Skip to main content
SpringerLink
Log in

Comparison of the Rhizobacteria Serratia sp. H6 and Enterobacter sp. L7 on Arabidopsis thaliana Growth Promotion

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

The genera Serratia and Enterobacter belong to the Enterobacteriaceae family and several members have been described as plant growth-promoting rhizobacteria (PGPR). However, how these bacteria influence growth and development is unclear. We performed in vitro interaction assays between either Serratia sp. H6 or Enterobacter sp. L7 with Arabidopsis thaliana seedlings to analyze their effects on plant growth. In experiments of co-cultivation distant from the root tip, Enterobacter sp. decreased root length, markedly increased lateral root number, and slightly increased plant biomass by 33%, 230%, and 69%, respectively, and relative to the control. The volatile organic compounds (VOCs) emitted from Serratia sp. H6 but not those from Enterobacter sp. L7 promoted Arabidopsis growth. A blend of volatile compounds from the two bacteria had effects on plant growth that were similar to those observed for volatile compounds from H6 only. At several densities, the direct contact of roots with Serratia sp. H6 had phytostimulant properties but Enterobacter sp. L7 had clear deleterious effects. Together, these results suggest that direct contact and VOCs of Serratia sp. H6 were the main mechanisms to promote plant growth of A. thaliana, while diffusible compounds of Enterobacter sp. L7 were predominant in their PGPR activity.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Hardoim PR, van Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471. https://doi.org/10.1016/j.tim.2008.07.008

    Article  CAS  PubMed  Google Scholar 

  2. Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071. https://doi.org/10.1094/MPMI-19-1062

    Article  CAS  PubMed  Google Scholar 

  3. Singh G, Singh N, Marwaha TS (2009) Crop genotype and a novel symbiotic fungus influences the root endophytic colonization potential of plant growth promoting rhizobacteria. Physiol Mol Biol Plants 15:87–92. https://doi.org/10.1007/s12298-009-0009-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Quadt-Hallman A, Hallman J, Kloepper JW (1997) Bacterial endophytes in cotton: location and interaction with other plant associated bacteria. Can J Microbiol 43:254–259. https://doi.org/10.1139/m97-035

    Article  Google Scholar 

  5. Pérez-Montaño F, Alías-Villegas C, Bellogín RA, Cerro PD, Espuny MR, Jiménez-Guerrero I, López-Baena FJ, Ollero FJ, Cubo T (2013) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336. https://doi.org/10.1016/j.micres.2013.09.011

    Article  PubMed  Google Scholar 

  6. Majeed A, Abbasi MK, Hameed S, Imran A, Rahim N (2015) Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion. Front Microbiol 6:198. https://doi.org/10.3389/fmicb.2015.00198

    Article  PubMed  PubMed Central  Google Scholar 

  7. Lucas JA, Ramos Solano B, Montes F, Ojeda J, Megias M, Gutierrez Mañero FJ (2009) Use of two PGPR strains in the integrated management of blast disease in rice (Oryza sativa) in Southern Spain. Field Crop Res 114:404–410. https://doi.org/10.1016/j.fcr.2009.09.013

    Article  Google Scholar 

  8. Qaisrani MM, Mirza MS, Zaheer A, Malik KA (2014) Isolation and identification by 16 srRNA sequence analysis of a Chromobacter, Azospirillum and Rhodococcus strains from the rhizosphere of maize and screening for the beneficial effect on plant growth. Pak J Agric Sci 51:91–99

    Google Scholar 

  9. Cassán F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35. https://doi.org/10.1016/j.ejsobi.2008.08.005

    Article  CAS  Google Scholar 

  10. Shahid M, Hameed S, Imran A, Ali S, van Elsas JD (2012) Root colonization and growth promotion of sunflower (Helianthus annuus L.) by phosphate solubilizing Enterobacter sp. Fs-11. World J Microbiol Biotechnol 28:2749–2758. https://doi.org/10.1007/s11274-012-1086-2

    Article  CAS  PubMed  Google Scholar 

  11. Martinez-Viveros O, Jorquera MA, Crowley DE, Gajardo G, Mora ML (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319. https://doi.org/10.4067/S0718-95162010000100006

