Skip to main content
Log in

Impact of Inoculation with Pseudomonas aestus CMAA 1215T on the Non-target Resident Bacterial Community in a Saline Rhizosphere Soil

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Plant growth reduction caused by osmotic stress, pathogens, and nutrient scarcity can be overcome by inoculation with plant growth-promoting rhizobacteria (PGPR). Knowing the effects of PGPR on the microbial community beyond those on plant growth can bring new options of soil microbiota management. The present study aimed to investigate the effect of inoculation with the newly described Pseudomonas aestus CMAA 1215T [a 1-aminocyclopropane-1-carboxylate (ACC) deaminase and glycine-betaine producer] on the rhizosphere bacterial community of Zea mays in natural (non-salinized) and saline soil. The bacterial community structure was assessed by sequencing the V6–V7 16S ribosomal RNA using the Ion Personal Genome Machine. The non-metric multidimensional scaling (NMDS) of the OTU profile (ANOSIM P < 0.01) distinguishes all the treatments (with and without inoculation under saline and natural soils). Inoculated samples shared 1234 OTUs with non-inoculated soil. The most abundant classes in all samples were Alphaproteobacteria, Gammaproteobacteria, Actinobacteria, Acidobacteriia, Bacteroidia, Thermoleophilia, Verrucomicrobiae, Ktenodobacteria, and Bacilli. The inoculation, on the other hand, caused an increase in the abundance of the genera Bacillus, Bryobacter, Bradyrhizobium, “Candidatus Xiphinematobacter”, and “Candidatus Udaeobacter” independent of soil salinization. “Candidatus Udaeobacter” has the largest Mean Decrease in Gini Values with higher abundance on inoculated salted soil. In addition, Pseudomonas inoculation reduced the abundance of Gammaproteobacteria and Phycisphaerae. Understanding how inoculation modifies the bacterial community is essential to manage the rhizospheric microbiome to create a multi-inoculant approach and to understand its effects on ecological function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Da Rocha UN, Plugge CM, George I et al (2013) The rhizosphere selects for particular groups of Acidobacteria and Verrucomicrobia. PLoS ONE 8:16–20. https://doi.org/10.1371/journal.pone.0082443

    Article  CAS  Google Scholar 

  2. Shi S, Nuccio E, Herman DJ et al (2015) Successional trajectories of rhizosphere bacterial communities over consecutive seasons. MBio 6:e00746-e815. https://doi.org/10.1128/mBio.00746-15

    Article  PubMed  PubMed Central  Google Scholar 

  3. Buée M, De BW, Martin F et al (2009) The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321:189–212. https://doi.org/10.1007/s11104-009-9991-3

    Article  CAS  Google Scholar 

  4. Xu X, Passey T, Wei F et al (2015) Amplicon-based metagenomics identified candidate organisms in soils that caused yield decline in strawberry. Hortic Res 2:15022. https://doi.org/10.1038/hortres.2015.22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Jha CK, Saraf M (2015) Plant growth promoting Rhizobacteria (PGPR): a review. J Agric Res Dev 5:108–119. https://doi.org/10.13140/RG.2.1.5171.2164

    Article  Google Scholar 

  6. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol i 190:63–68

    Article  CAS  Google Scholar 

  7. Chihaoui S-A, Trabelsi D, Jdey A et al (2015) Inoculation of Phaseolus vulgaris with the nodule-endophyte Agrobacterium sp. 10C2 affects richness and structure of rhizosphere bacterial communities and enhances nodulation and growth. Arch Microbiol. https://doi.org/10.1007/s00203-015-1118-z

    Article  PubMed  Google Scholar 

  8. Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. Biomed Res Int 2013:863240. https://doi.org/10.1155/2013/863240

    Article  PubMed  PubMed Central  Google Scholar 

  9. Mendes R, Kruijt M, de Bruijn I et al (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100. https://doi.org/10.1126/science.1203980

