Skip to main content

Studying the Life Cycle of Aerobic Endospore-forming Bacteria in Soil

  • Chapter
  • First Online:
Endospore-forming Soil Bacteria

Part of the book series: Soil Biology ((SOILBIOL,volume 27))

  • 5500 Accesses

Abstract

Members of the genus Bacillus are commonly isolated from soils, with members of the Bacillus cereus group being prevalent. Our knowledge of the ecology of B. cereus and other aerobic spore-forming bacteria in soil is far from complete. We have developed an in terra approach to study soil-associated aerobes, using filter-sterilized soil extracted soluble organic matter (SESOM). B. cereus is able to germinate, grow and then sporulate when inoculated into SESOM, or in artificial soil microcosms (ASM). Furthermore, B. cereus switches from single-celled growth to form chains that coalesce to form clumps when cultured in SESOM. Data indicate that the switch to form bundles of chains in soil contributed to translocation of the population through soil by a process termed sliding. Methods for preparing SESOM and ASM are outlined, as are approaches to proteomic analysis and screening transposon mutant libraries for genes contributing to the multicellular phenotype.

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

References

  • Bone EJ, Ellar DJ (1989) Transformation of Bacillus thuringiensis by electroporation. FEMS Microbiol Lett 49:171–177

    Article  PubMed  CAS  Google Scholar 

  • Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, Losick R, Kolter R (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 98:11621–11626

    Article  PubMed  CAS  Google Scholar 

  • Camilli A, Portnoy DA, Youngman P (1990) Insertional mutagenesis of Listeria monocytogenes with a novel Tn917 derivative that allows direct cloning of DNA flanking transposon insertions. J Bacteriol 172:3738–3744

    PubMed  CAS  Google Scholar 

  • Chattopadhyay A, Bhatnagar NB, Bhatnagar R (2004) Bacterial insecticidal toxins. Crit Rev Microbiol 30:33–54

    Article  PubMed  CAS  Google Scholar 

  • Clements MO, Moir A (1998) Role of the gerI operon of Bacillus cereus 569 in the response of spores to germinants. J Bacteriol 180:6729–6735

    PubMed  CAS  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 

  • Daniel R (2004) The soil metagenome–a rich resource for the discovery of novel natural products. Curr Opin Biotechnol 15:199–204

    Article  PubMed  CAS  Google Scholar 

  • Davey ME, O’Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867

    Article  PubMed  CAS  Google Scholar 

  • Davis KE, Joseph SJ, Janssen PH (2005) Effects of growth medium, inoculum size, and incubation time on culturability and isolation of soil bacteria. Appl Environ Microbiol 71:826–834

    Article  PubMed  CAS  Google Scholar 

  • Di Franco C, Beccari E, Santini T, Pisaneschi G, Tecce G (2002) Colony shape as a genetic trait in the pattern-forming Bacillus mycoides. BMC Microbiol 2:1–15

    Article  Google Scholar 

  • Dragon DC, Rennie RP (1995) The ecology of anthrax spores: tough but not invincible. Can Vet J 36:295–301

    PubMed  CAS  Google Scholar 

  • Dragon DC, Bader DE, Mitchell J, Woollen N (2005) Natural dissemination of Bacillus anthracis spores in Northern Canada. Appl Environ Microbiol 71:1610–1615

    Article  PubMed  CAS  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631

    Article  PubMed  CAS  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  PubMed  Google Scholar 

  • Garbeva P, Van Veen JA, Van Elsas JD (2003) Predominant Bacillus spp. in agricultural soil under different management regimes detected via PCR-DGGE. Microb Ecol 45:302–316

    Article  PubMed  CAS  Google Scholar 

  • Guggenberger G, Zech W (1993a) Dissolved organic-matter (Dom) dynamics in spruce forested sites – examinations by analytical dom fractionation. Zeitschrift Fur Pflanzenernahrung Und Bodenkunde 156:341–347

