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Isolation and Cultivation of Bacteria

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The Structure and Function of Aquatic Microbial Communities

Part of the book series: Advances in Environmental Microbiology ((AEM,volume 7))

Abstract

Isolation and cultivation of microorganisms enables in combination with cultivation-independent methods comprehensive research on ecology and function of microbes. The availability of cultures provides opportunities for ecophysiological experiments, enables high-quality genome research and represents a mandatory prerequisite for the description of new taxa of prokaryotes. Unfortunately, access to microorganism by cultivation methods is still quite limited, and the majority of the microbial diversity remains uncultured so far. This chapter discusses the potential reasons for this lack in cultivability and reviews advances in cultivation methods for prokaryotes. Detailed analysis of the media and methods used by taxonomists for isolation of bacterial strains used for description of >1000 new species revealed that the description of new taxa in the ranks of species and genera is currently not methodically limited. On the other hand, isolation of strains enabling the description of taxa representing higher ranks is obviously strongly limited by the currently applied methods. Consequently, different cultivation strategies are required according to the scientific goals of the respective research. While taxonomists interested in the description of new species affiliated with any genus or family can isolate new strains suitable for this task by using standard cultivation methods and media, ecologists interested in cultivation of model organisms appearing in natural systems with high cell numbers, as well as taxonomists interested in isolation of strains representing new higher ranking taxa like orders, classes and phyla, should rather use high-throughput non-standard methods in combination with optimized screening protocols.

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References

  • Alain K, Querellou J (2009) Cultivating the uncultured: limits, advances and future challenges. Extremophiles 13(4):583–594

    Article  PubMed  Google Scholar 

  • Alam M, Sadique A, Nur AH, Bhuiyan NA, Nair GB, Siddique AK, Sack DA, Ahsan S, Huq A, Sack RB, Colwell RR (2006) Effect of transport at ambient temperature on detection and isolation of Vibrio cholerae from environmental samples. Appl Environ Microbiol 72(3):2185–2190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410

    Article  CAS  PubMed  Google Scholar 

  • Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59(1):143–169

    CAS  PubMed  PubMed Central  Google Scholar 

  • Atlas RM (2010) Handbook of microbiological media. CRC Press, Boca Raton

    Book  Google Scholar 

  • Barer MR, Harwood CR (1999) Bacterial viability and culturability. Adv Microb Physiol 41:93–137

    Article  CAS  PubMed  Google Scholar 

  • Batut B, Knibbe C, Marais G, Daubin V (2014) Reductive genome evolution at both ends of the bacterial population size spectrum. Nat Rev Microbiol 12(12):841–850

    Article  CAS  PubMed  Google Scholar 

  • Becker S, Vogt J, Knopp S, Panning M, Warhurst D, Polman K, Marti H, von Muller L, Yansouni C, Jacobs J, Bottieau E, Sacko M, Rijal S, Meyanti F, Miles M, Boelaert M, Lutumba P, van Lieshout L, N’Goran E, Chappuis F, Utzinger J (2013) Persistent digestive disorders in the tropics: causative infectious pathogens and reference diagnostic tests. BMC Infect Dis 13(1):37

    Article  PubMed  PubMed Central  Google Scholar 

  • Biers EJ, Sun S, Howard EC (2009) Prokaryotic genomes and diversity in surface ocean waters: interrogating the global ocean sampling metagenome. Appl Environ Microbiol 75(7):2221–2229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blevins SM, Bronze MS (2010) Robert Koch and the ‘golden age’ of bacteriology. Int J Infect Dis 14(9):e744–e751

    Article  PubMed  Google Scholar 

  • Bogosian G, Aardema ND, Bourneuf EV, Morris PJL, O’Neil JP (2000) Recovery of hydrogen peroxide-sensitive culturable cells of Vibrio vulnificus gives the appearance of resuscitation from a viable but nonculturable state. J Bacteriol 182(18):5070–5075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bollmann A, Lewis K, Epstein SS (2007) Incubation of environmental samples in a diffusion chamber increases the diversity of recovered isolates. Appl Environ Microbiol 73(20):6386–6390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braine T (2011) Race against time to develop new antibiotics. Bull World Health Organ 89:88–89

    Article  PubMed  Google Scholar 

  • Britschgi TB, Giovannoni SJ (1991) Phylogenetic analysis of a natural marine bacterioplankton population by rRNA gene cloning and sequencing. Appl Environ Microbiol 57(6):1707–1713

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brock TD (1999) Robert Koch: a life in medicine and bacteriology. ASM Press, Washington, DC

