Skip to main content

Microbial Biofilms: How Effective in Rhizobium–Legume Symbiosis?

  • Chapter
Microbes for Legume Improvement

Abstract

Diverse genera of bacteria live as microbial communities called biofilms on biotic or abiotic surfaces, or interfaces. They exhibit elevated microbial action, as a result of symbiosis in biofilm structure and physiological adaptation. The formation of fungal–bacterial biofilms by bacterial colonization on biotic fungal surfaces gives the biofilms enhanced microbial effectiveness compared to monocultures. When the bacteria include rhizobia, they are called fungal–rhizobial biofilms. The role of biofilm formation in Rhizobium–legume N2-fixing symbiosis contributes to effective root colonization by rhizobia and provides an effective mode for defense and helping rhizobia to survive under harsh and nutrient-limiting environments. Biofilms also indirectly promote the symbiosis by assuring a healthy root system, preserving rhizospheric moisture, and modifying soil pH, leading to enhanced nutrient cycling, biocontrol etc. Poor survival of rhizobial monocultures in inoculant technology can be overcome by using biofilmed inocula called biofilmed biofertilizers (BBs), which could improve legume production. The use of BBs is also likely to develop cooperative symbioses between Rhizobium–legume interaction and microbe–microbe interactions in the biofilm, which will make an improved effect on the former, leading to increased legume production.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Artursson V, Jansson JK (2003) Use of bromodeoxyuridine immunocapture to identify active bacteria associated with arbuscular mycorrhizal hyphae. Appl Environ Microbiol 69:6208–6215

    Article  PubMed  CAS  Google Scholar 

  • Assmus B, Hutzler P, Kirchhof G, Amann R, Lawrence JR, Hartmann A (1995) In situ localization of Azospirillum brasilense in the rhizosphere of wheat with fluorescently labeled rRNA targeted oligonucleotide probes and scanning confocal laser microscopy. Appl Environ Microbiol 61:1013–1019

    PubMed  CAS  Google Scholar 

  • Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319

    Article  PubMed  CAS  Google Scholar 

  • Bandara WMMS, Seneviratne G, Kulasooriya SA (2006) Interactions among endophytic bacteria and fungi: effects and potentials. J Biosci 31:645–650

    Article  PubMed  CAS  Google Scholar 

  • Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778

    Article  PubMed  CAS  Google Scholar 

  • Bashan Y (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol Adv 16:729–770

    Article  CAS  Google Scholar 

  • Bianciotto V, Andreotti S, Balestrini R, Bonfante P, Perotto S (2001a) Extracellular polysaccharides are involved in the attachment of Azospirillum brasilense and Rhizobium leguminosarum to arbuscular mycorrhizal structures. Eur J Histochem 45:39–49

    PubMed  CAS  Google Scholar 

  • Bianciotto V, Andreotti S, Balestrini R, Bonfante P, Perotto S (2001b) Mucoid mutants of the biocontrol strain Pseudomonas fluorescens CHA0 show increased ability in biofilm formation on mycorrhizal and non-mycorrhizal carrot roots. Mol Plant Microbe Interact 14:255–260

    Article  PubMed  CAS  Google Scholar 

  • Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350

    Article  PubMed  CAS  Google Scholar 

  • Bottomley PJ, Myrold DD (2007) Biological N inputs. In: Paul EA (ed) Soil microbiology, ecology, and biochemistry. Academic, Burlington, MA, pp 365–387

    Chapter  Google Scholar 

  • Burmolle M, Webb JS, Rao D, Hansen LH, Sørensen SJ, Kjelleberg S (2006) Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 72:3916–3923

    Article  PubMed  Google Scholar 

  • Chalk PM, Souza RdeF, Urquiaga S, Alves BJR, Boddey RM (2006) The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biol Biochem 38:2944–2951