    Article  CAS  Google Scholar 

  • Guggenberger G, Zech W (1993b) Dissolved organic carbon control in acid forest soils of the Fichtelgebirge (Germany) as revealed by distribution patterns and structural composition analyses. Geoderma 59:109–129

    Article  CAS  Google Scholar 

  • Handelsman J, Stabb EV (1996) Biocontrol of soilborne plant pathogens. Plant Cell 8:1855–1869

    Article  PubMed  CAS  Google Scholar 

  • Helgason E, Tourasse NJ, Meisal R, Caugant DA, Kolstø AB (2004) Multilocus sequence typing scheme for bacteria of the Bacillus cereus group. Appl Environ Microbiol 70:191–201

    Article  PubMed  CAS  Google Scholar 

  • Henrichsen J (1972) Bacterial surface translocation: a survey and a classification. Bacteriol Rev 36:478–503

    PubMed  CAS  Google Scholar 

  • Henrici AT (1934) The biology of bacteria. D.C. Heath, Boston

    Google Scholar 

  • Honerlage W, Hahn D, Zeyer J (1995) Detection of mRNA of nprM in Bacillus megaterium ATCC 14581 grown in soil by whole-cell hybridization. Arch Microbiol 163:235–241

    Article  Google Scholar 

  • Huang Y, Eglinton G, Van Der Hage ERE, Boon JJ, Bol R, Ineson P (1998) Dissolved organic matter and its parent organic matter in grass upland soil horizons studied by analytical pyrolysis techniques. Eur J Soil Sci 49:1–15

    Article  Google Scholar 

  • Huang WE, Ferguson A, Singer AC, Lawson K, Thompson IP, Kalin RM, Larkin MJ, Bailey MJ, Whiteley AS (2009) Resolving genetic functions within microbial populations: in situ analyses using rRNA and mRNA stable isotope probing coupled with single-cell raman-fluorescence in situ hybridization. Appl Environ Microbiol 75:234–241

    Article  PubMed  CAS  Google Scholar 

  • Ivanova N, Sorokin A, Anderson I, Galleron N, Candelon B, Kapatral V, Bhattacharyya A, Reznik G, Mikhailova N, Lapidus A, Chu L, Mazur M, Goltsman E, Larsen N, D’Souza M, Walunas T, Grechkin Y, Pusch G, Haselkorn R, Fonstein M, Ehrlich SD, Overbeek R, Kyrpides N (2003) Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423:87–91

    Article  PubMed  CAS  Google Scholar 

  • Jensen GB, Hansen BM, Eilenberg J, Mahillon J (2003) The hidden lifestyles of Bacillus cereus and relatives. Environ Microbiol 5:631–640

    Article  PubMed  CAS  Google Scholar 

  • Jones DL, Kemmitt SJ, Wright D, Cuttle SP, Bol R, Edwards AC (2005) Rapid intrinsic rates of amino acid biodegradation in soils are unaffected by agricultural management strategy. Soil Biol Biochem 37:1267–1275

    Article  CAS  Google Scholar 

  • Kaiser K, Guggenberger G, Haumaier L, Zech W (2001) Seasonal variations in the chemical composition of dissolved organic matter in organic forest floor layer leachates of old-growth Scots pine (Pinus sylvestris L.) and European beech (Fagus sylvatica L.) stands in northeastern Bavaria, Germany. Biogeochemistry 55:103–143

    Article  CAS  Google Scholar 

  • Kalbitz K, Solinger S, Park JH, Michalzik B, Matzner E (2000) Controls on the dynamics dissolved organic matter in soils: a review. Soil Sci 165:277–304

    Article  CAS  Google Scholar 

  • Kalbitz K, Schwesig D, Schmerwitz J, Kaiser K, Haumaier L, Glaser B, Ellerbrock R, Leinweber P (2003) Changes in properties of soil-derived dissolved organic matter induced by biodegradation. Soil Biol Biochem 35:1129–1142

