist, Vol. 209, Issue 2 https://doi.org/10.1111/nph.13697	journal	October 2015
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
Beneficial Cyanosphere Heterotrophs Accelerate Establishment of Cyanobacterial Biocrust Nelson, Corey; Garcia-Pichel, Ferran Applied and Environmental Microbiology, Vol. 87, Issue 20 https://doi.org/10.1128/AEM.01236-21	journal	September 2021
The enhancement of plant growth by free-living bacteria Glick, Bernard R. Canadian Journal of Microbiology, Vol. 41, Issue 2 https://doi.org/10.1139/m95-015	journal	February 1995
Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere Couradeau, Estelle; Giraldo-Silva, Ana; De Martini, Francesca Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0661-2	journal	April 2019
Maize synthesized benzoxazinoids affect the host associated microbiome Kudjordjie, Enoch Narh; Sapkota, Rumakanta; Steffensen, Stine K. Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0677-7	journal	April 2019
The Evolution of a Capacity to Build Supra-Cellular Ropes Enabled Filamentous Cyanobacteria to Colonize Highly Erodible Substrates Garcia-Pichel, Ferran; Wojciechowski, Martin F. PLoS ONE, Vol. 4, Issue 11 https://doi.org/10.1371/journal.pone.0007801	journal	November 2009
p-Coumaric Acid Influenced Cucumber Rhizosphere Soil Microbial Communities and the Growth of Fusarium oxysporum f.sp. cucumerinum Owen Zhou, Xingang; Wu, Fengzhi PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0048288	journal	October 2012
Microbiome and Exudates of the Root and Rhizosphere of Brachypodium distachyon, a Model for Wheat Kawasaki, Akitomo; Donn, Suzanne; Ryan, Peter R. PLOS ONE, Vol. 11, Issue 10 https://doi.org/10.1371/journal.pone.0164533	journal	October 2016
Plant growth-promoting bacteria as inoculants in agricultural soils Souza, Rocheli de; Ambrosini, Adriana; Passaglia, Luciane M. P. Genetics and Molecular Biology, Vol. 38, Issue 4 https://doi.org/10.1590/S1415-475738420150053	journal	November 2015
Effects of Cryptogamic Soil Crust on the Population Dynamics of Arabis fecunda (Brassicaceae) Lesica, Peter; Shelly, J. Stephen American Midland Naturalist, Vol. 128, Issue 1 https://doi.org/10.2307/2426412	journal	July 1992
The Exometabolome of Two Model Strains of the Roseobacter Group: A Marketplace of Microbial Metabolites Wienhausen, Gerrit; Noriega-Ortega, Beatriz E.; Niggemann, Jutta Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01985	journal	October 2017
Putative Nitrogen-Fixing Bacteria Associated With the Rhizosphere and Root Endosphere of Wheat Plants Grown in an Andisol From Southern Chile Rilling, Joaquin I.; Acuña, Jacquelinne J.; Sadowsky, Michael J. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02710	journal	November 2018
Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases Yao, Yushu; Sun, Terence; Wang, Tony Metabolites, Vol. 5, Issue 3 https://doi.org/10.3390/metabo5030431	journal	July 2015
Different Secondary Metabolite Profiles of Phylogenetically almost Identical Streptomyces griseus Strains Originating from Geographically Remote Locations Sottorff, Ignacio; Wiese, Jutta; Lipfert, Matthias Microorganisms, Vol. 7, Issue 6 https://doi.org/10.3390/microorganisms7060166	journal	June 2019
Effects of biological soil crusts on seedling growth and element uptake in five desert plants in Junggar Basin, western China Zhang, Yuan-Ming; Nie, Hua-Li Chinese Journal of Plant Ecology, Vol. 35, Issue 4 https://doi.org/10.3724/SP.J.1258.2011.00380	journal	November 2011
The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria Abdel-Lateif, Khalid; Bogusz, Didier; Hocher, Valérie Plant Signaling & Behavior, Vol. 7, Issue 6 https://doi.org/10.4161/psb.20039	journal	June 2012

Similar Records

Assessing horizontal gene transfer in the rhizosphere of Brachypodium distachyon using fabricated ecosystems (EcoFABs)

Journal Article · 2024 · Applied and Environmental Microbiology · OSTI ID:2475875

Priya, Shweta; Rossbach, Silvia; Eng, Thomas; +6 more

Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin

Journal Article · 2019 · Microbiome · OSTI ID:1618948

Veach, Allison M.; Morris, Reese; Yip, Daniel Z.; +5 more

Altering the substitution and cross‐linking of glucuronoarabinoxylans affects cell wall architecture in Brachypodium distachyon

Journal Article · 2024 · New Phytologist · OSTI ID:2325390

Tryfona, Theodora; Pankratova, Yanina; Petrik, Deborah; +9 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Brachypodium distachyon
Microcoleus vaginatus
biocrusts
cyanosphere
exometabolomics
microbiome recruitment
plant growth-promoting bacteria (PGPB)
rhizosphere

Title: Conservation of beneficial microbes between the rhizosphere and the cyanosphere

Citation Formats

References (64)

Similar Records

Related Subjects