    Article  CAS  Google Scholar 

  • Chin-A-Woeng TFC, Bloemberg GV, Mulders IHM, Dekkers LC, Lugtenberg BJJ (2000) Root colonisation is essential for biocontrol of tomato foot and root rot by the phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391. Mol Plant Microbe Interact 13:1340–1345

    Article  PubMed  CAS  Google Scholar 

  • Costerton JW, Geesey GG, Cheng KJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:401–404

    Article  Google Scholar 

  • Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745

    Article  PubMed  CAS  Google Scholar 

  • Cunningham AB, Characklis WG, Abedeen F, Crawford D (1991) Influence of biofilm accumulation on porous media hydrodynamics. Environ Sci Technol 25:1305–1311

    Article  CAS  Google Scholar 

  • Davies DG, Chakrabarty AM, Geesey GG (1993) Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa. Appl Environ Microbiol 59:1181–1186

    PubMed  CAS  Google Scholar 

  • de Ruijter NCA, Bisseling T, Emons AMC (1999) Rhizobium nod factors induce an increase in sub-apical fine bundles of actin filaments in Vicia sativa root hairs within minutes. Mol Plant Microbe Interact 12:829–832

    Article  Google Scholar 

  • Dow JM, Fouhy Y, Lucey J, Ryan RP (2007) Cyclic di-GMP as an intracellular signal regulating bacterial biofilm formation. In: Kjelleberg S, Givskov M (eds) The biofilm mode of life: mechanisms and adaptations. Horizon Bioscience, Norwich, pp 71–94

    Google Scholar 

  • Elasri M, Delorme S, Lemanceau P, Stewart G, Laue B, Glickmann E, Oger PM, Dessaux Y (2001) Acyl-homoserine lactone production is more common among plant-associated Pseudomonas spp. than among soil borne Pseudomonas spp. Appl Environ Microbiol 67:1198–1209

    Article  PubMed  CAS  Google Scholar 

  • Elsas JDV, Tam L, Finlay RD, Killham K, Trevors T (2006) Microbial interactions in soil. In: Elsas JDV, Jansson JK, Trevors JT (eds) Modern soil microbiology. CRC press, Taylor and Francis Group, Boca Raton London, New York, pp 177–210

    Google Scholar 

  • Espinosa-Urgel M, Kolter R, Ramos JL (2002) Root colonization by Pseudomonas putida: love at first sight. Microbiology 148:341–343

    PubMed  CAS  Google Scholar 

  • Foster KR, Wenseleers T (2006) A general model for the evolution of mutualisms. J Evol Biol 19:1283–1293

    Article  PubMed  CAS  Google Scholar 

  • Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36

    Article  PubMed  CAS  Google Scholar 

  • Fujishige NA, Kapadia NN, DeHoff PL, Hirsch AM (2006a) Investigations of Rhizobium biofilm formation. FEMS Microbiol Ecol 56:195–206

    Article  PubMed  CAS  Google Scholar 

  • Fujishige NA, Kapadia NN, Hirsch AM (2006b) A feeling for the microorganism: structure on a small scale. Biofilms on plant roots. Bot J Linn Soc 150:79–88

    Article  Google Scholar 

  • Gage DJ (2002) Analysis of infection threads development using Gfp- and DsRed-expressing Sinorhizobium meliloti. J Bacteriol 184:7042–7046

    Article  PubMed  CAS  Google Scholar 

  • Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300

    Article  PubMed  CAS  Google Scholar 

  • Gilbert P, Das J, Foley I (1997) Biofilm susceptibility to antimicrobials. Adv Dent Res 11:160–167

    Article  PubMed  CAS  Google Scholar 

  • Harrison JJ, Turner RJ, Marques LLR, Ceri H (2005) Biofilms. Am Sci 93:508–515

    Google Scholar 

  • Hirsch AM (1999) Role of lectins (and rhizobial exopolysaccharides) in legume nodulation. Curr Opin Plant Biol 2:320–326

    Article  PubMed  CAS  Google Scholar 

  • Hirsch AM, Lum MR, Downie JA (2001) What makes the rhizobia–legume symbiosis so special? Plant Physiol 127:1484–1492

