Abstract
There is increased interest by the agricultural industry in microbial amendments that leverage natural beneficial interactions between plants and soil microbes to improve crop production. However, translating fundamental knowledge from laboratory experiments into efficient field application often has mixed results, and there is less clarity about the interaction between added microbes and the native microbial community, where microorganisms belonging to the same phylogenic clades often reside. In this study, four commercially available microbial amendments were examined in two greenhouse experiments using field soil to assess their impact on tomato plant growth and the native soil microbial communities. The amendments contained different formulations of plant growth-promoting bacteria (Lactobacilli, Rhizobia, etc.), yeasts, and mycorrhizal fungi. The application of the tested amendments in greenhouse conditions resulted in no significant impact on plant growth. A deeper statistical analysis detected variations in the microbial communities that accounted only for 0.25% of the total species, particularly in native taxa not related to the inoculated species and represented less than 1% of the total variance. This suggests that under commercial field conditions, additional confounding variables may play a role in the efficacy of soil microbial amendments. This study confirms the necessity of more in-depth validation requirements for the formulations of soil microbial amendments before delivery to the agricultural market in order to leverage their benefits for the producers, the consumers, and the environment.
Similar content being viewed by others
References
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci. 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Schlaeppi K, Bulgarelli D (2015) The plant microbiome at work. Mol. Plant-Microbe Interact. 28:212–217. https://doi.org/10.1094/MPMI-10-14-0334-FI
Bulgarelli D, Schlaeppi K, Spaepen S et al (2013) Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64:807–838. https://doi.org/10.1146/annurev-arplant-050312-120106
Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63:541–556. https://doi.org/10.1146/annurev.micro.62.081307.162918
Backer R, Rokem JS, Ilangumaran G et al (2018) Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front. Plant Sci. 9:1–17. https://doi.org/10.3389/fpls.2018.01473
Hacquard S, Garrido-Oter R, González A et al (2015) Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 17:603–616. https://doi.org/10.1016/j.chom.2015.04.009
Schulz-Bohm K, Zweers H, de Boer W, Garbeva P (2015) A fragrant neighborhood: volatile mediated bacterial interactions in soil. Front. Microbiol. 6:1–11. https://doi.org/10.3389/fmicb.2015.01212
Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol. Fertil. Soils 48:489–499. https://doi.org/10.1007/s00374-012-0691-4
Ersek B, Lange S.: Organic soil amendments and method for enhancing plant health. US Patent 8790436B2, July 2014
Pardey PG, Beddow JM, Hurley TM et al (2014) A bounds analysis of world food futures: global agriculture through to 2050. Aust. J. Agric. Resour. Econ. 58:571–589. https://doi.org/10.1111/1467-8489.12072
Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41. https://doi.org/10.1007/s11104-014-2131-8
Parnell JJ, Berka R, Young HA et al (2016) From the lab to the farm: an industrial perspective of plant beneficial microorganisms. Front. Plant Sci. 7:1401–1409. https://doi.org/10.3389/fpls.2016.01110
Sessitsch A, Brader G, Pfaffenbichler N et al (2018) The contribution of plant microbiota to economy growth. Microb. Biotechnol. https://doi.org/10.1111/1751-7915.13290
Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free-living bacterial inocula for enhancing crop productivity. Trends Biotechnol. 7:39–44. https://doi.org/10.1016/0167-7799(89)90057-7
Lamont JR, Wilkins O, Bywater-Ekegärd M, Smith DL (2017) From yogurt to yield: potential applications of lactic acid bacteria in plant production. Soil Biol. Biochem. 111:1–9. https://doi.org/10.1016/j.soilbio.2017.03.015
Giassi V, Kiritani C, Kupper KC (2016) Bacteria as growth-promoting agents for citrus rootstocks. Microbiol. Res. 190:46–54. https://doi.org/10.1016/j.micres.2015.12.006