    Article  Google Scholar 

  12. Verma JP, Yadav J, Tiwari KN, Lavakush S, Singh V (2010) Impact of plant growth promoting rhizobacteria on crop production. Int J Agric Res 5:954–983. https://doi.org/10.3923/ijar.2010.954.983

    Article  Google Scholar 

  13. Wilson M, McNab R, Henderson B (2002) Bacterial invasion as a virulence mechanism. In: Bacterial disease mechanisms. Cambridge University Press, Cambridge, pp 405–465

    Chapter  Google Scholar 

  14. Gilbert SF, McDonald E, Boyle N, Buttino N, Gyi L, Mai M, Prakash N, Robinson J (2010) Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy. Philos Trans R Soc B 365:671–678

    Article  Google Scholar 

  15. Partida-Martinez LP, Heil M (2011) The microbe-free plant: fact or artifact? Front Plant Sci 2:100. https://doi.org/10.3389/fpls.2011.00100

    Article  PubMed  PubMed Central  Google Scholar 

  16. Bulgari D, Bozkurt AI, Casati P (2012) Endophytic bacterial community living in roots of healthy and ‘Candidatus Phytoplasma mali’- infected apple (Malus domestica, Borkh.) trees. Antonie Van Leeuwenhoek 102:677–687. https://doi.org/10.1007/s10482-012-9766-3

    Article  PubMed  Google Scholar 

  17. Bhore SJ, Nithya R, Loh CY (2010) Screening of endophytic bacteria isolated from leaves of Sambung Nyawa [Gynura procumbens (Lour.) Merr.] for cytokinin-like compounds. Bioinformation 5:191–197. https://doi.org/10.6026/97320630005191

    Article  PubMed  PubMed Central  Google Scholar 

  18. Munif A, Hallmann J, Sikora RA (2012) Isolation of endophytic bacteria from tomato and their biocontrol activities against fungal disease. Microbiol Indones 6:148–156. https://doi.org/10.5454/mi.6.4.2

    Article  Google Scholar 

  19. Gangwar M, Kaur G (2009) Isolation and characterization of endophytic bacteria from endorhizosphere of sugarcane and ryegrass. Internet J Microbiol 7:139–144. https://doi.org/10.5580/181

    Article  Google Scholar 

  20. Kelemu S, Fory P, Zuleta C, Ricaurte J, Rao I, Lascano C (2011) Detecting bacterial endophytes in tropical grasses of the Brachiaria genus and determining their role in improving plant growth. Afr J Biotechnol 10:965–976. https://doi.org/10.5897/AJB10.1305

    Article  Google Scholar 

  21. Lin L, Ge HM, Yan T, Qin YH, Tan RX (2012) Thaxtomin A-deficient endophytic Streptomyces sp. enhances plant disease resistance to pathogenic Streptomyces scabies. Planta 236:1849–1861. https://doi.org/10.1007/s00425-012-1741-8

    Article  CAS  PubMed  Google Scholar 

  22. Miyamoto T, Kawahara M, Minamisawa K (2004) Novel endophytic nitrogen-fixing clostridia from the grass Miscanthus sinensis as revealed by terminal restriction fragment length polymorphism analysis. Appl Environ Microb 70:6580–6586. https://doi.org/10.1128/AEM.70.11.6580-6586.2004

    Article  CAS  Google Scholar 

  23. Rogers A, McDonald K, Muehlbauer MF, Hoffman A, Koenig K, Newman L, Taghavi S, van der Lelie D (2012) Inoculation of hybrid poplar with the endophytic bacterium Enterobacter sp. 638 increases biomass but does not impact leaf level physiology. GCB Bioenergy 4:364–370. https://doi.org/10.1111/j.1757-1707.2011.01119.x

    Article  Google Scholar 

  24. Basha NS, Ogbaghebriel A, Yemane K, Zenebe M (2012) Isolation and screening of endophytic fungi from Eritrean traditional medicinal plant Terminalia brownii leaves for antimicrobial activity. Int J Green Pharm 6:40–44. https://doi.org/10.4103/0973-8258.97124