    Article  PubMed  CAS  Google Scholar 

  • Hirsch AM, Bauer WD, Bird DM, Cullimore J, Tyler B, Yoder JI (2003) Molecular signals and receptors: controlling rhizosphere interactions between plants and other organisms. Ecology 84:858–868

    Article  Google Scholar 

  • Ibekwe AM, Angle JS, Chaney RL, Vonberkum P (1997) Enumeration and nitrogen fixation potential of Rhizobium leguminosarum biovar trifolii grown in soil with varying pH values and heavy metal concentrations. Agric Ecosyst Environ 61:103–111

    Article  CAS  Google Scholar 

  • Jayasinghearachchi HS, Seneviratne G (2004a) Can mushrooms fix atmospheric nitrogen? J Biosci 23:293–296

    Article  Google Scholar 

  • Jayasinghearachchi HS, Seneviratne G (2004b) A Bradyrhizobial–Penicillium spp. biofilm with nitrogenase activity improves N2 fixing symbiosis of soybean. Biol Fertil Soils 40:432–434

    Article  CAS  Google Scholar 

  • Jayasinghearachchi HS, Seneviratne G (2006) Fungal solubilization of rock phosphate is enhanced by forming fungal–rhizobia biofilms. Soil Biol Biochem 38:405–408

    Article  CAS  Google Scholar 

  • Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244

    Article  CAS  Google Scholar 

  • Kijne JW, Smit G, Diaz CL, Lugtenberg BJJ (1988) Lectin enhanced accumulation of manganese-limited Rhizobium leguminosarum cells on pea root hair tips. J Bacteriol 170:2994–3000

    PubMed  CAS  Google Scholar 

  • Lazdunski AM, Ventre I, Sturgis JN (2004) Regulatory circuits and communication in gram-negative bacteria. Nat Rev Microbiol 2:581–592

    Article  PubMed  CAS  Google Scholar 

  • Long SR (2001) Genes and signals in the rhizobium–legume symbiosis. Plant Physiol 125:69–72

    Article  PubMed  CAS  Google Scholar 

  • Lugtenberg BJJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490

    Article  PubMed  CAS  Google Scholar 

  • Lum MR, Hirsch AM (2003) Roots and their symbiotic microbes: strategies to obtain nitrogen and phosphorus in a nutrient-limiting environment. J Plant Growth Regul 21:368–382

    Article  Google Scholar 

  • Matthysse AG, Kijne JW (1998) Attachment of Rhizobiaceae to plant cells. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae: molecular biology of plant-associated bacteria. Kluwer Academic Publishers, Dordrecht, Netherlands, pp 235–249

    Google Scholar 

  • Matthysse AG, McMahan S (2001) The effect of the Agrobacterium tumefaciens attR mutation on attachment and root colonization differs between legumes and other dicots. Appl Environ Microbiol 67:1070–1075

    Article  PubMed  CAS  Google Scholar 

  • Matz C, Bergfeld T, Rice SA, Kjelleberg S (2004) Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing. Environ Microbiol 6:218–226

    Article  PubMed  Google Scholar 

  • Morris CE, Monier JM (2003) The ecological significance of biofilm formation by plant-associated bacteria. Annu Rev Phytopathol 41:455–482

    Article  Google Scholar 

  • Nurmiaholassila EL, Haahtela K, Sen R, Timonen S (1997) Bacterial colonization patterns of intact Pinus sylvestris mycorrizospheres in dry pine forest soil – an electron microscopy study. Can J Microbiol 43:1017–1035

    Article  CAS  Google Scholar 

  • Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125

    Article  PubMed  CAS  Google Scholar 

  • Parsek MR, Fuqua C (2004) Biofilms 2003: emerging themes and challenges in studies of surface-associated microbial life. J Bacteriol 186:4427–4440

