Skip to main content

Signal and Nutrient Exchange in the Interactions Between Soil Algae and Bacteria

  • Chapter
  • First Online:
Biocommunication in Soil Microorganisms

Part of the book series: Soil Biology ((SOILBIOL,volume 23))

Abstract

Microbial consortia of soil algae and prokaryotes have important functions in terrestrial ecosystems. Recent studies helped delineate phylogenetic diversity of microbiota associated with soil algae. Some signals and nutrients exchanged between algae and the associated bacteria were also identified. Both algae and bacteria appear to benefit from the interactions: algae derive fixed nitrogen, vitamins, and hormones from their bacterial associates. Soil algae also produce vitamin signals (lumichrome and riboflavin) that act as agonists of bacterial cell-to-cell communication known as “quorum sensing.” Further studies are needed to establish the ecological consequences of algal–bacterial nutrient and signal exchange.

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 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Notes

  1. 1.

    “Novel” was defined by the authors as having less than 94% similarity in the V3 region of the 16S rRNA gene to the closest known relative (Otsuka et al. 2008).

References

  • Arevalo-Ferro C et al (2003) Identification of quorum-sensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics. Environ Microbiol 5:1350–1369

    Article  PubMed  CAS  Google Scholar 

  • Baldani JI, Baldani VL (2005) History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An Acad Bras Cienc 77:549–579

    Article  PubMed  CAS  Google Scholar 

  • Bjarnsholt T et al (2005) Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology 151:3873–3880

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2004) Only six kingdoms of life. Proc Biol Sci 271:1251–1262

    Article  PubMed  CAS  Google Scholar 

  • Charlton TS et al (2000) A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. Environ Microbiol 2:530–541

    Article  PubMed  CAS  Google Scholar 

  • Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93

    Article  PubMed  CAS  Google Scholar 

  • Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61:401–422

    Article  PubMed  CAS  Google Scholar 

  • de-Bashan LE, Antoun H, Bashan Y (2008) Involvement of indole-3-acetic acid produced by the growth-promoting bacterium Azospirillum spp. in promoting growth of Chlorella vulgaris. J Phycol 44:938–947

    Article  CAS  Google Scholar 

  • De-Bashan LE, Bashan Y (2008) Joint immobilization of plant growth-promoting bacteria and green microalgae in alginate beads as an experimental model for studying plant-bacterium interactions. Appl Environ Microbiol 74:6797–6802

    Article  PubMed  CAS  Google Scholar 

  • Dobretsov S, Teplitski M, Paul V (2009) Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25:413–427

    Article  PubMed  CAS  Google Scholar 

  • Dong H, Beer SV (2000) Riboflavin induces disease resistance in plants by activating a novel signal transduction pathway. Phytopathology 90:801–811

    Article  PubMed  CAS  Google Scholar 

  • Dworjanyn S, de Nys R, Steinberg P (1999) Localisation and surface quantification of secondary metabolites in the red alga Delisea pulchra. Mar Biol 133:727–736

    Article  CAS  Google Scholar 

  • Dworjanyn SA, de Nys R, Steinberg PD (2006) Chemically mediated antifouling in the red alga Delisea pulchra. Mar Ecol Prog Ser 318:153–163

    Article  CAS  Google Scholar 

  • Flechtner VR (1998) Enigmatic desert soil algae. In: Seckbach J (ed) Enigmatic microorganisms and life in extreme environments. Kluwer Academic Publishers, Dordecht/Boston/London, pp 233–241

    Google Scholar 

  • Gao M et al (2007) Effects of AiiA-mediated quorum quenching in Sinorhizobium meliloti on quorum-sensing signals, proteome patterns, and symbiotic interactions. Mol Plant Microbe Interact 20:843–856

    Article  PubMed  CAS  Google Scholar 

  • Gao M, Teplitski M (2008) RIVET-a tool for in vivo analysis of symbiotically relevant gene expression in Sinorhizobium meliloti. Mol Plant Microbe Interact 21:162–170

    Article  PubMed  CAS  Google Scholar 

  • Gao M, Teplitski M, Robinson JB, Bauer WD (2003) Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol Plant Microbe Interact 16:827–834

    Article  PubMed  CAS  Google Scholar 

  • Gil R, Latorre A, Moya A (2004) Bacterial endosymbionts of insects: insights from comparative genomics. Environ Microbiol 6:1109–1122

    Article  PubMed  CAS  Google Scholar 

  • Givskov M et al (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J Bacteriol 178:6618–6622

    PubMed  CAS  Google Scholar 

  • Grossman AR et al (2007) Novel metabolism in Chlamydomonas through the lens of genomics. Curr Opin Plant Biol 10:190–198

    Article  PubMed  CAS  Google Scholar 

  • Gyurjan I, Nghia NH, Toth G, Turtoczky I, Stefanovits P (1986) Photosynthesis, Nitrogen fixation and enzyme activities in Chlamydomonas–Azotobacter symbioses. Biochem Physiol Pflanz 181:147–153