    Article  Google Scholar 

  25. Ma L, Cao YH, Cheng MH, Huang Y, Mo MH, Wang Y, Yang JZ, Yang FX (2013) Phylogenetic diversity of bacterial endophytes of Panax notoginseng with antagonistic characteristics towards pathogens of root-rot disease complex. Antonie Van Leeuwenhoek 103:299–312. https://doi.org/10.1007/s10482-012-9810-3

    Article  PubMed  Google Scholar 

  26. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026. https://doi.org/10.1104/pp.103.026583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Fincheira P, Quiroz A (2018) Microbial volatiles as plant growth inducers. Microbiol Res 208:63–75. https://doi.org/10.1016/j.micres.2018.01.002

    Article  CAS  PubMed  Google Scholar 

  28. Mhlongo MI, Piater LA, Dubery IA (2022) Profiling of volatile organic compounds from four plant growth-promoting rhizobacteria by SPME–GC–MS: a metabolomics study. Metabolites 12(8):763. https://doi.org/10.3390/metabo12080763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lemfack MC, Gohlke B-O, Toguem SMT, Preissner S, Piechulla B, Preissner R (2018) mVOC 2.0: a database of microbial volatiles. Nucl Acids Res 46:1261–1265. https://doi.org/10.1093/nar/gkx1016

    Article  CAS  Google Scholar 

  30. Tahir HA, Gu Q, Wu H, Raza W, Hanif A, Wu L, Colman MV, Gao X (2017) Plant growth promotion by volatile organic compounds produced by Bacillus subtilis SYST2. Front Microbiol 8:171. https://doi.org/10.3389/fmicb.2017.00171

    Article  PubMed  PubMed Central  Google Scholar 

  31. Lee B, Farag MA, Park HB, Kloepper JW, Lee SH, Ryu CM (2012) Induced resistance by a long-chain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PLoS ONE 7:e48744. https://doi.org/10.1371/journal.pone.0048744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Farag MA, Zhang H, Ryu CM (2013) Dynamic chemical communication between plants and bacteria through airborne signals: Induced resistance by bacterial volatiles. J Chem Ecol 39:1007–1018. https://doi.org/10.1007/s10886-013-0317-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ledger T, Rojas S, Timmermann T, Pinedo I, Poupin MJ, Garrido T, Richter P, Tamayo J, Donoso R (2016) Volatile-mediated effects predominate in Paraburkholderia phytofirmans growth promotion and salt stress tolerance of Arabidopsis thaliana. Front Microbiol 7:1838. https://doi.org/10.3389/fmicb.2016.01838

    Article  PubMed  PubMed Central  Google Scholar 

  34. Vlot AC, Rosenkranz M (2022) Volatile compounds—the language of all kingdoms? J Exp Bot 73:445–448. https://doi.org/10.1093/jxb/erab528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Octavia S, Lan R (2014). In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin. https://doi.org/10.1007/978-3-642-38922-1_167

    Chapter  Google Scholar 

  36. Rodríguez-Díaz M, Belén RG, Clementina PC, Maria Victoria M, Jesús G (2008) A review on the taxonomy and possible screening traits of plant growth promoting rhizobacteria. In: Iqbal A, John P, Shamsul H (eds) Plant–bacteria interactions. Strategies and techniques to promote plant growth. WILEY-VCH Verlag GmbH and Co. KGaA, Weinheim

    Google Scholar 

  37. Sonali JMI, Gayathri KV, Kumar PS, Rangasamy G (2023) A study of potent biofertiliser and its degradation ability of monocrotophos and its in silico analysis. Chemosphere 312:137304. https://doi.org/10.1016/j.chemosphere.2022.137304

    Article  CAS  Google Scholar 

  38. Diksha SK, Sindhu SS, Rakesh Kumar R (2022) Biofertilizers: an ecofriendly technology for nutrient recycling and environmental sustainability. Curr Res Microb Sci 3:100094. https://doi.org/10.1016/j.crmicr.2021.100094

    Article  CAS  PubMed  Google Scholar 

  39. Raimi A, Adeleke R (2022) 16S ribosomal RNA gene-based identification and plant growth-promoting potential of cultivable endophytic bacteria colonising vegetable crops. Agron J 00:00–00. https://doi.org/10.1002/agj2.21241