    Article  CAS  Google Scholar 

  • Liebeke M, Brozel VS, Hecker M, Lalk M (2009) Chemical characterization of soil extract as growth media for the ecophysiological study of bacteria. Appl Microbiol Biotechnol 83:161–173

    Article  PubMed  CAS  Google Scholar 

  • Luo Y, Vilain S, Voigt B, Albrecht D, Hecker M, Brozel VS (2007) Proteomic analysis of Bacillus cereus growing in liquid soil organic matter. FEMS Microbiol Lett 271:40–47

    Article  PubMed  CAS  Google Scholar 

  • Lynch JM (1982) Limits to microbial-growth in soil. J Gen Microbiol 128:405–410

    Google Scholar 

  • Margulis L, Jorgensen JZ, Dolan S, Kolchinsky R, Rainey FA, Lo SC (1998) The Arthromitus stage of Bacillus cereus: intestinal symbionts of animals. Proc Natl Acad Sci USA 95:1236–1241

    Article  PubMed  CAS  Google Scholar 

  • Mishustin EN (1972) Microflora of soils in the northern and central USSR. Israel Program for Scientific Translations, Jerusalem, Israel

    Google Scholar 

  • Musat N, Halm H, Winterholler B, Hoppe P, Peduzzi S, Hillion F, Horreard F, Amann R, Jorgensen BB, Kuypers MM (2008) A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. Proc Natl Acad Sci USA 105:17861–17866

    Article  PubMed  CAS  Google Scholar 

  • Olsen RA, Bakken LR (1987) Viability of soil bacteria: optimization of plate-counting technique and comparison between total counts and plate counts within different size groups. Microb Ecol 13:59–74

    Article  Google Scholar 

  • Oosthuizen MC, Steyn B, Theron J, Cosette P, Lindsay D, Von Holy A, Brözel VS (2002) Proteomic analysis reveals differential protein expression by Bacillus cereus during biofilm formation. Appl Environ Microbiol 68:2770–2780

    Article  PubMed  CAS  Google Scholar 

  • O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79

    Article  PubMed  Google Scholar 

  • Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740

    Article  PubMed  CAS  Google Scholar 

  • Pizzeghello D, Zanella A, Carletti P, Nardi S (2006) Chemical and biological characterization of dissolved organic matter from silver fir and beech forest soils. Chemosphere 65:190–200

    Article  PubMed  CAS  Google Scholar 

  • Priest FG, Barker M, Baillie LW, Holmes EC, Maiden MC (2004) Population structure and evolution of the Bacillus cereus group. J Bacteriol 186:7959–7970

    Article  PubMed  CAS  Google Scholar 

  • Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394

    Article  PubMed  CAS  Google Scholar 

  • Rickard AH, Gilbert P, High NJ, Kolenbrander PE, Handley PS (2003) Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol 11:94–100

    Article  PubMed  CAS  Google Scholar 

  • Rihani M, Cancela Da Fonseca JP, Kiffer E (1995) Decomposition of beech leaf litter by microflora and mesofauna. II. Food preferences and action of oribatid mites on different substrates. Eur J Soil Biol 31:67–79

    Google Scholar 

  • Saggar S, Parshotam A, Hedley C, Salt G (1999) 14C-labelled glucose turnover in New Zealand soils. Soil Biol Biochem 31:2025–2037

    Article  CAS  Google Scholar 

  • Saleh SM, Harris RF, Allen ON (1970) Fate of Bacillus thuringiensis in soil: effect of soil pH and organic amendment. Can J Microbiol 16:677–680

    Article  PubMed  CAS  Google Scholar 

  • Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2:e92

    Article  PubMed  Google Scholar 

  • Schneckenberger K, Demin D, Stahr K, Kuzyakov Y (2008) Microbial utilization and mineralization of [14C]glucose added in six orders of concentration to soil. Soil Biol Biochem 40:1981–1988