Sundaramoorthy S, Raguchander T, Ragupathi N, Samiyappan R (2011) Combinatorial effect of endophytic and plant growth promoting rhizobacteria against wilt disease of Capsicum annum L. caused by Fusarium solani. Biol. Control 50:155–174. https://doi.org/10.1016/j.biocontrol.2011.10.002
Rudresh DL, Shivaprakash MK, Prasad RD (2005) Effect of combined application of rhizobium, phosphate solubilizing bacterium and Trichoderma spp. on growth, nutrient uptake and yield of chickpea (Cicer aritenium L.). Appl. Soil Ecol. 28:139–146. https://doi.org/10.1016/j.apsoil.2004.07.005
Ghorchiani M, Etesami H, Alikhani HA (2018) Improvement of growth and yield of maize under water stress by co-inoculating an arbuscular mycorrhizal fungus and a plant growth promoting rhizobacterium together with phosphate fertilizers. Agric. Ecosyst. Environ. 258:59–70. https://doi.org/10.1016/j.agee.2018.02.016
Wintermute EH, Silver PA (2010) Dynamics in the mixed microbial concourse. Genes Dev. 24:2603–2614
Xia Y, Sun J (2017) Hypothesis testing and statistical analysis of microbiome. Genes Dis 4:138–148. https://doi.org/10.1016/j.gendis.2017.06.001
Stegen JC, Bottos EM, Jansson JK (2018) A unified conceptual framework for prediction and control of microbiomes. Curr. Opin. Microbiol. 44:20–27. https://doi.org/10.1016/j.mib.2018.06.002
Ruzzi M, Aroca R (2015) Plant growth-promoting rhizobacteria act as biostimulants in horticulture. Sci Hortic (Amsterdam) 196:124–134. https://doi.org/10.1016/j.scienta.2015.08.042
Owen D, Williams AP, Griffith GW, Withers PJA (2015) Use of commercial bio-inoculants to increase agricultural production through improved phosphorus acquisition. Appl. Soil Ecol. 86:41–54. https://doi.org/10.1016/j.apsoil.2014.09.012
Nicot PC, Bardin M, Alabouvette C, et al (2011) Potential of biological control based on published research. 1. Protection against plant pathogens of selected crops. In: Nicot PC (ed) Classical and augmentative biological control against diseases and pests: critical status analysis and review of factors influencing their success. IOBC/WPRS Publications, Montfavet cedex, FR, pp 1–11
Schneider S, Tajrin T, Lundström JO, Hendriksen NB, Melin P, Sundh I (2017) Do multi-year applications of Bacillus thuringiensis subsp. israelensis for control of mosquito larvae affect the abundance of B. cereus group populations in riparian wetland soils? Microb. Ecol. 74:901–909. https://doi.org/10.1007/s00248-017-1004-0
Díaz S, Fargione J, Chapin FS, Tilman D (2006) Biodiversity loss threatens human well-being. PLoS Biol. 4:e277. https://doi.org/10.1371/journal.pbio.0040277
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat. Methods 9:671–675
Apprill A, McNally S, Parsons R, Weber L (2015) Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat. Microb. Ecol. 75:129–137. https://doi.org/10.3354/ame01753
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes--application to the identification of mycorrhizae and rusts. Mol. Ecol. 2:113–118
Bolyen E, Rideout JR, Dillon MR et al (2018) QIIME 2: Reproducible, interactive, scalable, and extensible microbiome data science. PeerJ:9–10. https://doi.org/10.7287/peerj.preprints.27295v1
Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30:614–620. https://doi.org/10.1093/bioinformatics/btt593
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17:10. https://doi.org/10.14806/ej.17.1.200
Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13:581
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41:D590–D596. https://doi.org/10.1093/nar/gks1219
Tedersoo L, Sánchez-Ramírez S, Kõljalg U et al (2018) High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fungal Divers. 90:135–159. https://doi.org/10.1007/s13225-018-0401-0
Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Gregory Caporaso J (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6:90. https://doi.org/10.1186/s40168-018-0470-z
Price MN, Dehal PS, Arkin AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. https://doi.org/10.1371/journal.pone.0009490
Core Team R (2016) R: a language and environment for statistical computing. R Found Stat Comput 1:409. https://doi.org/10.1007/978-3-540-74686-7
Venables WN, Ripley BD (2002) Modern Applied Statistics with S, Springer, New York https://doi.org/10.1007/978-0-387-21706-2
Mendiburu F, Simon R (2015) Agricolae-ten years of an open source statistical tool for experiments in breeding, agriculture and biology. PeerJ Prepr 3:1–17. https://doi.org/10.7287/peerj.preprints.1404v1
McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol. https://doi.org/10.1371/journal.pcbi.1003531
Oksanen AJ, Blanchet FG, Friendly M, et al (2016) Vegan: community ecology package. https://github.com/vegandevs/vegan
Wei T and Simko V (2017). R package ‘‘corrplot’’: Visualization of a Correlation Matrix (Version 0.84). Available from https://github.com/taiyun/corrplot
Bokulich N, Dillon M, Bolyen E et al (2018) q2-sample-classifier: machine-learning tools for microbiome classification and regression. bioRxiv. https://doi.org/10.1101/306167
Mendes R, Kruijt M, de Bruijn I et al (2011) Deciphering the Rhizosphere microbiome for disease-suppressive bacteria. Science (80- ) 332:1097–1100. https://doi.org/10.1126/science.1203980
Povero G, Mejia JF, Di Tommaso D et al (2016) A systematic approach to discover and characterize natural plant biostimulants. Front. Plant Sci. 7:1–9. https://doi.org/10.3389/fpls.2016.00435
Kaminsky LM, Trexler RV, Malik RJ, Hockett KL, Bell TH (2019) The inherent conflicts in developing soil microbial inoculants. Trends Biotechnol. 37:140–151. https://doi.org/10.1016/j.tibtech.2018.11.011
Stewart EJ (2012) Growing unculturable bacteria. J. Bacteriol. 194:4151–4160. https://doi.org/10.1128/JB.00345-12
Großkopf T, Soyer OS (2014) Synthetic microbial communities. Curr. Opin. Microbiol. 18:72–77. https://doi.org/10.1016/j.mib.2014.02.002
Singh DP, Singh HB, Prabha R (2016) Microbial inoculants in sustainable agricultural productivity: vol. 2: functional applications. Microb Inoculants Sustain Agric Product 2 Funct Appl:1–308. https://doi.org/10.1007/978-81-322-2644-4
Welc M, Ravnskov S, Kieliszewska-Rokicka B, Larsen J (2010) Suppression of other soil microorganisms by mycelium of arbuscular mycorrhizal fungi in root-free soil. Soil Biol. Biochem. 42:1534–1540. https://doi.org/10.1016/j.soilbio.2010.05.024
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 62:227–250. https://doi.org/10.1146/annurev-arplant-042110-103846
González-Guerrero M, Escudero V, Saéz Á, Tejada-Jiménez M (2016) Transition metal transport in plants and associated endosymbionts: arbuscular mycorrhizal fungi and rhizobia. Front. Plant Sci. 7:1–21. https://doi.org/10.3389/fpls.2016.01088
Cameron DD, Neal AL, van Wees SCM, Ton J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci. 18:539–545. https://doi.org/10.1016/j.tplants.2013.06.004
Gajbhiye MH, Kapadnis BP (2016) Antifungal-activity-producing lactic acid bacteria as biocontrol agents in plants. Biocontrol Sci. Tech. 26:1451–1470. https://doi.org/10.1080/09583157.2016.1213793
Ashour SM, Kheiralla ZMH, Badawy FMI, Zaki SS (2015) Killer toxins of the yeasts; Candida utilis 22 and Kluyveromyces marxianus and their potential applications as biocontrol agents. Egypt J Biol Pest Control 25:317–325
Pii Y, Mimmo T, Tomasi N et al (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol. Fertil. Soils 51:403–415. https://doi.org/10.1007/s00374-015-0996-1
Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl. Microbiol. Biotechnol. 84:11–18. https://doi.org/10.1007/s00253-009-2092-7
Jangir M, Pathak R, Sharma S, Sharma S (2018) Biocontrol mechanisms of Bacillus sp., isolated from tomato rhizosphere, against Fusarium oxysporum f. sp. lycopersici. Biol. Control 123:60–70. https://doi.org/10.1016/j.biocontrol.2018.04.018
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56. https://doi.org/10.1038/nrmicro797
Bates ST, Garcia-Pichel F (2009) A culture-independent study of free-living fungi in biological soil crusts of the Colorado Plateau: their diversity and relative contribution to microbial biomass. Environ. Microbiol. 11:56–67. https://doi.org/10.1111/j.1462-2920.2008.01738.x
Yu L, Nicolaisen M, Larsen J, Ravnskov S (2013) Organic fertilization alters the community composition of root associated fungi in Pisum sativum. Soil Biol. Biochem. 58:36–41. https://doi.org/10.1016/j.soilbio.2012.11.004
Prado IGD, da Silva MDS, Prado DGD, Kemmelmeier K et al (2019) Revegetation processes increases the diversity of total and arbuscular mycorrhizal fungi in areas affected by the Fundao dam failure in Mariana, Brazil. Appl. Soil Ecol 141:84–95. https://doi.org/10.1016/j.apsoil.2019.05.008