    Book  Google Scholar 

  • Bruns A, Cypionka H, Overmann J (2002) Cyclic AMP and acyl homoserine lactones increase the cultivation efficiency of heterotrophic bacteria from the central Baltic Sea. Appl Environ Microbiol 68(8):3978–3987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruns A, Hoffelner H, Overmann J (2003a) A novel approach for high throughput cultivation assays and the isolation of planktonic bacteria. FEMS Microbiol Ecol 45(2):161–171

    Article  CAS  PubMed  Google Scholar 

  • Bruns A, Nubel U, Cypionka H, Overmann J (2003b) Effect of signal compounds and incubation conditions on the culturability of freshwater bacterioplankton. Appl Environ Microbiol 69(4):1980–1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Button DK, Robertson BR (2001) Determination of DNA content of aquatic bacteria by flow cytometry. Appl Environ Microbiol 67(4):1636–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Button DK, Schut F, Quang P, Martin R, Robertson BR (1993) Viability and isolation of marine bacteria by dilution culture: theory, procedures, and initial results. Appl Environ Microbiol 59(3):881–891

    CAS  PubMed  PubMed Central  Google Scholar 

  • Canale-Parola E, Rosenthal SL, Kupfer DG (1966) Morphological and physiological characteristics of Spirillum gracile sp. n. Antonie Van Leeuwenhoek 32(2):113–124

    Article  CAS  PubMed  Google Scholar 

  • Carini P, Steindler L, Beszteri S, Giovannoni SJ (2013) Nutrient requirements for growth of the extreme oligotroph ‘Candidatus Pelagibacter ubique’ HTCC1062 on a defined medium. ISME J 7(3):592–602

    Article  CAS  PubMed  Google Scholar 

  • Cho JC, Giovannoni SJ (2004) Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Appl Environ Microbiol 70(1):432–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choo Y-J, Lee K, Song J, Cho J-C (2007) Puniceicoccus vermicola gen. nov., sp. nov., a novel marine bacterium, and description of Puniceicoccaceae fam. nov., Puniceicoccales ord. nov., Opitutaceae fam. nov., Opitutales ord. nov. and Opitutae classis nov. in the phylum ‘Verrucomicrobia’. Int J Syst Evol Microbiol 57(3):532–537

    Article  CAS  PubMed  Google Scholar 

  • Connon SA, Giovannoni SJ (2002) High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. Appl Environ Microbiol 68(8):3878–3885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Connon SA, Lester ED, Shafaat HS, Obenhuber DC, Ponce A (2007) Bacterial diversity in hyperarid Atacama Desert soils. J Geophys Res Biogeosci 112(G4)

    Article  CAS  Google Scholar 

  • Crosbie ND, Pockl M, Weisse T (2003) Dispersal and phylogenetic diversity of nonmarine picocyanobacteria, inferred from 16S rRNA gene and cpcBA-intergenic spacer sequence analyses. Appl Environ Microbiol 69(9):5716–5721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Curtis TP, Head IM, Lunn M, Woodcock S, Schloss PD, Sloan WT (2006) What is the extent of prokaryotic diversity? Philos Trans R Soc B Biol Sci 361(1475):2023–2037

    Article  Google Scholar 

  • Curtis TP, Sloan WT, Scannell JW (2002) Estimating prokaryotic diversity and its limits. Proc Natl Acad Sci U S A 99(16):10494–10499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Onofrio A, Crawford JM, Stewart EJ, Witt K, Gavrish E, Epstein S, Clardy J, Lewis K (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 17(3):254–264

    Article  PubMed  PubMed Central  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(2):826–834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis KE, Sangwan P, Janssen PH (2011) Acidobacteria, Rubrobacteridae and Chloroflexi are abundant among very slow-growing and mini-colonyforming soil bacteria. Environ Microbiol 13:798–805

    Article  PubMed  Google Scholar 

  • Delmée M, Van Broeck J, Simon A, Janssens M, Avesani V (2005) Laboratory diagnosis of Clostridium difficile-associated diarrhoea: a plea for culture. J Med Microbiol 54(2):187–191

    Article  PubMed  CAS  Google Scholar 

  • Dufresne A, Garczarek L, Partensky F (2005) Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol 6(2):R14

    Article  PubMed  PubMed Central  Google Scholar 

  • Dykhuizen D (2005) Species numbers in bacteria. Proc Calif Acad Sci 56(6 Suppl 1):62–71