    Article  CAS  PubMed  Google Scholar 

  10. Défago G, Keel C, Moënne-Loccoz Y (1997) Fate of released Pseudomonas bacteria in the soil profile: implications for the use of genetically modified microbial inoculants. In: Zelikoff JT, Lynch JM, Shepers J (eds) Ecotoxicology: responses, biomarkers and risk assessment. SOS Publications, Fair Heaven, NJ, pp 403–418

    Google Scholar 

  11. Trabelsi D, Mengoni A, Ben Ammar H, Mhamdi R (2011) Effect of on-field inoculation of Phaseolus vulgaris with rhizobia on soil bacterial communities. FEMS Microbiol Ecol 77:211–222. https://doi.org/10.1111/j.1574-6941.2011.01102.x

    Article  CAS  PubMed  Google Scholar 

  12. Schmidt R, Köberl M, Mostafa A et al (2014) Effects of bacterial inoculants on the indigenous microbiome and secondary metabolites of chamomile plants. Front Microbiol 5:1–11. https://doi.org/10.3389/fmicb.2014.00064

    Article  CAS  Google Scholar 

  13. Andreote FD, da Rocha UN, Araújo WL et al (2010) Effect of bacterial inoculation, plant genotype and developmental stage on root-associated and endophytic bacterial communities in potato (Solanum tuberosum). Antonie Van Leeuwenhoek 97:389–399. https://doi.org/10.1007/s10482-010-9421-9

    Article  PubMed  PubMed Central  Google Scholar 

  14. Gomes NCM, Kosheleva IA, Abraham WR, Smalla K (2005) Effects of the inoculant strain Pseudomonas putida KT2442 (pNF142) and of naphthalene contamination on the soil bacterial community. FEMS Microbiol Ecol 54:21–33. https://doi.org/10.1016/j.femsec.2005.02.005

    Article  CAS  PubMed  Google Scholar 

  15. Özen AI, Ussery DW (2012) Defining the Pseudomonas genus: where do we draw the line with azotobacter? Microb Ecol 63:239–248. https://doi.org/10.1007/s00248-011-9914-8

    Article  PubMed  Google Scholar 

  16. Loper JE, Hassan KA, Mavrodi DV et al (2012) Comparative genomics of plant-associated Pseudomonas spp.: Insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet. https://doi.org/10.1371/journal.pgen.1002784

    Article  PubMed  PubMed Central  Google Scholar 

  17. Winsor GL, Lam DKW, Fleming L et al (2011) Pseudomonas genome database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res 39:D596–D600. https://doi.org/10.1093/nar/gkq869

    Article  CAS  PubMed  Google Scholar 

  18. Tkacz A, Poole P (2015) Role of root microbiota in plant productivity. J Exp Bot 66:2167–2175. https://doi.org/10.1093/jxb/erv157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Yang J, Kloepper JW, Ryu C (2008) Rhizosphere bacteria help plants tolerate abiotic stress. Cell Press 14:1–4

    Google Scholar 

  20. D’Souza-Ault MR, Smith LT, Smith GM (1993) Roles of N-acetylglutaminylglutamine amide and glycine betaine in adaptation of Pseudomonas aeruginosa to osmotic stress. Appl Environ Microbiol 59:473–478

    Article  PubMed  PubMed Central  Google Scholar 

  21. Mäkelä P, Jokinen K, Kontturi M et al (1998) Foliar application of glycinebetaine—a novel product from sugar beet—as an approach to increase tomato yield. Ind Crops Prod 7:139–148

    Article  Google Scholar 

  22. Bharti N, Barnawal D, Maji D, Kalra A (2014) Halotolerant PGPRs prevent major shifts in indigenous microbial community structure under salinity stress. Microb Ecol. https://doi.org/10.1007/s00248-014-0557-4

    Article  PubMed  Google Scholar 

  23. Cheng Z, Woody OZ, McConkey BJ, Glick BR (2012) Combined effects of the plant growth-promoting bacterium Pseudomonas putida UW4 and salinity stress on the Brassica napus proteome. Appl Soil Ecol 61:255–263. https://doi.org/10.1016/j.apsoil.2011.10.006

