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Physiological and Ecological Adaptations of Slow-Growing, Heterotrophic Microbes and Consequences for Cultivation

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Uncultivated Microorganisms

Part of the book series: Microbiology Monographs ((MICROMONO,volume 10))

Abstract

There is a large discrepancy between the number of microbes that can be visualized in samples from most natural environments and the small number that grows readily in the laboratory. This anomaly hinders opportunities to advance our understanding of the vast metabolic and evolutionary diversity of microbes, and imposes severe limitations on our capacity to link patterns of ecological diversity with the functioning of microbial communities. This chapter focuses on slow-growing, heterotrophic microbes as a potential source of cultures to represent the remarkable phylogenetic diversity of the microbial world. Despite the obvious advantages conferred upon microbes that leave the most progeny per unit time, chronic limitation of nutrients in many environments selects for microbes that are able to survive and use resources efficiently, even if it involves a trade-off for faster growth when resources are abundant. Understanding the ecological strategies of slow-growing microbes and adjusting expectations for cultivation to match the physiological capabilities of these microbes offer an opportunity to narrow the tremendous gap between the microscopically visible microbes and those that are readily cultivated.

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References

  • Alden L, Demoling F et al. (2001) Rapid method of determining factors limiting bacterial growth in soil. Appl Environ Microbiol 67(4):1830–1838

    Article  PubMed  CAS  Google Scholar 

  • Baath E (1998) Growth rates of bacterial communities in soils at varying pH: a comparison of the thymidine and leucine incorporation techniques. Microb Ecol 36(3):316–327

    Article  PubMed  CAS  Google Scholar 

  • Becker JM, Parkin T et al. (2006) Bacterial activity, community structure, and centimeter-scale spatial heterogeneity in contaminated soil. Microb Ecol 51(2):220–231

    Article  PubMed  Google Scholar 

  • Bloomfield S F, Stewart G et al. (1998)The viable but non-culturable phenomenon explained. Microbiology 144 (Part 1):1–3

    Article  PubMed  CAS  Google Scholar 

  • Brock TD (1966) Principles of microbial ecology. Prentice Hall, Englewood Cliffs, NJ

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Burns DG, Camakaris HM et al. (2004) Combined use of cultivation-dependent and cultivation-independent methods indicates that members of most haloarchaeal groups in an Australian crystallizer pond are cultivable. Appl Environ Microbiol 70(9):5258–5265

    Article  PubMed  CAS  Google Scholar 

  • Button DK (1985) Kinetics of nutrient-limited transport and microbial-growth. Microbiol Rev 49(3):270–297

    PubMed  CAS  Google Scholar 

  • Button DK (1994) The physical base of marine bacterial ecology. Microb Ecol 28(2):273–285

    Article  CAS  Google Scholar 

  • Button DK (1998) Nutrient uptake by microorganisms according to kinetic parameters from theory as related to cytoarchitecture. Microbiol Mol Biol Rev 62(3):636–645

    PubMed  CAS  Google Scholar 

  • Button DK, Schut F et al. (1993) Viability and isolation of marine-bacteria by dilution culture – theory, procedures, and initial results. Appl Environ Microbiol 59(3):881–891

    PubMed  CAS  Google Scholar 

  • Button DK, Robertson BR et al. (1996) Microflora of a subalpine lake: bacterial populations, size and DNA distributions, and their dependence on phosphate. FEMS Microbiol Ecol 21(2):87–101

    Article  CAS  Google Scholar 

  • Button DK, Robertson BR et al. (1998) A small, dilute-cytoplasm, high-affinity, novel bacterium isolated by extinction culture and having kinetic constants compatible with growth at ambient concentrations of dissolved nutrients in seawater. Appl Environ Microbiol 64(11):4467–4476

    PubMed  CAS  Google Scholar 

  • Button DK, Robertson B et al. (2004) Experimental and theoretical bases of specific affinity, a cytoarchitecture-based formulation of nutrient collection proposed to supercede the Michaels-Menten paradigm of microbial kinetics. Appl Environ Microbiol 70(9):5511–5521

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Coale KH, Johnson KS et al. (1996) A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean. Nature 383(6600):495–501

    Article  PubMed  CAS  Google Scholar 

  • Cole JJ, Findlay S et al. (1988) Bacterial production in fresh and saltwater ecosystems – a cross-system overview. Mar Ecol Prog Ser 43(1–2):1–10

    Article  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  PubMed  CAS  Google Scholar 

  • Davis KER, Joseph SJ et al. (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  PubMed  CAS  Google Scholar 

  • Dethlefsen L, Schmidt TM (2007) Performance of the translational apparatus varies with the ecological strategies of bacteria. J Bacteriol 189(8):3237–3245