Stockinger H, Krüger M, Schüßler A (2010) DNA barcoding of arbuscular mycorrhizal fungi. New Phytol. 187:461–474. https://doi.org/10.1111/j.1469-8137.2010.03262.x
Ryan MH, Graham JH (2018) Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytol. 220:1092–1107. https://doi.org/10.1111/nph.15308
Tarbell TJ, Koske RE (2007) Evaluation of commercial arbuscular mycorrhizal inocula in a sand/peat medium. Mycorrhiza 18:51–56. https://doi.org/10.1007/s00572-007-0152-3
Nowrouzian FL, Stadler LS, Adlerberth I, Wold AE (2017) The 16S rRNA gene-based PCR method used for the detection of segmented filamentous bacteria in the intestinal microbiota generates false-positive results. Apmis 125:940–942. https://doi.org/10.1111/apm.12743
Almeida A, Mitchell AL, Tarkowska A, Finn RD (2018) Benchmarking taxonomic assignments based on 16S rRNA gene profiling of the microbiota from commonly sampled environments. Gigascience 7:1–10. https://doi.org/10.1093/gigascience/giy054
Baffoni L, Gaggia F, Dalanaj N, Prodi A, Nipoti P, Pisi A, Biavati B, di Gioia D (2015) Microbial inoculants for the biocontrol of Fusarium spp. in durum wheat. BMC Microbiol. 15:8–10. https://doi.org/10.1186/s12866-015-0573-7
Gaggìa F, Baffoni L, Di Gioia D et al (2013) Inoculation with microorganisms of Lolium perenne L.: evaluation of plant growth parameters and endophytic colonization of roots. New Biotechnol. 30:695–704. https://doi.org/10.1016/j.nbt.2013.04.006
Jilani G, Akram A, Ali RM et al (2007) Enhancing crop growth, nutrients availability, economics and beneficial rhizosphere microflora through organic and biofertilizers. Ann Microbiol 57:177–184. https://doi.org/10.1007/BF03175204
Agler MT, Ruhe J, Kroll S et al (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol. 14:1–31. https://doi.org/10.1371/journal.pbio.1002352
Jones DL, Oburger E (2011) Solubilization of phosphorus by soil microorganisms. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling. Springer Berlin Heidelberg, Berlin, pp 169–198
Verbruggen E (2017) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. Minireview. 1104–1109. https://doi.org/10.1111/j.1469-8137.2012.04348.x
Jackson MA, Dunlap CA, Jaronski ST (2010) Ecological considerations in producing and formulating fungal entomopathogens for use in insect biocontrol. Ecol Fungal Entomopathog:129–145. https://doi.org/10.1007/978-90-481-3966-8_10
Dorrestein PC, Mazmanian SK, Knight R (2014) Finding the missing links among metabolites, microbes, and the host. Immunity 40:824–832. https://doi.org/10.1016/j.immuni.2014.05.015
Gloor GB, Wu JR, Pawlowsky-Glahn V, Egozcue JJ (2016) It’s all relative: analyzing microbiome data as compositions. Ann. Epidemiol. 26:322–329. https://doi.org/10.1016/j.annepidem.2016.03.003
Tsilimigras MCB, Fodor AA (2016) Compositional data analysis of the microbiome: fundamentals, tools, and challenges. Ann. Epidemiol. 26:330–335. https://doi.org/10.1016/j.annepidem.2016.03.002
Wang J, Jia H (2016) Metagenome-wide association studies: fine-mining the microbiome. Nat Rev Microbiol 14:508–522. https://doi.org/10.1038/nrmicro.2016.83
Chang H-X, Haudenshield JS, Bowen CR, Hartman GL (2017) Metagenome-wide association study and machine learning prediction of bulk soil microbiome and crop productivity. Front. Microbiol. 8:1–11. https://doi.org/10.3389/fmicb.2017.00519
Soueidan H, Nikolski M (2017) Machine learning for metagenomics: methods and tools. Metagenomics 1:1–19. https://doi.org/10.1515/metgen-2016-0001
Callahan BJ, Sankaran K, Fukuyama JA et al (2016) Bioconductor workflow for microbiome data analysis: from raw reads to community analyses. F1000Research 5:1492. https://doi.org/10.12688/f1000research.8986.2
Acknowledgments
The authors would like to acknowledge Rachel Berner and Bryce Meyering at UF/IFAS Southwest Florida Research and Education Center for the help and support during the design of the greenhouse setup, sampling of the tomato plants, and soil DNA extractions.
Funding
This work was supported by the USDA National Institute of Food and Agriculture Hatch project 1011186.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Nuzzo, A., Satpute, A., Albrecht, U. et al. Impact of Soil Microbial Amendments on Tomato Rhizosphere Microbiome and Plant Growth in Field Soil. Microb Ecol 80, 398–409 (2020). https://doi.org/10.1007/s00248-020-01497-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-020-01497-7