    PubMed  PubMed Central  Google Scholar 

  • Dykhuizen DE (1998) Santa Rosalia revisited: why are there so many species of bacteria? Anton Leeuw Int J Gen Mol Microbiol 73(1):25–33

    Article  CAS  Google Scholar 

  • Eichorst SA, Breznak JA, Schmidt TM (2007) Isolation and characterization of soil bacteria that define Terriglobus gen. nov., in the phylum Acidobacteria. Appl Environ Microbiol 73(8):2708–2717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emerson D, Rentz JA, Lilburn TG, Davis RE, Aldrich H, Chan C, Moyer CL (2007) A novel lineage of proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PLoS One 2(7):e667

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ewann F, Hoffman PS (2006) Cysteine metabolism in Legionella pneumophila: characterization of an L-cystine-utilizing mutant. Appl Environ Microbiol 72(6):3993–4000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrari BC, Binnerup SJ, Gillings M (2005) Microcolony cultivation on a soil substrate membrane system selects for previously uncultured soil bacteria. Appl Environ Microbiol 71(12):8714–8720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrari BC, Winsley T, Gillings M, Binnerup S (2008) Cultivating previously uncultured soil bacteria using a soil substrate membrane system. Nat Protoc 3(8):1261–1269

    Article  CAS  PubMed  Google Scholar 

  • Foesel BU, Nägele V, Naether A, Wüst PK, Weinert J, Bonkowski M, Lohaus G, Polle A, Alt F, Oelmann Y, Fischer M, Friedrich MW, Overmann J (2014) Determinants of Acidobacteria activity inferred from the relative abundances of 16S rRNA transcripts in German grassland and forest soils. Environ Microbiol 16(3):658–675

    Article  CAS  PubMed  Google Scholar 

  • Garcia SL, McMahon KD, Grossart HP, Warnecke F (2014) Successful enrichment of the ubiquitous freshwater acI Actinobacteria. Environ Microbiol Rep 6(1):21–27

    Article  CAS  PubMed  Google Scholar 

  • Gich F, Schubert K, Bruns A, Hoffelner H, Overmann J (2005) Specific detection, isolation, and characterization of selected, previously uncultured members of the freshwater bacterioplankton community. Appl Environ Microbiol 71(10):5908–5919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giovannoni SJ, Bibbs L, Cho JC, Stapels MD, Desiderio R, Vergin KL, Rappe MS, Laney S, Wilhelm LJ, Tripp HJ, Mathur EJ, Barofsky DF (2005a) Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438(7064):82–85

    Article  CAS  PubMed  Google Scholar 

  • Giovannoni SJ, Cameron Thrash J, Temperton B (2014) Implications of streamlining theory for microbial ecology. ISME J 8(8):1553–1565

    Article  PubMed  PubMed Central  Google Scholar 

  • Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, Baptista D, Bibbs L, Eads J, Richardson TH, Noordewier M, Rappe MS, Short JM, Carrington JC, Mathur EJ (2005b) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309(5738):1242–1245

    Article  CAS  PubMed  Google Scholar 

  • Glockner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, Pernthaler A, Amann R (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria. Appl Environ Microbiol 66(11):5053–5065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godoy F, Vancanneyt M, Martínez M, Steinbüchel A, Swings J, Rehm BHA (2003) Sphingopyxis chilensis sp. nov., a chlorophenol-degrading bacterium that accumulates polyhydroxyalkanoate, and transfer of Sphingomonas alaskensis to Sphingopyxis alaskensis comb. nov. Int J Syst Evol Microbiol 53(2):473–477

    Article  CAS  PubMed  Google Scholar 

  • Gould LH, Bopp C, Strockbine N, Atkinson R, Baselski V, Body B, Carey R, Crandall C, Hurd S, Kaplan R, Neill M, Shea S, Somsel P, Tobin-D’Angelo M, Griffin PM, Gerner-Smidt P (2009) Recommendations for diagnosis of shiga toxin–producing Escherichia coli infections by clinical laboratories. MMWR Recomm Rep 58(Rr-12):1–14

    PubMed  Google Scholar 

  • Hahn MW (2003) Isolation of strains belonging to the cosmopolitan Polynucleobacter necessarius cluster from freshwater habitats located in three climatic zones. Appl Environ Microbiol 69(9):5248–5254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hahn MW (2004) Broad diversity of viable bacteria in ‘sterile’ (0.2 μm) filtered water. Res Microbiol 155(8):688–691

    Article  PubMed  Google Scholar 

  • Hahn MW (2009) Description of seven candidate species affiliated with the phylum Actinobacteria, representing planktonic freshwater bacteria. Int J Syst Evol Microbiol 59:112–117