    Article  Google Scholar 

  24. King AJ, Farrer EC, Suding KN, Schmidt SK (2012) Co-occurrence patterns of plants and soil bacteria in the high-alpine subnival zone track environmental harshness. Front Microbiol 3:1–14. https://doi.org/10.3389/fmicb.2012.00347

    Article  Google Scholar 

  25. Ashraf M, Hasnain S, Berge O, Mahmood T (2004) Inoculating wheat seedlings with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol Fertil Soils 40:157–162. https://doi.org/10.1007/s00374-004-0766-y

    Article  CAS  Google Scholar 

  26. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39. https://doi.org/10.1016/j.micres.2013.09.009

    Article  CAS  PubMed  Google Scholar 

  27. Singh A (2015) Soil salinization and waterlogging: a threat to environment and agricultural sustainability. Ecol Indic 57:128–130. https://doi.org/10.1016/j.ecolind.2015.04.027

    Article  Google Scholar 

  28. Ghassemi F, Jakeman AJ, Nix HA (1995) Salinisation of land and water resources: human causes, extent, management and case studies. CAB International, Wallingford

    Google Scholar 

  29. El-Ashry MT, Duda AM (1999) Future perspectives on agricultural drainage. In: Skaggs RW, Van Schilfgaarde J (eds) Agricultural drainage, Agronomy S. American Society of Agronomy, Madison

  30. Fu Q, Liu C, Ding N et al (2010) Ameliorative effects of inoculation with the plant growth-promoting rhizobacterium Pseudomonas sp. DW1 on growth of eggplant (Solanum melongena L.) seedlings under salt stress. Agric Water Manag 97:1994–2000. https://doi.org/10.1016/j.agwat.2010.02.003

    Article  Google Scholar 

  31. Setia R, Gottschalk P, Smith P et al (2012) Soil salinity decreases global soil organic carbon stocks. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2012.08.028

    Article  PubMed  Google Scholar 

  32. Bruning B, Rozema J (2013) Symbiotic nitrogen fixation in legumes: perspectives for saline agriculture. Environ Exp Bot 92:134–143. https://doi.org/10.1016/j.envexpbot.2012.09.001

    Article  CAS  Google Scholar 

  33. Mavi MS, Marschner P (2013) Salinity affects the response of soil microbial activity and biomass to addition of carbon and nitrogen. Soil Res 51:68–75. https://doi.org/10.1071/SR12191

    Article  CAS  Google Scholar 

  34. Canfora L, Bacci G, Pinzari F et al (2014) Salinity and bacterial diversity: to what extent does the concentration of salt affect the bacterial community in a saline soil? PLoS ONE. https://doi.org/10.1371/journal.pone.0106662

    Article  PubMed  PubMed Central  Google Scholar 

  35. Egamberdieva D (2011) Pseudomonas chlororaphis: a salt-tolerant bacterial inoculant for plant growth stimulation under saline soil conditions. Acta Physiol Plant 34:751–756. https://doi.org/10.1007/s11738-011-0875-9

    Article  CAS  Google Scholar 

  36. Avila LA (2012) Diversity and biotechnological potential of Pseudomonas spp. from mangrove sediments. Dissertation, University of São Paulo

  37. Vasconcellos RLF, Santos SN, Zucchi TD et al (2017) Pseudomonas aestus sp. nov., a plant growth-promoting bacterium isolated from mangrove sediments. Arch Microbiol. https://doi.org/10.1007/s00203-017-1410-1

    Article  PubMed  Google Scholar 

  38. Vasconcellos R, Mendes R, Taketani R et al (2013) Draft genome sequence of Pseudomonas sp. strain CMAA 1215, a plant growth-promoting bacterium isolated from a Brazilian mangrove. Genome Announc 1:e00995-e1013. https://doi.org/10.1128/genomeA.00763-13.4