    Article  CAS  Google Scholar 

  • Schoeni JL, Wong AC (2005) Bacillus cereus food poisoning and its toxins. J Food Prot 68:636–648

    PubMed  CAS  Google Scholar 

  • Stabb EV, Jacobson LM, Handelsman J (1994) Zwittermicin A-producing strains of Bacillus cereus from diverse soils. Appl Environ Microbiol 60:4404–4412

    PubMed  CAS  Google Scholar 

  • Stoodley P, Dodds I, Boyle JD, Lappin-Scott HM (1999) Influence of hydrodynamics and nutrients on biofilm structure. J Appl Microbiol Suppl 85:19S–28S

    Article  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 

  • Stotzky G, Burns RG (1982) The soil environment: Clay – Humus – Microbe interactions. In: Burns RG and Slater JH (eds) Experimental microbial ecology. Blackwell Scientific, Oxford

    Google Scholar 

  • Strobel BW (2001) Influence of vegetation on low-molecular-weight carboxylic acids in soil solution: a review. Geoderma 99:169–198

    Article  CAS  Google Scholar 

  • Sutherland IW (2001) The biofilm matrix – an immobilized but dynamic microbial environment. Trends Microbiol 9:222–227

    Article  PubMed  CAS  Google Scholar 

  • Tiunov AV, Scheu S (2004) Carbon availability controls the growth of detritivores (Lumbricidae) and their effect on nitrogen mineralization. Oecologia 138:83–90

    Article  PubMed  Google Scholar 

  • Torsvik V, Øvreås L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245

    Article  PubMed  CAS  Google Scholar 

  • Torsvik V, Goksoyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787

    PubMed  CAS  Google Scholar 

  • Van Hees PAW, Jones DL, Finlay R, Godbold DL, Lundstromd US (2005) The carbon we do not see – the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13

    Article  Google Scholar 

  • Van Ness GB (1971) Ecology of anthrax. Science 172:1303–1307

    Article  PubMed  Google Scholar 

  • Veening JW, Smits WK, Kuipers OP (2008) Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol 62:193–210

    Article  PubMed  CAS  Google Scholar 

  • Vilain S, Brozel 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 

  • Vilain S, Luo Y, Hildreth MB, Brözel VS (2006) Analysis of the life cycle of the soil saprophyte Bacillus cereus in liquid soil extract and in soil. Appl Environ Microbiol 72:4970–4977

    Article  PubMed  CAS  Google Scholar 

  • Vilain S, Pretorius JM, Theron J, Brozel VS (2009) DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 75:2861–2868

    Article  PubMed  CAS  Google Scholar 

  • von Stetten F, Mayr R, Scherer S (1999) Climatic influence on mesophilic Bacillus cereus and psychrotolerant Bacillus weihenstephanensis populations in tropical, temperate and alpine soil. Environ Microbiol 1:503–515

    Article  Google Scholar 

  • Waksman SA (1932) Principles of soil microbiology. Williams and Wilkins, Baltimore

    Google Scholar 

  • Wilson AC, Perego M, Hoch JA (2007) New transposon delivery plasmids for insertional mutagenesis in Bacillus anthracis. J Microbiol Methods 71:332–335

    Article  PubMed  CAS  Google Scholar 

  • Wolfaardt GM, Lawrence JR, Robarts RD, Caldwell SJ, Caldwell DE (1994) Multicellular organization in a degradative biofilm community. Appl Environ Microbiol 60:434–446

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Volker S. Brözel .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Brözel, V.S., Luo, Y., Vilain, S. (2011). Studying the Life Cycle of Aerobic Endospore-forming Bacteria in Soil. In: Logan, N., Vos, P. (eds) Endospore-forming Soil Bacteria. Soil Biology, vol 27. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19577-8_6

Download citation

Publish with us

Policies and ethics