    Article  CAS  PubMed  Google Scholar 

  • Hahn MW, Kasalicky V, Jezbera J, Brandt U, Jezberova J, Simek K (2010) Limnohabitans curvus gen. nov., sp nov., a planktonic bacterium isolated from a freshwater lake. Int J Syst Evol Microbiol 60:1358–1365

    Article  CAS  PubMed  Google Scholar 

  • Hahn MW, Lang E, Brandt U, Wu QL, Scheuerl T (2009) Emended description of the genus Polynucleobacter and the species Polynucleobacter necessarius and proposal of two subspecies, P. necessarius subsp. necessarius subsp nov and P. necessarius subsp asymbioticus subsp nov. Int J Syst Evol Microbiol 59:2002–2009

    Article  CAS  PubMed  Google Scholar 

  • Hahn MW, Minasyan A, Lang E, Koll U, Sproeer C (2012a) Polynucleobacter difficilis sp nov., a planktonic freshwater bacterium affiliated with subcluster B1 of the genus Polynucleobacter. Int J Syst Evol Microbiol 62:376–383

    Article  PubMed  Google Scholar 

  • Hahn MW, Pockl M, Wu QL (2005) Low intraspecific diversity in a Polynucleobacter subcluster population numerically dominating bacterioplankton of a freshwater pond. Appl Environ Microbiol 71(8):4539–4547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hahn MW, Scheuerl T, Jezberova J, Koll U, Jezbera J, Simek K, Vannini C, Petroni G, Wu QLL (2012b) The passive yet successful way of planktonic life: genomic and experimental analysis of the ecology of a free-living Polynucleobacter population. PLoS One 7(3):e32772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hahn MW, Schmidt J, Taipale SJ, Doolittle WF, Koll U (2014) Rhodoluna lacicola gen. nov., sp. nov., a planktonic freshwater bacterium with stream-lined genome. Int J Syst Evol Microbiol 64(Pt 9):3254–3263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hahn MW, Stadler P, Wu QL, Pockl M (2004) The filtration-acclimatization method for isolation of an important fraction of the not readily cultivable bacteria. J Microbiol Methods 57(3):379–390

    Article  CAS  PubMed  Google Scholar 

  • Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68(4):669–685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hazan R, Que Y-A, Maura D, Rahme L (2012) A method for high throughput determination of viable bacteria cell counts in 96-well plates. BMC Microbiol 12(1):259

    Article  PubMed  PubMed Central  Google Scholar 

  • Hesse W (1992) Walther and Angelina Hesse-Early contributors to bacteriology. ASM News 58:425–428

    Google Scholar 

  • Huber R, Burggraf S, Mayer T, Barns SM, Rossnagel P, Stetter KO (1995) Isolation of a hyperthermophilic archaeum predicted by in situ RNA analysis. Nature 376(6535):57–58

    Article  CAS  PubMed  Google Scholar 

  • Huber R, Huber H, Stetter KO (2000) Towards the ecology of hyperthermophiles: biotopes, new isolation strategies and novel metabolic properties. FEMS Microbiol Rev 24(5):615–623

    Article  CAS  PubMed  Google Scholar 

  • Hugenholtz P (2002) Exploring prokaryotic diversity in the genomic era. Genome Biol 3(2):reviews0003.0001–reviews0003.0008

    Article  Google Scholar 

  • Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180(18):4765–4774

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jannasch HW, Jones GE (1959) Bacterial populations in sea water as determined by different methods of enumeration. Limnol Oceanogr 4(2):128–139

    Article  Google Scholar 

  • Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72(3):1719–1728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janssen PH, Schuhmann A, Morschel E, Rainey FA (1997) Novel anaerobic ultramicrobacteria belonging to the Verrucomicrobiales lineage of bacterial descent isolated by dilution culture from anoxic rice paddy soil. Appl Environ Microbiol 63(4):1382–1388

    CAS  PubMed  PubMed Central  Google Scholar 

  • Janssen PH, Yates PS, Grinton BE, Taylor PM, Sait M (2002) Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia. Appl Environ Microbiol 68(5):2391–2396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaspers E, Overmann J (2004) Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl Environ Microbiol 70(8):4831–4839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jezbera J, Jezberova J, Koll U, Hornak K, Simek K, Hahn MW (2012) Contrasting trends in distribution of four major planktonic betaproteobacterial groups along a pH gradient of epilimnia of 72 freshwater habitats. FEMS Microbiol Ecol 81(2):467–479

