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Distribution of ultramicrobacteria in a gulf coast estuary and induction of ultramicrobacteria

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Abstract

The abundance of ultramicrobacteria (i.e., bacteria that pass through a 0.2μm filter) in a subtropical Alabama estuary was determined during a 1-year period. Although phenotypic and molecular characterization indicated that the population of ultramicrobacteria was dominated byVibrio species, species ofListonella andPseudomonas were also abundant. Vibrios occurred with the greatest frequency in waters whose salinities were less than 14‰, and were the most abundant species of the total ultramicrobacterial population year-round, whilePseudomonas species were absent or considerably reduced during the winter months. The total number of ultramicrobacteria showed an inverse relationship to total heterotrophic bacteria as measured by colony-forming units (CFU)/ml and to water quality as measured by several parameters. Analysis by generic composition indicated that both salinity and temperature significantly affected the distribution of these organisms. Laboratory studies revealed that strains of vibrios under starvation in both static and continuous-flow microcosms could be induced to form cells that passed through 0.2 and/or 0.4μm filters. Cells exposed to low nutrients became very small; some grew on both oligotrophic (5.5 mg carbon/liter) and eutrophic (5.5 g carbon/liter) media; and some few cells grew only on oligotrophic media. By passing selected vibrio strains on progressively diluted nutrient media, cells were also obtained that were small, that passed through 0.4μm filters, and that could grow in oligotrophic media. These results suggest that ultramicrobacteria in estuaries (at least some portion of the population) may be nutrientstarved or low nutrient-induced forms of certain heterotrophic, eutrophic, autochthonous, estuarine bacteria.

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References

  1. American Public Health Association (1974) Standard methods for the examination of waters and waste waters, 14th ed. APHA, New York, New York

    Google Scholar 

  2. Amy PS, Morita RY (1983) Starvation-survival patterns of sixteen freshly isolated open-ocean bacteria. Appl Environ Microbiol 45:1109–1115

    Google Scholar 

  3. Baker RM, Singleton FL, Hood MA (1983) Effects of nutrient deprivation onVibrio cholerae. Appl Environ Microbiol 46:930–940

    PubMed  Google Scholar 

  4. Baumann P, Baumann L, Mandel M, Allen RD (1977) Taxonomy of marine bacteria:Beneckea nigrapulchrituda sp. nov. J Bacteriol 108:1380–1383

    Google Scholar 

  5. Baumann P, Bang SS, Baumann L (1978) Phenotypic characterization ofBeneckea anguillara biotypes I and II. Curr Microbiol 1:85–88

    Google Scholar 

  6. Bird R, Lark KG (1968) Initiation and termination of DNA replication after amino acid starvation ofE. coli 15T. Cold Spring Harbor Symposium on Quantitative Biology 33: 799–808

    Google Scholar 

  7. Black PM (1984) Prevention of food-borne disease caused byVibrio species. In: Colwell RR (ed) Vibrios in the environment. Wiley-Interscience, New York, pp 579–591

    Google Scholar 

  8. Buchanan RE, Gibbons NE (1974) Bergey's manual of determinative bacteriology, 9th ed. Williams and Wilkins, Baltimore

    Google Scholar 

  9. Colwell RR, Kaper J, Joseph SW (1977)Vibrio cholerae, Vibrio parahaemolyticus, and other vibrios: occurrence and distribution in Chesapeake Bay. Science 198:394–396

    PubMed  Google Scholar 

  10. D'Aoust JY, Kushner DJ (1972)Vibrio psycheroerythrus sp. nov.: classification of the psychrophilic marine bacterium, NRC 1004. J Bacteriol 111:340–342

    PubMed  Google Scholar 

  11. Davis CL, Koop KL, Muir DG, Robb FT (1983) Bacterial diversity in adjacent kelp-dominated ecosystems. Mar Ecol Prog Ser 13:115–119

    Google Scholar 

  12. Dawson MP, Humphrey BA, Marshall KC (1981) Adhesion: a tactic in the survival strategy of a marine vibrio during starvation. Curr Microbiol 6:195–199

    Google Scholar 

  13. Frazer AC, Curtis R III (1975) Production, properties, and utility of bacterial minicells. In: Current topics in microbiology and immunology, vol. 69. Springer-Verlag, New York, pp 1–84

    Google Scholar 

  14. Furniss AL, Lee JV, Donovan TJ (1978) The Vibrios. Public Health Laboratory Services Board. Monograph Series 11. HMSO, London, pp 1–58