    Article  PubMed  PubMed Central  Google Scholar 

  39. Embrapa (1997) Manual de métodos de análise de solo, 2nd ed. Empresa Brasileira de Pesquisa Agropecuária, Rio de Janeiro

  40. Nadeem SM, Zahir ZA, Naveed M, Arshad M (2007) Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can J Microbiol 53:1141–1149. https://doi.org/10.1139/W07-081

    Article  CAS  PubMed  Google Scholar 

  41. Wang Y, Qian P (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS ONE 4:e7401. https://doi.org/10.1371/journal.pone.0007401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Bessieres M-A, Gibon Y, Lefeuvre JC, Larher F (1999) A single-step purification for glycine betaine determination in plant extracts by isocratic HPLC. J Agric Food Chem 47:3718–3722. https://doi.org/10.1021/jf990031h

    Article  CAS  PubMed  Google Scholar 

  43. Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 2016:1–22. https://doi.org/10.7717/peerj.2584

    Article  Google Scholar 

  44. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303.QIIME

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  Google Scholar 

  46. McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:e1003531. https://doi.org/10.1371/journal.pcbi.1003531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Oksanen J, Blanchet FG, Friendly M et al (2019) vegan: community ecology package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan

  48. Mendiburu F (2020) agricolae: statistical procedures for agricultural research. R package version 1.3-3. https://CRAN.R-project.org/package=agricolae

  49. Liaw A, Wiener M (2002) Classification and regression by randomForest. R News 2:18–22

    Google Scholar 

  50. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216. https://doi.org/10.1016/j.envexpbot.2005.12.006

    Article  CAS  Google Scholar 

  51. Cunha S, d’Avó AF, Mingote A et al (2013) Mannosylglucosylglycerate biosynthesis in the deep-branching phylum planctomycetes: characterization of the uncommon enzymes from Rhodopirellula baltica. Sci Rep 3:2378. https://doi.org/10.1038/srep02378

    Article  PubMed  PubMed Central  Google Scholar 

  52. Sindhu SS, Gupta SK, Dadarwal KR (1999) Antagonistic effect of Pseudomonas spp. on pathogenic fungi and enhancement of growth of green gram (Vigna radiata). Biol Fertil Soils 29:62–68. https://doi.org/10.1007/s003740050525

    Article  CAS  Google Scholar 

  53. Kumawat KC, Sharma P, Sirari A et al (2019) Synergism of Pseudomonas aeruginosa (LSE-2) nodule endophyte with Bradyrhizobium sp. (LSBR-3) for improving plant growth, nutrient acquisition and soil health in soybean. World J Microbiol Biotechnol 35:47. https://doi.org/10.1007/s11274-019-2622-0

    Article  CAS  PubMed  Google Scholar 

  54. Egamberdieva D, Wirth S, Jabborova D et al (2017) Coordination between Bradyrhizobium and Pseudomonas alleviates salt stress in soybean through altering root system architecture. J Plant Interact 12:100–107. https://doi.org/10.1080/17429145.2017.1294212

    Article  CAS  Google Scholar 

  55. Kloepper JW, Ryu C-M, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    Article  CAS  PubMed  Google Scholar 

  56. Nassal D, Spohn M, Eltlbany N et al (2018) Effects of phosphorus-mobilizing bacteria on tomato growth and soil microbial activity. Plant Soil 427:17–37. https://doi.org/10.1007/s11104-017-3528-y

    Article  CAS  Google Scholar 

  57. Ahmad M, Zahir ZA, Nazli F et al (2013) Effectiveness of halo-tolerant, auxin producing Pseudomonas and Rhizobium strains to improve osmotic stress tolerance in mung bean (Vigna radiata L.). Braz J Microbiol 44:1341–1348