    Article  CAS  PubMed  Google Scholar 

  • Jezbera J, Sharma AK, Brandt U, Doolittle WF, Hahn MW (2009) ‘Candidatus Planktophila limnetica’, an actinobacterium representing one of the most numerically important taxa in freshwater bacterioplankton. Int J Syst Evol Microbiol 59:2864–2869

    Article  CAS  PubMed  Google Scholar 

  • Jezberova J, Jezbera J, Brandt U, Lindstrom ES, Langenheder S, Hahn MW (2010) Ubiquity of Polynucleobacter necessarius ssp. asymbioticus in lentic freshwater habitats of a heterogenous 2000 km2 area. Environ Microbiol 12(3):658–669

    Article  PubMed  Google Scholar 

  • Jogler M, Chen H, Simon J, Rohde M, Busse H-J, Klenk H-P, Tindall BJ, Overmann J (2013) Description of Sphingorhabdus planktonica gen. nov., sp. nov. and reclassification of three related members of the genus Sphingopyxis in the genus Sphingorhabdus gen. nov. Int J Syst Evol Microbiol 63(Pt 4):1342–1349

    Article  PubMed  Google Scholar 

  • Johnson RC (1977) The Spirochetes. Annu Rev Microbiol 31(1):89–106

    Article  CAS  PubMed  Google Scholar 

  • Joseph SJ, Hugenholtz P, Sangwan P, Osborne CA, Janssen PH (2003) Laboratory cultivation of widespread and previously uncultured soil bacteria. Appl Environ Microbiol 69(12):7210–7215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaeberlein T, Lewis K, Epstein SS (2002) Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296(5570):1127–1129

    Article  CAS  PubMed  Google Scholar 

  • Kasalicky V, Jezbera J, Hahn MW, Simek K (2013) The diversity of the Limnohabitans genus, an important group of freshwater bacterioplankton, by characterization of 35 isolated strains. PLoS One 8(3):e58209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasalicky V, Jezbera J, Simek K, Hahn MW (2010) Limnohabitans planktonicus sp nov and Limnohabitans parvus sp nov., planktonic betaproteobacteria isolated from a freshwater reservoir, and emended description of the genus Limnohabitans. Int J Syst Evol Microbiol 60:2710–2714

    Article  CAS  PubMed  Google Scholar 

  • Kell D, Kaprelyants A, Weichart D, Harwood C, Barer M (1998) Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie Van Leeuwenhoek 73(2):169–187

    Article  CAS  PubMed  Google Scholar 

  • Kenters N, Henderson G, Jeyanathan J, Kittelmann S, Janssen PH (2011) Isolation of previously uncultured rumen bacteria by dilution to extinction using a new liquid culture medium. J Microbiol Methods 84(1):52–60

    Article  PubMed  Google Scholar 

  • Kim H, Choo Y-J, Cho J-C (2007) Litoricolaceae fam. nov., to include Litoricola lipolytica gen. nov., sp. nov., a marine bacterium belonging to the order Oceanospirillales. Int J Syst Evol Microbiol 57(8):1793–1798

    Article  PubMed  Google Scholar 

  • Koch IH, Gich F, Dunfield PF, Overmann J (2008) Edaphobacter modestus gen. nov., sp. nov., and Edaphobacter aggregans sp. nov., acidobacteria isolated from alpine and forest soils. Int J Syst Evol Microbiol 58(5):1114–1122

    Article  CAS  PubMed  Google Scholar 

  • Köpke B, Wilms R, Engelen B, Cypionka H, Sass H (2005) Microbial diversity in coastal subsurface sediments: a cultivation approach using various electron acceptors and substrate gradients. Appl Environ Microbiol 71(12):7819–7830

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krebs CJ (1999) Ecological methodology, 2nd edn. Addison Wesley Longman, Menlo Park, CA

    Google Scholar 

  • Kunin V, Engelbrektson A, Ochman H, Hugenholtz P (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12(1):118–123

    Article  CAS  PubMed  Google Scholar 

  • Lesmana M, Rockhill RC, Sutanti D, Sutomo A (1985) An evaluation of alkaline peptone water for enrichment of Vibrio cholerae in feces. Southeast Asian J Trop Med Public Health 16(2):265–267