    Article  PubMed  CAS  Google Scholar 

  • Eichorst SA, Breznak JA et al. (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  Google Scholar 

  • Fenchel T, King GM et al. (1998) Bacterial biogeochemistry: the ecophysiology of mineral cycling. Academic, San Diego, CA

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gans J, Wolinsky M et al. (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309(5739):1387–1390

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hahn MW, Stadler P et al. (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  PubMed  CAS  Google Scholar 

  • Hamaki T, Suzuki M et al. (2005) Isolation of novel bacteria and actinomycetes using soil-extract agar medium. J Biosci Bioeng 99(5):485–492

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto T, Hattori T (1989) Grouping of soil bacteria by analysis of colony formation on agar plates. Biol Fertil Soils 7(3):198–201

    Article  Google Scholar 

  • Hattori T, Mitsui H et al. (1997) Advances in soil microbial ecology and the biodiversity. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 72(1):21–28

    Article  CAS  Google Scholar 

  • Inoue K, Nishimura M et al. (2007) Separation of marine bacteria according to buoyant density by use of the density-dependent cell sorting method. Appl Environ Microbiol 73(4):1049–1053

    Article  PubMed  CAS  Google Scholar 

  • Janssen PH, Yates PS et al. (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  PubMed  CAS  Google Scholar 

  • Jassby AD, Platt T (1976) Mathematical formulation of relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21(4):540–547

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kalasinsky KS, Hadfield T et al. (2007) Raman chemical imaging spectroscopy reagentless detection and identification of pathogens: signature development and evaluation. Anal Chem 79(7):2658–2673

    Article  PubMed  CAS  Google Scholar 

  • Kirchman DL (1990) Limitation of bacterial-growth by dissolved organic-matter in the sub-arctic Pacific. Mar Ecol Prog Ser 62(1–2):47–54

    Article  CAS  Google Scholar 

  • Kirchman DL, Meon B et al. (2001) Glucose fluxes and concentrations of dissolved combined neutral sugars (polysaccharides) in the Ross Sea and Polar Front Zone, Antarctica. Deep-Sea Res. II. Topical Stud Oceanogr 48(19–20):4179–4197

    Article  CAS  Google Scholar 

  • Klappenbach JA, Dunbar JM et al. (2000) rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol 66(4):1328–1333

    Article  PubMed  CAS  Google Scholar 

  • Koch AL (1997) Microbial physiology and ecology of slow growth. Microbiol Mol Biol Rev 61(3):305–318

    PubMed  CAS  Google Scholar 

  • Koch AL (2001) Oligotrophs versus copiotrophs. BioEssays 23:657–661

    Article  PubMed  CAS  Google Scholar 

  • Leadbetter JR (2003) Cultivation of recalcitrant microbes: cells are alive, well and revealing their secrets in the 21st century laboratory. Curr Opin Microbiol 6(3):274–281

    Article  PubMed  CAS  Google Scholar 

  • Lovley DR, Klug MJ (1982) Intermediary metabolism of organic-matter in the sediments of a utrophic lake. Appl Environ Microbiol 43(3):552–560

    PubMed  CAS  Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, NJ

    Google Scholar 

  • Martin JH, Fitzwater SE (1988) Iron-deficiency limits phytoplankton growth in the northeast Pacific subarctic. Nature 331(6154):341–343

    Article  CAS  Google Scholar 

  • Mitsui H, Gorlach K et al. (1997) Incubation time and media requirements of culturable bacteria from different phylogenetic groups. J Microbiol Methods 30(2):103–110

    Article  CAS  Google Scholar 

  • Morris RM, Rappe MS et al. (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420(6917):806–810

    Article  PubMed  CAS  Google Scholar 

  • Naumann D, Helm D et al. (1991) Microbiological characterizations by FT-IR spectroscopy. Nature 351(6321):81–82

    Article  PubMed  CAS  Google Scholar 

  • Nystrom T (2001) Not quite dead enough: on bacterial life, culturability, senescence, and death. Arch Microbiol 176(3):159–164

    Article  PubMed  CAS  Google Scholar 

  • Park HS, Schumacher R et al. (2005) New method to characterize microbial diversity using flow cytometry. J Ind Microbiol Biotechnol 32(3):94–102

    Article  PubMed  CAS  Google Scholar 

  • Parkin TB, Brock TD (1980) Photosynthetic bacterial production in lakes – the effects of light-intensity. Limnol Oceanogr 25(4):711–718

    Article  Google Scholar 

  • Poindexter JS (1981) Oligotrophy – fast and famine existence. Adv Microb Ecol 5:63–89