    Article  Google Scholar 

  40. O’Callaghan M, Ballard RA, Wright D (2022) Soil microbial inoculants for sustainable agriculture: limitations and opportunities. Soil Use Manage 38:1340–1369. https://doi.org/10.1111/sum.12811

    Article  Google Scholar 

  41. Islam S, Akanda AM, Prova A, Islam MT, Hossain MM (2016) Isolation and identification of plant growth promoting rhizobacteria from Cucumber rhizosphere and their effect on plant growth promotion and disease suppression. Front Microbiol 6:1360. https://doi.org/10.3389/fmicb.2015.01360

    Article  PubMed  PubMed Central  Google Scholar 

  42. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

    Article  CAS  PubMed  Google Scholar 

  43. Oo KT, Win TT, Khai AA, Fu PC (2020) Isolation, screening and molecular characterization of multifunctional plant growth promoting rhizobacteria for a sustainable agriculture. Am J Plant Sci 11:773–792. https://doi.org/10.4236/ajps.2020.116055

    Article  CAS  Google Scholar 

  44. Zhu M-L, Wu X-Q, Wang Y-H, Dai Y (2020) Role of biofilm formation by Bacillus pumilus HR10 in biocontrol against pine seedling damping-off disease caused by Rhizoctonia solani. Forests 11:652. https://doi.org/10.3390/f11060652

    Article  Google Scholar 

  45. Collins CH, Lyne PM, Grange JM, Falkinham JO (2004) Microbiological methods. Hodder & Stoughton Ltd, London

    Google Scholar 

  46. Swain MR, Kar S, Padmaja G, Ray RC (2006) Partial characterization and optimization of production of extracellular alpha-amylase from Bacillus subtilis isolated from culturable cow dung microflora. Pol J Microbiol 55:289–296

    CAS  PubMed  Google Scholar 

  47. Wood DA, Claydon N, Dudley KJ, Stephens SK, Allan M (1988) Cellulase production in the life cycle of the cultivated mushroom Agaricus bisporus. In: Aubert JP (ed) FEMS Symposium, biochemistry and genetics of cellulose degradation. Academic press, Cambridge, pp 1–53

    Google Scholar 

  48. Wood PJ, Weisz J (1987) Detection and assay of (1–4)-beta-D-glucanase, (1–3)-beta-D-glucanase, (1–3)(1–4)-beta-D-glucanase, and xylanase based on complex formation of substrate with Congo red. Cereal Chem 64:8–15

    CAS  Google Scholar 

  49. Méndez-Gómez M, Castro-Mercado E, Peña-Uribe CA, Reyes-de la Cruz H, López-Bucio J, García-Pineda E (2020) TARGET OF RAPAMYCIN signaling plays a role in Arabidopsis growth promotion by Azospirillum brasilense Sp245. Plant Sci 293:110416. https://doi.org/10.1016/j.plantsci.2020.110416

    Article  CAS  PubMed  Google Scholar 

  50. Spaepen S, Bossuyt S, Engelen K, Marchal K, Vanderleyden J (2014) Phenotypical and molecular responses of Arabidopsis thaliana roots as a result of inoculation with the auxin-producing bacterium Azospirillum brasilense. New Phytol 201:850–861. https://doi.org/10.1111/nph.12590

    Article  CAS  PubMed  Google Scholar 

  51. Jha CK, Aeron A, Patel BV, Dinesh K, Maheshwari DK, Saraf M (2011) Enterobacter: role in plant growth promotion. In: Maheshwari DK (ed) Bacteria in agrobiology: plant growth responses. Springer, Berlin. https://doi.org/10.1007/978-3-642-20332-9_8

    Chapter  Google Scholar 

  52. Fatima I, Hakim S, Imran A, Ahmad N, Imtiaz M, Ali H, Islam E-U, Yousaf S, Mirza MS, Mubeen F (2022) Exploring biocontrol and growth-promoting potential of multifaceted PGPR isolated from natural suppressive soil against the causal agent of chickpea wilt. Microbiol Res 260:127015. https://doi.org/10.1016/j.micres.2022.127015