    CAS  PubMed  Google Scholar 

  • Makita H, Tanaka E, Mitsunobu S, Miyazaki M, Nunoura T, Uematsu K, Takaki Y, Nishi S, Shimamura S, Takai K (2017) Mariprofundus micogutta sp. nov., a novel iron-oxidizing zetaproteobacterium isolated from a deep-sea hydrothermal field at the Bayonnaise knoll of the Izu-Ogasawara arc, and a description of Mariprofundales ord. nov. and Zetaproteobacteria classis nov. Arch Microbiol 199:335–346

    Article  CAS  PubMed  Google Scholar 

  • Mannisto MK, Rawat S, Starovoytov V, Haggblom MM (2011) Terriglobus saanensis sp. nov., an acidobacterium isolated from tundra soil. Int J Syst Evol Microbiol 61(Pt 8):1823–1828

    Article  CAS  PubMed  Google Scholar 

  • Markowitz VM, Chen IMA, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang JH, Williams P, Huntemann M, Anderson I, Mavromatis K, Ivanova NN, Kyrpides NC (2012) IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res 40(D1):D115–D122

    Article  CAS  PubMed  Google Scholar 

  • Mira A, Ochman H, Moran NA (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17(10):589–596

    Article  CAS  PubMed  Google Scholar 

  • Moore LR, Rocap G, Chisholm SW (1998) Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393:464–467

    Article  CAS  PubMed  Google Scholar 

  • Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B (2011) How many species are there on earth and in the ocean? PLoS Biol 9(8):e1001127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori K, Yamaguchi K, Sakiyama Y, Urabe T, Suzuki K-I (2009) Caldisericum exile gen. nov., sp. nov., an anaerobic, thermophilic, filamentous bacterium of a novel bacterial phylum, Caldiserica phyl. nov., originally called the candidate phylum OP5, and description of Caldisericaceae fam. nov., Caldisericales ord. nov. and Caldisericia classis nov. Int J Syst Evol Microbiol 59(11):2894–2898

    Article  CAS  PubMed  Google Scholar 

  • Morris JJ, Kirkegaard R, Szul MJ, Johnson ZI, Zinser ER (2008) Facilitation of robust growth of Prochlorococcus colonies and dilute liquid cultures by “helper” heterotrophic bacteria. Appl Environ Microbiol 74(14):4530–4534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris RM, Rappe MS, Connon SA, Vergin KL, Siebold WA, Carlson CA, Giovannoni SJ (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420(6917):806–810

    Article  CAS  PubMed  Google Scholar 

  • Mullins TD, Britschgi TB, Krest RL, Giovannoni SJ (1995) Genetic comparisons reveal the same unknown bacterial lineages in Atlantic and Pacific bacterioplankton communities. Limnol Oceanogr 40(1):148–158

    Article  CAS  Google Scholar 

  • Muniesa M, Blanch AR, Lucena F, Jofre J (2005) Bacteriophages may bias outcome of bacterial enrichment cultures. Appl Environ Microbiol 71(8):4269–4275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75(1):14–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nocker A, Cheung CY, Camper AK (2006) Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J Microbiol Methods 67(2):310–320

    Article  CAS  PubMed  Google Scholar 

  • Oliver JD (2010) Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34(4):415–425

    Article  CAS  PubMed  Google Scholar 

  • Pace N, Stahl D, Lane D, Olsen G (1986) The analysis of natural microbial populations by ribosomal RNA sequences. In: Marshall KC (ed) Advances in microbial ecology, vol 9. Springer US, pp 1–55

    Google Scholar 

  • Page KA, Connon SA, Giovannoni SJ (2004) Representative freshwater bacterioplankton isolated from Crater Lake, Oregon. Appl Environ Microbiol 70(11):6542–6550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parte AC (2014) LPSN–list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42(D1):D613–D616

    Article  CAS  PubMed  Google Scholar 

  • Petri RJ (1887) Eine kleine Modification des Koch’schen Plattenverfahrens. Cntralbl Bakteriol Pasitenkunde 1:279–280

    Google Scholar 

  • Pham VH, Kim J (2012) Cultivation of unculturable soil bacteria. Trends Biotechnol 30(9):475–484

    Article  CAS  PubMed  Google Scholar 

  • Postgate JR, Hunter JR (1963) Acceleration of bacterial death by growth substrates. Nature 198(4877):273–273

    Article  CAS  PubMed  Google Scholar 

  • Puspita ID, Kamagata Y, Tanaka M, Asano K, Nakatsu CH (2012) Are uncultivated bacteria really uncultivable? Microbes Environ 27(4):356–366

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rappe MS, Connon SA, Vergin KL, Giovannoni SJ (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418(6898):630–633

    Article  CAS  PubMed  Google Scholar 

  • Reasoner DJ, Geldreich EE (1985) A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 49(1):1–7