    Article  PubMed  CAS  Google Scholar 

  • Parsek MR, Tolker-Nielsen T (2008) Pattern formation in Pseudomonas aeruginosa biofilms. Curr Opin Microbiol 11:560–566

    Article  PubMed  CAS  Google Scholar 

  • Pearce D, Bzin MJ, Lynch JM (1995) The rhizosphere as a biofilm. In: Lappin-Scott HM, Costerton JW (eds) Microbial biofilms. Cambridge University Press, Cambridge, pp207–220

    Chapter  Google Scholar 

  • Pérez-Giménez J, Elías JM, Althabegoiti MJ, Covelli J, Quelas JI, López-García SL, Lodeiro AR (2009) Soybean lectin enhances biofilm formation by Bradyrhizobium japonicum in the absence of plants. Int J Microbiol. doi:10.1155/2009/719367

    PubMed  Google Scholar 

  • Pueppke SG, Freund TG, Schulz BC, Friedman HP (1980) Interaction of lectins from soybean and peanut with rhizobia that nodulate soybean, peanut, or both plants. Can J Microbiol 26:1489–1497

    Article  PubMed  CAS  Google Scholar 

  • Raman N, Sambandan K (1998) Distribution of VAM fungi in tannery effluent polluted soils of Tamil Nadu, India. Bull Environ Contam Toxicol 60:142–150

    Article  PubMed  CAS  Google Scholar 

  • Ramey BE, Matthysse AG, Fuqua C (2004) The FNR-type transcriptional regulator SinR controls maturation of Agrobacterium tumefaciens biofilms. Mol Microbiol 52:1495–1511

    Article  PubMed  CAS  Google Scholar 

  • Rinaudi LV, Giordano W (2009) An integrated view of biofilm formation in rhizobia. FEMS Microbiol Lett 304:1–11

    Article  PubMed  Google Scholar 

  • Rinaudi L, Fujishige NA, Hirsch AM, Banchio E, Zorreguieta A, Giordano W (2006) Effects of nutritional and environmental conditions on Sinorhizobium meliloti biofilm formation. Res Microbiol 157:867–875

    Article  PubMed  CAS  Google Scholar 

  • Roberts ME, Stewart PS (2005) Modelling protection from antimicrobial agents in biofilms through the formation of persister cells. Microbiology 51:75–80

    Article  Google Scholar 

  • Rodríguez-Navarro DN, Dardanelli MS, Ruíz-Saínz JE (2007) Attachment of bacteria to the roots of higher plants. FEMS Microbiol Lett 272:127–136

    Article  PubMed  Google Scholar 

  • Romanova YM, Smirnova TA, Andreev AL, Il'ina TS, Didenko LV, Gintsburg AL (2006) Formation of biofilms as an example of the social behavior of bacteria. Microbiology 75:481–485

    Article  CAS  Google Scholar 

  • Rudrappa T, Biedrzycki ML, Bais HP (2008) Causes and consequences of plant-associated biofilms. FEMS Microbiol Ecol 641:53–166

    Google Scholar 

  • Russo DM, Williams A, Edwards A, Posadas DM, Finnie C, Dankert M, Downie JA, Zorreguieta A (2006) Proteins exported via the PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum. J Bacteriol 188:4474–4486

    Article  PubMed  CAS  Google Scholar 

  • Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195

    Article  PubMed  CAS  Google Scholar 

  • Seneviratne G (2003) Development of eco-friendly, beneficial microbial biofilms. Curr Sci 85:1395–1396

    Google Scholar 

  • Seneviratne G, Indrasena IK (2006) Nitrogen fixation in lichens is important for improved rock weathering. J Biosci 31:639–643

    Article  PubMed  Google Scholar 

  • Seneviratne G, Jayasinghearachchi HS (2003) Mycelial colonization by bradyrhizobia and azorhizobia. J Biosci 28:243–247

    Article  PubMed  Google Scholar 

  • Seneviratne G, Jayasinghearachchi HS (2005) A rhizobial biofilm with nitrogenase activity alters nutrient availability in a soil. Soil Biol Biochem 37:1975–1978