    Google Scholar 

  15. Gilpin ML, Dale JW (1979) A rapid method for determining the base composition of DNA using unpurified bacterial extracts. Microbios Lett 12:31–35

    Google Scholar 

  16. Guelin AM, Mishustina IE, Andreev LV, Bobyk MA, Labina VA (1979) Some problems of the ecology and taxonomy of marine microvibrios. Biol Bull Acad Sci USSR 5:36–40

    Google Scholar 

  17. Harder W, Dijkhuizen L (1983) Physiological responses to nutrient limitation. Ann Rev Microbiol 37:1–23

    Google Scholar 

  18. Harwood CS (1978)Beneckea gazogenes sp. nov., a red, facultatively anaerobic marine bacterium. Curr Microbiol 1:233–238

    Google Scholar 

  19. Hickman FW, Farmer JJ III, Hollis DG, Fanning GR, Steigerwalt AG, Weaver RE, Brenner DJ (1982) Identification ofVibrio hollisae sp. nov. from patients with diarrhea. J Clin Microbiol 15:395–401

    PubMed  Google Scholar 

  20. Hobbie JE, Daley RS, Jasper S (1977) Use of nucleopore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33:1225–1228

    PubMed  Google Scholar 

  21. Hood MA, Ness GE, Rodrick GE, Blake NJ (1983) Ecology ofVibrio cholerae in two Florida estuaries. Microbiol Ecol 9:65–75

    Google Scholar 

  22. Hugh R, Leifson E (1953) The taxonomic significance of fermentative vs. oxidative metabolism of carbohydrates by various gram-negative bacteria. J Bacteriol 66:24–26

    PubMed  Google Scholar 

  23. Humphrey B, Kjelleberg B, Marshall KC (1983) Responses of marine bacteria under starvation conditions at solid-water interfaces. App Environ Microbiol 45:43–47

    Google Scholar 

  24. Jensen MJ, Tebo BM, Baumann P, Mandel M, Nealson KH (1980) Characterization ofAlteromonas hanedai (sp. nov.), a nonfermentative luminous species of marine origin. Curr Microbiol 3:311–315

    Google Scholar 

  25. Kalina GP, Somova AG, Podosinnikova LS, Grafova TI (1978)Allomonas, a new group of microorganisms of the family Vibrionaceae. Communication I. Method of study and preliminary results of differentiatingAllomonas fromAeromonas andVibrio (in Russian). Zhurnal Mikrobiologii, Epidimiologii, i Immunobiologii 57(1):40–46

    Google Scholar 

  26. Kalina GP, Nikonova VA, Grafova TI, Podosinnikova LS, Somova AG, Lapenkov MI (1979)Allomonas, a new group of the family Vibrionaceae. Communication III. Taxonomic analysis of similarity betweenAllomonas and the other genera of the family (in Russian). Zhurnal Mikrobiologii, Epidimiologii, i Immunobiologii 57(8): 16–21

    Google Scholar 

  27. Kjelleberg S, Humphrey BA, Marshall KC (1982) Effect of interfaces on small, starved marine bacteria. Appl Environ Microbiol 42:1166–1172

    Google Scholar 

  28. Kjelleberg S, Humphrey BA, Marshall KC (1983) Initial phases of starvation and activity of bacteria at surfaces. Appl Environ Microbiol 46:978–984

    Google Scholar 

  29. Krieg NR (1984) Bergey's manual of systematic bacteriology, vol. 1. Williams and Wilkins, Baltimore

    Google Scholar 

  30. MacDonell MT, Colwell RR (1985) Phylogeny of the Vibrionaceae and recommendation for two new genera,Listonella andShewanella. Syst Appl Microbiol 6:171–182

    Google Scholar 

  31. MacDonell MT, Hood MA (1982) Isolation and characterization of ultramicrobacteria from a Gulf Coast estuary. Appl Environ Microbiol 43:556–571

    Google Scholar 

  32. MacDonell MT, Hood MA (1984) Ultramicrovibrios in Gulf Coast estuarine waters: isolation, characterization, and incidence. In: Colwell RR (ed) Vibrios in the environment. Wiley-Interscience, New York, pp 551–562

    Google Scholar 

  33. MacDonell MT, Singleton FL, Roszak DB, Hood MA, Tison DL, Seidler RJ (1983) Rapid GC mol% screening of primary culture lysates using horizontal slab gel electrophoresis. J Microbiol Meth 1:81–88