    CAS  Google Scholar 

  • Gyurjan I, Turtoczky I, Toth G, Paless G, Nghia NH (1984) Intercellular symbiosis of nitrogen-fixing bacteria and green algae. Acta Bot Hung 30:249–256

    Google Scholar 

  • Hasegawa Y, Martin JL, Giewat MW, Rooney-Varga JN (2007) Microbial community diversity in the phycosphere of natural populations of the toxic alga, Alexandrium fundyense. Environ Microbiol 9:3108–3121

    Article  PubMed  CAS  Google Scholar 

  • Hentzer M, Givskov M (2003) Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 112:1300–1307

    PubMed  CAS  Google Scholar 

  • Hentzer M et al (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815

    Article  PubMed  CAS  Google Scholar 

  • Hernandez JP, De-Bashan LE, Rodriguez DJ, Rodriguez Y, Bashan Y (2009) Growth promotion of the freshwater microalga Chlorella vulgaris by the nitrogen-fixing, plant growth-promoting bacterium Bacillus pumilus from arid zone soils. Eur J Soil Biol 45:88–93

    Article  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 

  • Imase M, Watanabe K, Aoyagi H, Tanaka H (2008) Construction of an artificial symbiotic community using a Chlorella-symbiont association as a model. FEMS Microbiol Ecol 63:273–282

    Article  PubMed  CAS  Google Scholar 

  • Joint I et al (2002) Cell-to-cell communication across the prokaryote–eukaryote boundary. Science 298:1207

    Article  PubMed  Google Scholar 

  • Joseph CM, Phillips DA (2003) Metabolites from soil bacteria affect plant water relations. Plant Physiol Biochem 41:189–192

    Article  CAS  Google Scholar 

  • Kiratisin P, Tucker KD, Passador L (2002) LasR, a transcriptional activator of Pseudomonas aeruginosa virulence genes, functions as a multimer. J Bacteriol 184:4912–4919

    Article  PubMed  CAS  Google Scholar 

  • Knee EM et al (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant Microbe Interact 14:775–784

    Article  PubMed  CAS  Google Scholar 

  • Koch B, Liljefors T, Persson T, Nielsen J, Kjelleberg S, Givskov M (2005) The LuxR receptor: the sites of interaction with quorum-sensing signals and inhibitors. Microbiology 151:3589–3602

    Article  PubMed  CAS  Google Scholar 

  • Lambrecht M, Okon Y, Vande Broek A, Vanderleyden J (2000) Indole-3-acetic acid: a reciprocal signalling molecule in bacteria-plant interactions. Trends Microbiol 8:298–300

    Article  PubMed  CAS  Google Scholar 

  • Langhans TM, Storm C, Schwabe A (2009) Community assembly of biological soil crusts of different successional stages in a temperate sand ecosystem, as assessed by direct determination and enrichment techniques. Microb Ecol 58(2):394–407

    Article  PubMed  Google Scholar 

  • Manefield M et al (2002) Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 148:1119–1127

    PubMed  CAS  Google Scholar 

  • Manefield M, Welch M, Givskov M, Salmond GP, Kjelleberg S (2001) Halogenated furanones from the red alga, Delisea pulchra, inhibit carbapenem antibiotic synthesis and exoenzyme virulence factor production in the phytopathogen Erwinia carotovora. FEMS Microbiol Lett 205:131–138

    Article  PubMed  CAS  Google Scholar 

  • Mathesius U et al (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100:1444–1449

    Article  PubMed  CAS  Google Scholar 

  • Matiru VN, Dakora FD (2005) The rhizosphere signal molecule lumichrome alters seedling development in both legumes and cereals. New Phytol 166:439–444

    Article  PubMed  CAS  Google Scholar 

  • McClean KH et al (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143(Pt 12):3703–3711

    Article  PubMed  CAS  Google Scholar 

  • Medina C, Crespo-Rivas JC, Moreno J, Espuny MR, Cubo MT (2009) Mutation in the cobO gene generates auxotrophy for cobalamin and methionine and impairs the symbiotic properties of Sinorhizobium fredii HH103 with soybean and other legumes. Arch Microbiol 191:11–21

    Article  PubMed  CAS  Google Scholar 

  • Nikolaev YA et al (2008) Effect of bacterial satellites on Chlamydomonas reinhardtii growth in an algo-bacterial community. Microbiology 77:78–83

    Article  CAS  Google Scholar 

  • Nyholm SV, Mcfall-Ngai MJ (2004) The winnowing: establishing the squid-Vibrio symbiosis. Nat Rev Microbiol 2:632–642

    Article  PubMed  CAS  Google Scholar 

  • Otsuka S, Abe Y, Fukui R, Nishiyama M, Sendoo K (2008) Presence of previously undescribed bacterial taxa in non-axenic Chlorella cultures. J Gen Appl Microbiol 54:187–193