    Article  CAS  Google Scholar 

  • Seneviratne G, Tennakoon NS, Weerasekara MLMAW, Nandasena KA (2006) Polyethylene biodegradation by a developed Penicillium–Bacillus biofilm. Curr Sci 90:20–21

    CAS  Google Scholar 

  • Seneviratne G, Zavahir JS, Bandara WMMS, Weerasekara MLMAW (2008a) Fungal–bacterial biofilms: their development for novel biotechnological applications. World J Microbiol Biotechnol 24:739–743

    Article  CAS  Google Scholar 

  • Seneviratne G, Kecskés ML, Kennedy IR (2008b) Biofilmed biofertilisers: novel inoculants for efficient nutrient use in plants. In: Kennedy IR, Choudhury ATMA, Kecskés ML, Rose MT (eds) Efficient nutrient use in rice production in Vietnam achieved using inoculants biofertilisers. Proceedings of a project (SMCN/2002/073) workshop held in Hanoi, Vietnam, 12–13 October 2007. ACIAR Proceeding No. 130, ACIAR, Canberra, pp 126–130

    Google Scholar 

  • Seneviratne G, Thilakaratne RMMS, Jayasekara APDA, Seneviratne KACN, Padmathilake KRE, De Silva MSDL (2009) Developing beneficial microbial biofilms on roots of non-legumes: a novel biofertilizing technique. In: Khan MS, Zaidi A, Musarrat J (eds) Microbial strategies for crop improvement. Springer-Verlag, Berlin, Heidelberg, pp 51–62

    Chapter  Google Scholar 

  • Singh R, Paul D, Jain RK (2006) Biofilms: implications in bioremediation. Trends Microbiol 14:389–397

    Article  PubMed  CAS  Google Scholar 

  • Stewart P, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138

    Article  PubMed  CAS  Google Scholar 

  • Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209

    Article  PubMed  CAS  Google Scholar 

  • Sutherland IW (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3–9

    PubMed  CAS  Google Scholar 

  • Triplett EW, Sadowsky MJ (1992) Genetics of competition for nodulation of legumes. Annu Rev Microbiol 46:399–428

    Article  PubMed  CAS  Google Scholar 

  • Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition: plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397

    Article  PubMed  CAS  Google Scholar 

  • Vilain S, Brözel VS (2006) Multivariate approach to comparing whole-cell proteomes of Bacillus cereus indicates a biofilm specific proteome. J Proteome Res 5:1924–1930

    Article  PubMed  CAS  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    Article  PubMed  CAS  Google Scholar 

  • Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP (2001) Quorum sensing in gram-negative bacteria. FEMS Microbiol Rev 25:365–404

    Article  PubMed  CAS  Google Scholar 

  • Williams A, Wilkinson A, Krehenbrink M, Russo DM, Zorreguieta A (2008) Glucomannan-mediated attachment of Rhizobium leguminosarum to pea root hairs is required for competitive nodule infection. J Bacteriol 190:4706–4715

    Article  PubMed  CAS  Google Scholar 

  • Zahran HH (1999) Rhizobium–legume symbiosis and nitrogen fixation under sever conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    PubMed  CAS  Google Scholar 

  • Zavahir JS, Seneviratne G (2007) Potential of developed microbial biofilms in generating bioactive compounds. Res J Microbiol 2:397–401

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to G. Seneviratne .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag/Wien

About this chapter

Cite this chapter

Seneviratne, G., Weerasekara, M.L.M.A.W., Zavahir, J.S. (2010). Microbial Biofilms: How Effective in Rhizobium–Legume Symbiosis?. In: Khan, M.S., Musarrat, J., Zaidi, A. (eds) Microbes for Legume Improvement. Springer, Vienna. https://doi.org/10.1007/978-3-211-99753-6_6

Download citation

Publish with us

Policies and ethics