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rosenstock B, Simon M (2001) Sources and sinks of dissolved free amino acids and protein in a large and deep mesotrophic lake. Limnol Oceanogr 46(3):644–654

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sangwan P, Kovac S et al. (2005) Detection and cultivation of soil verrucomicrobia. Appl Environ Microbiol 71(12):8402–8410

    Article  PubMed  CAS  Google Scholar 

  • Schoenborn L, Yates PS et al. (2004) Liquid serial dilution is inferior to solid media for isolation of cultures representative of the phylum-level diversity of soil bacteria. Appl Environ Microbiol 70(7):4363–4366

    Article  PubMed  CAS  Google Scholar 

  • Schut F, Devries EJ et al. (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

    PubMed  CAS  Google Scholar 

  • Schut F, Prins RA et al. (1997) Oligotrophy and pelagic marine bacteria: facts and fiction. Aquat Microb Ecol 12(2):177–202

    Article  Google Scholar 

  • Sessitsch A, Weilharter A et al. (2001) Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Appl Environ Microbiol 67(9):4215–4224

    Article  PubMed  CAS  Google Scholar 

  • Seymour JR, Mitchell JG et al. (2004) Microscale heterogeneity in the activity of coastal bacterioplankton communities. Aquat Microb Ecol 35(1):1–16

    Article  Google Scholar 

  • Smith EM, Prairie YT (2004) Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnol Oceanogr 49(1):137–147

    Article  CAS  Google Scholar 

  • Sogin ML, Morrison HG et al. (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103(32):12115–12120

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stevenson BS, Schmidt TM (2004) Life history implications of rRNA gene copy number in Escherichia coli. Appl Environ Microbiol 70(11):6670–6677

    Article  PubMed  CAS  Google Scholar 

  • Stevenson BS, Eichorst SA et al. (2004) New strategies for cultivation and detection of previously uncultured microbes. Appl Environ Microbiol 70(8):4748–4755

    Article  PubMed  CAS  Google Scholar 

  • Tempest DW, Neijssel OM et al. (1983) Properties and performance of microorganisms in laboratory culture: their relevance to growth in natural ecosystems. Symp Soc Gen Microbiol 34:119–152

    Google Scholar 

  • Tilman D (1981) Tests of resource competition theory using four species of Lake Michigan algae. Ecology 62(3):802–815

    Article  Google Scholar 

  • Torsvik V, Daae FL et al. (1998) Novel techniques for analysing microbial diversity in natural and perturbed environments. J Biotechnol 64(1):53–62

    Article  PubMed  CAS  Google Scholar 

  • Vancanneyt M, Schut F et al. (2001) Sphingomonas alaskensis sp nov., a dominant bacterium from a marine oligotrophic environment. Int J Syst Evol Microbiol 51:73–80

    PubMed  CAS  Google Scholar 

  • Vargha M, Takats Z et al. (2006) Optimization of MALDI-TOF MS for strain level differentiation of Arthrobacter isolates. J Microbiol Methods 66(3):399–409

    Article  PubMed  CAS  Google Scholar 

  • Vives-Rego J, Lebaron P et al. (2000) Current and future applications of flow cytometry in aquatic microbiology. FEMS Microbiol Rev 24(4):429–448

    Article  PubMed  CAS  Google Scholar 

  • Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647

    Article  PubMed  CAS  Google Scholar 

  • Watve M, Shejval V et al. (2000) The ‘K’ selected oligophilic bacteria: a key to uncultured diversity? Curr Sci 78(12):1535–1542

    Google Scholar 

  • Whitman WB, Coleman DC et al. (1998) Prokaryotes: the unseen majority. PNAS 95(12):6578–6583

    Article  PubMed  CAS  Google Scholar 

  • Yokokawa T, Nagata T et al. (2004) Growth rate of the major phylogenetic bacterial groups in the Delaware estuary. Limnol Oceanogr 49(5):1620–1629

    Article  Google Scholar 

  • Zengler K, Toledo G et al. (2002) Cultivating the uncultured. PNAS 99(24):15681–15686

    Article  PubMed  CAS  Google Scholar 

  • Zhou JZ, Xia BC et al. (2002) Spatial and resource factors influencing high microbial diversity in soil. Appl Environ Microbiol 68(1):326–334

    Article  PubMed  CAS  Google Scholar 

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Schmidt, T.M., Konopka, A.E. (2009). Physiological and Ecological Adaptations of Slow-Growing, Heterotrophic Microbes and Consequences for Cultivation. In: Epstein, S. (eds) Uncultivated Microorganisms. Microbiology Monographs, vol 10. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-85465-4_11

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