Feeding selection of heterotrophic marine nanoflagellates based on the surface hydrophobicity of their picoplankton prey

Limnology and Oceanography

Volumn 44, Issue 8, 1999, Pages 1917-1927

  Monger, Bruce C ^a   Landry, Michael R ^b   Brown, Susan L ^b  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATOGRAPHY; HYDROPHOBICITY; PREDATION; UNITED STATES;

BACTERIUM; BACTERIVORY; FLAGELLATE; FOOD PREFERENCE; FOOD SELECTION; GRAZING; HYDROPHOBICITY; INTERSPECIFIC INTERACTION;

HAWAII; KANEOHE BAY; UNITED STATES;

ALOHA; BACTERIA (MICROORGANISMS); MASTIGOPHORA (FLAGELLATES); PROCHLOROCOCCUS; SYNECHOCOCCUS; TRIXIS;

EID: 0032738923     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.1999.44.8.1917     Document Type: Article

References (68)

1. ABSOLOM, D. R. 1988. The role of bacterial hydrophobicity in infection: Bacterial adhesion and phagocytic ingestion. Can. J. Microbiol. 34: 287-298.
2. _, D. W. FRANCIS, W. ZINGG, C. J. VAN OSS, AND A. W. NEUMANN. 1982. Phagocytosis of bacteria by platelets: Surface thermodynamics. J. Colloid Interface Sci. 85: 168-177.
3. _, F. V. LAMBERTI, Z. POLICOVA, W. ZINGG, C. J. VAN OSS AND W. NEUMANN. 1983. Surface thermodynamics of bacterial adhesion. Appl. Environ. Microbiol. 46: 90-97.
4. AZAM, F., T. FENCHEL, J. G. FIELD, J. S. GRAY, L. A. MEYER-REIL, AND F. THINGSTAD. 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10: 257-263.
5. BENNETT, S. J., R. W. SAUNDERS, AND K. G. PORTER. 1988. Chemosensory responses of heterotrophic and mixotrophic flagellates to potential food sources. Bull. Mar. Sci. 43: 764-771.
6. CAMPBELL, L., AND E. J. CARPENTER. 1986. Estimating the grazing pressure of heterotrophic nanoplankton on Synechococcus spp. using the sea water dilution and selective inhibitor techniques. Mar. Ecol. Prog. Ser. 33: 121-129.
7. _, H. A. NOLLA, AND D. VAULOT. 1994. The importance of Prochlorococcus to community structure in the central North Pacific Ocean. Limnol. Oceanogr. 39: 954-961.
8. CARON, D. A., J. C. GOLDMAN, O. K. ANDERSON, AND M. R. DENNETT. 1985. Nutrient cycling in a microflagellate food chain: II. Population dynamics and carbon cycling. Mar. Ecol. Prog. Ser. 24: 243-254.
9. CHRISTENSON, H. K. 1992. The long-range attraction between macroscopic hydrophobic surfaces, p. 29-51. In M. E. Schrader and G. Loeb [eds.], Modern approaches to wetability: Theory and application. Plenum.
10. CLARK, W. B., M. D. LANE, J. E. BEEM, S. L. BRAGG, AND T. T. WHEELER. 1985. Relative hydrophobicities of Actinomyces viscosus and Actinomyces naeslundii strains and their adsorption to saliva-treated hydroxyapatite. Infect. Immun. 47: 730-736.
11. DAHLBÄCK, B., M. HERMANSSON, S. KJELLEBERG, AND B. NORKRANS. 1981. The hydrophobicity of bacteria - an important factor in their initial adhesion at the air-water interface. Arch. Microbiol. 128: 267-270.
12. DAWSON, M. P., B. A. HUMPHREY, AND K. C. MARSHALL. 1981. Adhesion: A tactic in the survival strategy of a marine Vibrio during starvation. Curr. Microbiol. 6: 195-199.
13. EISEN, A., AND G. REID. 1989. Effects of culture media on Lactobacillus hydrophobicity and electrophoretic mobility. Microb. Ecol. 17: 17-25.
14. FENCHEL, T. 1982a. Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Mar. Ecol. Prog. Ser. 8: 225-231.
15. _. 1982b. Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as consumers of bacteria. Mar. Ecol. Prog. Ser. 9: 35-42.
16. _. 1984. Suspended marine bacteria as a food source, p. 301-315. In M. J. Fasham [ed.], Flow of material and energy in marine ecosystems. Plenum.