    Article  CAS  PubMed  Google Scholar 

  53. Neves Proença D, Schwab S, Soares Vidal M, Baldani JI, Ribeiro Xavier G, Morais PV (2019) The nematicide Serratia plymuthica M24T3 colonizes Arabidopsis thaliana, stimulates plant growth, and presents plant beneficial potential. Braz J Microbiol 50:777–789. https://doi.org/10.1007/s42770-019-00098-y

    Article  CAS  Google Scholar 

  54. Kai M, Crespo E, Cristescu SM, Harren FJ, Francke W, Piechulla B (2010) Serratia odorifera: analysis of volatile emission and biological impact of volatile compounds on Arabidopsis thaliana. Appl Microbiol Biotechnol 88:965–976. https://doi.org/10.1007/s00253-010-2810-1

    Article  CAS  PubMed  Google Scholar 

  55. Wenke K, Kopka J, Schwachtje J, van Dongen J, Piechulla B (2018) Volatiles of rhizobacteria Serratia and Stenotrophomonas alter growth and metabolite composition of Arabidopsis thaliana. Plant Biol 21:109–119. https://doi.org/10.1111/plb.12878

    Article  CAS  PubMed  Google Scholar 

  56. Ranawat B, Mishra S, Singh A (2021) Enterobacter hormaechei (MF957335) enhanced yield, disease and salinity tolerance in tomato. Arch Microbiol 203:2659–2667. https://doi.org/10.1007/s00203-021-02226-5

    Article  CAS  PubMed  Google Scholar 

  57. Meldau DG, Meldau S, Hoang LH, Underberg S, Wünsche H, Baldwin IT (2013) Dimethyl disulfide produced by the naturally associated bacterium Bacillus sp B55 promotes Nicotiana attenuata growth by enhancing sulfur nutrition. Plant Cell 25:2731–2747. https://doi.org/10.1105/tpc.113.114744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Panneerselvam P, Senapati A, Kumar U et al (2019) Antagonistic and plant-growth promoting novel Bacillus species from long-term organic farming soils from Sikkim, India. 3 Biotech 9:416. https://doi.org/10.1007/s13205-019-1938-7

    Article  PubMed  PubMed Central  Google Scholar 

  59. Silva Dias BH, Jung S-H, de Castro V, Oliveira J, Ryu C-M (2021) C4 bacterial volatiles improve plant health. Pathogens 10:682. https://doi.org/10.3390/pathogens10060682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported by the Coordinación de la Investigación Científica, Universidad Michoacana de San Nicolás de Hidalgo, México.

Author information

Authors and Affiliations

  1. Instituto de Investigaciones Químico Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, Ciudad Universitaria, Edif. A1´, CP 58040, Morelia, Michoacán, Mexico

    Narmy Sareli González-Ista, Elda Castro-Mercado, Homero Reyes-de la Cruz, Jesús Campos-García, José López-Bucio & Ernesto García-Pineda

Authors
  1. Narmy Sareli González-Ista
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elda Castro-Mercado
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Homero Reyes-de la Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jesús Campos-García
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José López-Bucio
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ernesto García-Pineda
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NSGI performed the experiments; ECM contributed to technical assistance; EGP designed the study and the methodological strategy; HRC, JCG, JLB, and EGP wrote and revised the manuscript.

Corresponding author

Correspondence to Ernesto García-Pineda.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

Phylogenetic trees of H6 (a) and L7 (b) strains and type strains (superscript T) of the closely related species derived from the maximum likelihood method based on the partial sequence of the 16S rRNA gene. GenBank accession numbers are indicated in parentheses. Bootstrap values (based on 1000 replication) > 50% are shown at branch points. (EPS 1161 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González-Ista, N.S., Castro-Mercado, E., la Cruz, H.Rd. et al. Comparison of the Rhizobacteria Serratia sp. H6 and Enterobacter sp. L7 on Arabidopsis thaliana Growth Promotion. Curr Microbiol 80, 117 (2023). https://doi.org/10.1007/s00284-023-03227-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03227-x

Search

Navigation