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rippka R (1988) Isolation and purification of cyanobacteria. Methods Enzymol 167:3–27

    Article  CAS  PubMed  Google Scholar 

  • Roszak DB, Colwell RR (1987) Survival strategies of bacteria in the natural environment. Microbiol Rev 51(3):365–379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sait M, Davis KE, Janssen PH (2006) Effect of pH on isolation and distribution of members of subdivision 1 of the phylum Acidobacteria occurring in soil. Appl Environ Microbiol 72(3):1852–1857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sait M, Hugenholtz P, Janssen PH (2002) Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys. Environ Microbiol 4(11):654–666

    Article  CAS  PubMed  Google Scholar 

  • Sangwan P, Kovac S, Davis KE, Sait M, Janssen PH (2005) Detection and cultivation of soil Verrucomicrobia. Appl Environ Microbiol 71(12):8402–8410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schleifer KH (2004) Microbial diversity: facts, problems and prospects. Syst Appl Microbiol 27(1):3–9

    Article  PubMed  Google Scholar 

  • Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71(3):1501–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Westcott SL (2011) Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl Environ Microbiol 77(10):3219–3226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schut F, Devries EJ, Gottschal JC, Robertson BR, Harder W, Prins RA, Button DK (1993) Isolation of typical marine bacteria by dilution culture: growth, maintenance, and characteristics of isolates under laboratory conditions. Appl Environ Microbiol 59(7):2150–2160

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci U S A 103(32):12115–12120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155

    Google Scholar 

  • Stackebrandt E, Goebel BM (1994) A place for DNA–DNA reassociation and 16S ribosomal-RNA sequence-analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44(4):846–849

    Article  CAS  Google Scholar 

  • Staley JT, Konopka A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346

    Article  CAS  PubMed  Google Scholar 

  • Stevenson BS, Eichorst SA, Wertz JT, Schmidt TM, Breznak JA (2004) New strategies for cultivation and detection of previously uncultured microbes. Appl Environ Microbiol 70(8):4748–4755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194(16):4151–4160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stingl U, Tripp HJ, Giovannoni SJ (2007) Improvements of high-throughput culturing yielded novel SAR11 strains and other abundant marine bacteria from the Oregon coast and the Bermuda Atlantic Time Series study site. ISME J 1(4):361–371

    Article  CAS  PubMed  Google Scholar 

  • Swan BK, Tupper B, Sczyrba A, Lauro FM, Martinez-Garcia M, Gonzalez JM, Luo HW, Wright JJ, Landry ZC, Hanson NW, Thompson BP, Poulton NJ, Schwientek P, Acinas SG, Giovannoni SJ, Moran MA, Hallam SJ, Cavicchioli R, Woyke T, Stepanauskas R (2013) Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean. Proc Natl Acad Sci U S A 110(28):11463–11468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamaki H, Sekiguchi Y, Hanada S, Nakamura K, Nomura N, Matsumura M, Kamagata Y (2005) Comparative analysis of bacterial diversity in freshwater sediment of a shallow eutrophic lake by molecular and improved cultivation-based techniques. Appl Environ Microbiol 71(4):2162–2169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamaki H, Tanaka Y, Matsuzawa H, Muramatsu M, Meng X-Y, Hanada S, Mori K, Kamagata Y (2011) Armatimonas rosea gen. nov., sp. nov., of a novel bacterial phylum, Armatimonadetes phyl. nov., formally called the candidate phylum OP10. Int J Syst Evol Microbiol 61(6):1442–1447

    Article  PubMed  Google Scholar 

  • Tanaka T, Kawasaki K, Daimon S, Kitagawa W, Yamamoto K, Tamaki H, Tanaka M, Nakatsu CH, Kamagata Y (2014) A hidden pitfall in the preparation of agar media undermines microorganism cultivability. Appl Environ Microbiol 80(24):7659–7666

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thompson J, Pacocha S, Pharino C, Klepac-Ceraj V, Hunt D, Benoit J, Sarma-Rupavtarm R, Distel D, Polz M (2005) Genotypic diversity within a natural coastal bacterioplankton population. Science 307:1311–1313

    Article  CAS  PubMed  Google Scholar 

  • Tindall BJ, Kaempfer P, Euzeby JP, Oren A (2006) Valid publication of names of prokaryotes according to the rules of nomenclature: past history and current practice. Int J Syst Evol Microbiol 56:2715–2720

    Article  PubMed  Google Scholar 

  • Tindall BJ, Rosselló-Móra R, Busse H-J, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60(1):249–266