  58. Barea J-M, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778. https://doi.org/10.1093/jxb/eri197

    Article  CAS  PubMed  Google Scholar 

  59. Kozdrój J, Trevors JT, van Elsas JD (2004) Influence of introduced potential biocontrol agents on maize seedling growth and bacterial community structure in the rhizosphere. Soil Biol Biochem 36:1775–1784. https://doi.org/10.1016/j.soilbio.2004.04.034

    Article  CAS  Google Scholar 

  60. Dedysh SN (2019) Bryobacter. Bergey’s manual of systematics of archaea and bacteria. Wiley, New Jersey, pp 1–5

    Google Scholar 

  61. Kulichevskaya IS, Suzina NE, Liesack W, Dedysh SN (2010) Bryobacter aggregatus gen. nov., sp. nov., a peat-inhabiting, aerobic chemo-organotroph from subdivision 3 of the Acidobacteria. Int J Syst Evol Microbiol 60:301–306. https://doi.org/10.1099/ijs.0.013250-0

    Article  PubMed  Google Scholar 

  62. Glick BR, Todorovic B, Czarny J et al (2007) Promotion of plant growth by bacterial ACC deaminase. CRC Crit Rev Plant Sci 26:227–242. https://doi.org/10.1080/07352680701572966

    Article  CAS  Google Scholar 

  63. Bruce T, Martinez IB, Neto OM et al (2010) Bacterial community diversity in the Brazilian Atlantic forest soils. Microb Ecol 60:840–849. https://doi.org/10.1007/s00248-010-9750-2

    Article  CAS  PubMed  Google Scholar 

  64. Hedlund BP (2010) Phylum XXIII. Verrucomicrobia phyl. nov. Bergey’s manual® of systematic bacteriology. Springer New York, New York, pp 795–841

    Chapter  Google Scholar 

  65. Brewer TE, Handley KM, Carini P et al (2017) Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’. Nat Microbiol 2:16198. https://doi.org/10.1038/nmicrobiol.2016.198

    Article  CAS  Google Scholar 

  66. Ofek M, Hadar Y, Minz D (2012) Ecology of root colonizing Massilia (Oxalobacteraceae). PLoS ONE 7:e40117. https://doi.org/10.1371/journal.pone.0040117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Wang X, Sharp CE, Jones GM et al (2015) Stable-isotope probing identifies uncultured planctomycetes as primary degraders of a complex heteropolysaccharide in soil. Appl Environ Microbiol 81:4607–4615. https://doi.org/10.1128/AEM.00055-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Dedysh SN (2011) Cultivating uncultured bacteria from Northern Wetlands: knowledge gained and remaining gaps. Front Microbiol. https://doi.org/10.3389/fmicb.2011.00184

    Article  PubMed  PubMed Central  Google Scholar 

  69. García-Salamanca A, Molina-Henares MA, van Dillewijn P et al (2013) Bacterial diversity in the rhizosphere of maize and the surrounding carbonate-rich bulk soil. Microb Biotechnol 6:36–44. https://doi.org/10.1111/j.1751-7915.2012.00358.x

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by the São Paulo Research Foundation—FAPESP (Grant No. 2012/16623-4) and the Brazilian Agricultural Research Corporation—Embrapa (Unit: Embrapa Environment).

Author information

Authors and Affiliations

Authors

Contributions

RLFV designed, directed the project, and wrote the manuscript in consultation with TDZ and ISM. RLFV and ISM conceived of the presented idea. EMR and SNS carried out the metagenome and the greenhouse experiments. RGT contributed to the analysis of the results. All authors discussed the results and contributed to the final manuscript.

Corresponding author

Correspondence to Rafael L. F. Vasconcellos.

Ethics declarations

Conflict of interest

The authors hereby declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 18 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vasconcellos, R.L.F., Romagnoli, E.M., Taketani, R.G. et al. Impact of Inoculation with Pseudomonas aestus CMAA 1215T on the Non-target Resident Bacterial Community in a Saline Rhizosphere Soil. Curr Microbiol 78, 218–228 (2021). https://doi.org/10.1007/s00284-020-02285-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-020-02285-9

Navigation