    Article  PubMed  CAS  Google Scholar 

  • Pasmore M, Costerton JW (2003) Biofilms, bacterial signaling, and their ties to marine biology. J Ind Microbiol Biotechnol 30:407–413

    Article  PubMed  CAS  Google Scholar 

  • Phillips DA, Joseph CM, Yang GP, Martinez-Romero E, Sanborn JR, Volpin H (1999) Identification of lumichrome as a Sinorhizobium enhancer of alfalfa root respiration and shoot growth. Proc Natl Acad Sci USA 96:12275–12280

    Article  PubMed  CAS  Google Scholar 

  • Pierson LS 3rd, Pierson EA (1996) Phenazine antibiotic production in Pseudomonas aureofaciens: role in rhizosphere ecology and pathogen suppresion. FEMS Microbiol Lett 136:101–108

    Article  CAS  Google Scholar 

  • Rajamani S et al (2008) The vitamin riboflavin and its derivative lumichrome activate the LasR bacterial Quorum-Sensing receptor. Mol Plant Microbe Interact 21:1184–1192

    Article  PubMed  CAS  Google Scholar 

  • Ramos C, Licht TR, Sternberg C, Krogfelt KA, Molin S (2001) Monitoring bacterial growth activity in biofilms from laboratory flow chambers, plant rhizosphere, and animal intestine. Meth Enzymol 337:21–42

    Article  PubMed  CAS  Google Scholar 

  • Sapp M, Schwaderer AS, Wiltshire KH, Hoppe HG, Gerdts G, Wichels A (2007) Species-specific bacterial communities in the phycosphere of microalgae? Microb Ecol 53:683–699

    Article  PubMed  Google Scholar 

  • Skindersoe ME, Ettinger-Epstein P, Rasmussen TB, Bjarnsholt T, de Nys R, Givskov M (2008) Quorum sensing antagonism from marine organisms. Mar Biotechnol (NY) 10:56–63

    Article  CAS  Google Scholar 

  • Smith RS, Kelly R, Iglewski BH, Phipps RP (2002) The Pseudomonas autoinducer N-(3-oxododecanoyl) homoserine lactone induces cyclooxygenase-2 and prostaglandin E2 production in human lung fibroblasts: implications for inflammation. J Immunol 169:2636–2642

    PubMed  CAS  Google Scholar 

  • Stanley NR, Lazazzera BA (2004) Environmental signals and regulatory pathways that influence biofilm formation. Mol Microbiol 52:917–924

    Article  PubMed  CAS  Google Scholar 

  • Teplitski M et al (2004) Chlamydomonas reinhardtii secretes compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria. Plant Physiol 134:1–10

    Article  Google Scholar 

  • Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant Microbe Interact 13:637–648

    Article  PubMed  CAS  Google Scholar 

  • Treadwell GE, Metzler DE (1972) Photoconversion of riboflavin to lumichrome in plant tissues. Plant Physiol 49:991–993

    Article  PubMed  CAS  Google Scholar 

  • van Thielen N, Garbary DJ (1998) Life in the rocks – endolithic algae. In: Seckbach J (ed) Enigmatic microorganisms and life in extreme environments. Kluwer Academic Publishers, Dordrecht/Boston/London, pp 245–253

    Google Scholar 

  • Watanabe K, Imase M, Sasaki K, Ohmura N, Saiki H, Tanaka H (2006) Composition of the sheath produced by the green alga Chlorella sorokiniana. Lett Appl Microbiol 42:538–543

    Article  PubMed  CAS  Google Scholar 

  • Watanabe K et al (2005) Symbiotic association in Chlorella culture. FEMS Microbiol Ecol 51:187–196

    Article  PubMed  CAS  Google Scholar 

  • Weinberger F et al (2007) Spore release in Acrochaetium sp (Rhodophyta) is bacterially controlled. J Phycol 43:235–241

    Article  Google Scholar 

  • Wheeler GL, Tait K, Taylor A, Browlee C, Joint I (2005) Acyl-homoserine lactones modulate the settlement rate of zoospores of the marine alga Ulva intestinalis via a novel chemokinetic mechanism. Plant Cell Environ 29:608–618

    Article  Google Scholar 

  • Winson MK et al (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163:185–192

    Article  PubMed  CAS  Google Scholar 

  • Wolfe AJ et al (2003) Evidence that acetyl phosphate functions as a global signal during biofilm development. Mol Microbiol 48:977–988

    Article  PubMed  CAS  Google Scholar 

  • Zhang RG et al (2002) Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 417:971–974

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Max Teplitski .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Teplitski, M., Rajamani, S. (2011). Signal and Nutrient Exchange in the Interactions Between Soil Algae and Bacteria. In: Witzany, G. (eds) Biocommunication in Soil Microorganisms. Soil Biology, vol 23. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-14512-4_16

Download citation

Publish with us

Policies and ethics