    Article  CAS  PubMed  Google Scholar 

  • Torsvik V, Goksøyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56(3):782–787

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tripp HJ, Kitner JB, Schwalbach MS, Dacey JWH, Wilhelm LJ, Giovannoni SJ (2008) SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452(7188):741–744

    Article  CAS  PubMed  Google Scholar 

  • Vancanneyt M, Schut F, Snauwaert C, Goris J, Swings J, Gottschal JC (2001) Sphingomonas alaskensis sp. nov., a dominant bacterium from a marine oligotrophic environment. Int J Syst Evol Microbiol 51(1):73–79

    Article  CAS  PubMed  Google Scholar 

  • Vartoukian SR, Palmer RM, Wade WG (2010) Strategies for culture of ‘unculturable’ bacteria. FEMS Microbiol Lett 309(1):1–7

    CAS  PubMed  Google Scholar 

  • Vergin KL, Tripp HJ, Wilhelm LJ, Denver DR, Rappe MS, Giovannoni SJ (2007) High intraspecific recombination rate in a native population of Candidatus Pelagibacter ubique (SAR11). Environ Microbiol 9(10):2430–2440

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe K, Komatsu N, Ishii Y, Negishi M (2009) Effective isolation of bacterioplankton genus Polynucleobacter from freshwater environments grown on photochemically degraded dissolved organic matter. FEMS Microbiol Ecol 67(1):57–68

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K, Komatsu N, Kitamura T, Ishii Y, Park H-D, Miyata R, Noda N, Sekiguchi Y, Satou T, Watanabe M, Yamamura S, Imai A, Hayashi S (2012) Ecological niche separation in the Polynucleobacter subclusters linked to quality of dissolved organic matter: a demonstration using a high sensitivity cultivation-based approach. Environ Microbiol 14(9):2511–2525

    Article  PubMed  Google Scholar 

  • Wilson KH, Blitchington RB (1996) Human colonic biota studied by ribosomal DNA sequence analysis. Appl Environ Microbiol 62(7):2273–2278

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yooseph S, Nealson KH, Rusch DB, McCrow JP, Dupont CL, Kim M, Johnson J, Montgomery R, Ferriera S, Beeson K, Williamson SJ, Tovchigrechko A, Allen AE, Zeigler LA, Sutton G, Eisenstadt E, Rogers Y-H, Friedman R, Frazier M, Venter JC (2010) Genomic and functional adaptation in surface ocean planktonic prokaryotes. Nature 468(7320):60–66

    Article  CAS  PubMed  Google Scholar 

  • Zengler K, Toledo G, Rappé M, Elkins J, Mathur EJ, Short JM, Keller M (2002) Cultivating the uncultured. Proc Natl Acad Sci U S A 99(24):15681–15686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zengler K, Walcher M, Clark G, Haller I, Toledo G, Holland T, Mathur EJ, Woodnutt G, Short JM, Keller M (2005) High-throughput cultivation of microorganisms using microcapsules. Methods Enzymol 397:124–130

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, Kamagata Y, Nakamura K (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53(4):1155–1163

    Article  CAS  PubMed  Google Scholar 

  • Zobell CE (1941) Studies on marine bacteria. I The cultural requirements of heterotrophic aerobes. J Mar Res 4:42–75

    Google Scholar 

  • Zwart G, Crump BC, Agterveld M, Hagen F, Han SK (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28(2):141–155

    Article  Google Scholar 

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Authors and Affiliations

  1. Research Department for Limnology, University of Innsbruck, Mondsee, Austria

    Martin W. Hahn, Ulrike Koll & Johanna Schmidt

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  1. Martin W. Hahn
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  2. Ulrike Koll
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  3. Johanna Schmidt
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Correspondence to Martin W. Hahn .

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  1. Cincinnati, OH, USA

    Christon J. Hurst

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This study was supported by the Austrian Science Fund (FWF) project 27160-B22 (Mikroevolution eines planktischen Süßwasserbakteriums).

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Martin W. Hahn declares that he has no conflict of interest. Ulrike Koll declares that she has no conflict of interest. Johanna Schmidt declares that she has no conflict of interest.

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

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Hahn, M.W., Koll, U., Schmidt, J. (2019). Isolation and Cultivation of Bacteria. In: Hurst, C. (eds) The Structure and Function of Aquatic Microbial Communities. Advances in Environmental Microbiology, vol 7. Springer, Cham. https://doi.org/10.1007/978-3-030-16775-2_10

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