    Google Scholar 

  34. Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3:208–218

    Google Scholar 

  35. Martin P, MacLoad RA (1984) Observation on the distinction between oligotrophic and eutrophic marine bacteria. Appl Environ Microbiol 47:1017–1022

    Google Scholar 

  36. Mishustina IE, Kameneva TG (1981) Bacterial cells of minimal sizes in the Barents Sea during the polar night. Mikrobiologiya 50:360–363

    Google Scholar 

  37. Morita RY (1982) Starvation-survival of heterotrophs in the marine environment. In: Marshall KC (ed) Advances in microbial ecology, vol. 6. Plenum Press, New York, pp 171–198

    Google Scholar 

  38. Nealson KH (1978) Isolation, identification, and manipulation of luminous bacteria. Meth Enzymol 432:153–166

    Google Scholar 

  39. Novitsky JA, Morita RY (1976) Morphological characterization of small cells resulting from nutrient starvation of a psychrophilic marine vibrio. Appl Environ Microbiol 32:617–622

    PubMed  Google Scholar 

  40. Novitsky JA, Morita RY (1977) Survival of a psychrophilic marine vibrio under long-term starvation. Appl Environ Microbiol 33:635–641

    Google Scholar 

  41. Novitsky JA, Morita RY (1978) Possible strategy for the survival of marine bacteria under starvation conditions. Mar Biol 48:289–295

    Google Scholar 

  42. Paul JH, Carlson DJ (1984) Genetic material in the marine environment: implication for bacterial DNA. Limnol Oceanogr 29:1091–1097

    Google Scholar 

  43. Poindexter JS (1981) Oligotrophy: fast and famine existence. In: Alexander M (ed) Advances in microbial ecology, vol. 5. Plenum Press, New York, pp 63–89

    Google Scholar 

  44. Reichardt W, Morita RY (1982) Survival stages of a psychrotrophicCytophaga johnsonae strain. Can J Microbiol 28:841–850

    Google Scholar 

  45. Schaechter M (1962) Patterns of cellular growth during unbalanced growth. Cold Spring Harbor symposium on quantitative biology 26:53–62

    Google Scholar 

  46. Schiewe MH, Trust TJ, Crosa JH (1981)Vibrio ordalii sp. nov.: a causative agent of vibriosis in fish. Curr Microbiol 6:343–348

    Google Scholar 

  47. Seidler RJ, Allen DA, Colwell RR, Joseph SW, Daily OP (1980) Biochemical characteristics and virulence of environmental Group F bacteria isolated in the United States. Appl Environ Microbiol 40:715–720

    PubMed  Google Scholar 

  48. Smith HL (1970) A presumptive test for vibrios: the “string test.” Bull WHO 42:817–818

    PubMed  Google Scholar 

  49. Tabor PS, Ohwada K, Colwell RR (1981) Filterable marine bacteria found in the deep sea: distribution, taxonomy, and response to starvation. Microbial Ecol 7:67–83

    Google Scholar 

  50. Tison DL, Seidler RJ (1981) Genetic relatedness of clinical and environmental isolates of lactose-positiveVibrio vulnificus. Curr Microbiol 58:371–380

    Google Scholar 

  51. Torella F, Morita RY (1981) Microcultural study of bacterial size changes and microcolony and ultramicrocolony formation by heterotrophic bacteria in seawater. Appl Environ Microbiol 41:518–527

    Google Scholar 

  52. Watson SW, Novitsky TJ, Quinby HL, Valois FW (1977) Determination of bacterial number and biomass in the marine environment. Appl Environ Microbiol 33:940–946

    PubMed  Google Scholar 

  53. Zeiger RS, Salomon R, Dignman CW, Peacock AC (1972) Role of base composition in the electrophoresis of microbial and crab DNA in polyacrylamide gels. Nature New Biol 238: 65–69

    PubMed  Google Scholar 

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  1. M. T. MacDonell

    Present address: Biotechnology Group, Idaho National Engineering Laboratory, P.O. Box 1625, 83415, Idaho Falls, ID, USA

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  1. Department of Biology, University of West Florida, 32514-5751, Pensacola, Florida, USA

    Mary A. Hood & M. T. MacDonell

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Hood, M.A., MacDonell, M.T. Distribution of ultramicrobacteria in a gulf coast estuary and induction of ultramicrobacteria. Microb Ecol 14, 113–127 (1987). https://doi.org/10.1007/BF02013017

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