17. FITZPATRICK, J. A. 1972. Mechanisms of particle capture in water filtration. Ph.D. thesis, Harvard Univ.
18. GALDIERO, E., A. MARCATILI, G. DONNARUMMA, L. DE MARTINO, AND G. CIPOLLARO DE L'ERO. 1993. Correlation between changes in surface hydrophobicity and interaction of Streptococcus phyrogenes with human polymorphonuclear leukocytes after prolonged starvation in sea water. Res. Microbiol. 144: 609-616.
19. GOERICKE, R., AMD N. A. WELSCHMEYER. 1993. The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep-Sea Res. 40: 2283-2294.
20. GOLDMAN, J. C., AND D. A. CARON. 1985. Experimental studies on an omnivorous microflagellate: Implications for grazing and nutrient regeneration in the marine microbial food chain. Deep-Sea Res. 32: 899-915.
21. GURIJALA, K. R., AND M. ALEXANDER. 1990. Effect of growth rate and hydrophobicity on bacteria surviving protozoan grazing. Appl. Environ. Microbiol. 56: 1631-1635.
22. HERBLAND, A., A. LE BOUTEILLER, AND P. RAIMBAULT. 1985. Size structure of phytoplankton biomass in the equatorial Atlantic ocean. Deep-Sea Res. 32: 819-836.
23. HERMANSSON, M., S. KJELLEBERG, T. K. KORHONEN, AND T.-A. STENSTRÖM. 1982. Hydrophobic and electrostatic characterization of surface structures of bacteria and its relationship to adhesion to an air-water interface. Arch. Microbiol. 131: 308-312.
24. ISRAELACHVILI, J. N. 1985. Intermolecular and surface forces with applications to colloidal and biological systems. Academic.
25. _. 1987. Hydrophobic interactions, p. 101-113. In S. A. Safran and N. A. Clark [eds.], Physics of complex and supermolecular fluids. John Wiley and Sons.
26. _, AND P. M. MCGUIGGAN. 1988. Forces between surfaces in liquids. Science 241: 795-800.
27. _, AND R. PASHLEY. 1982. The hydrophobic interaction is long range, decaying exponentially with distance. Nature 300: 341-342.
28. JACQUET, S., J. F. LENNON, D. MARIE, AND D. VAULOT. 1998. Picoplankton population dynamics in coastal waters of the northwestern Mediterranean Sea. Limnol. Oceanogr. 43: 1916-1931.
29. JOHANNES, R. E. 1965. Influence of marine protozoa on nutrient regeneration. Limnol. Oceanogr. 10: 434-442.
30. JÜRGENS, K., AND H. GÜDE. 1994. The potential importance of grazing-resistant bacteria in planktonic systems. Mar. Ecol. Prog. Ser. 112: 69-188.
31. _, J. PARNTHALER, S. SCHALLA, AND R. AMANN. 1999. Morphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing. Appl. Environ. Microbiol. 65: 1241-1250.
32. KJELLEBERG, S., AND M. HERMANSSON. 1984. Starvation-induced effects on bacterial surface characteristics. Appl. Environ. Microbiol. 48: 497-503.
33. LANDRY, M. R., J. CONSTANTINOU, AND J. KIRSHTEIN. 1995. Microzooplankton grazing in the central tropical Pacific during February and August, 1992. Deep-Sea Res. 42: 657-671.
34. LANDRY, M. R., AND OTHERS. 1997. Iron and grazing constraints on primary production in the equatorial Pacific: An EqPac synthesis. Limnol. Oceanogr. 42: 405-418.
35. LEMKE, M. J., P. F. CHURCHILL, AND R. G. WETZEL. 1995. Effect of substrate and cell surface hydrophobicity on phosphate utilization in bacteria. Appl. Environ. Microbiol. 61: 913-919.
36. LETELIER, R. M., J. E. DORE, C. D. WINN, AND D. M. KARL. 1996. Seasonal and interannual variations in photosynthetic carbon assimilation at Station ALOHA. Deep-Sea Res. II 43: 467-490.
37. LI, W. K. W., D. V. SUBBA RAO, W. G. HARRISON, J. C. SMITH, J. J. CULLEN, B. IRWIN, AND T. PLATT. 1983. Autotrophic picoplankton in the tropical ocean. Science 219: 292-295.
38. MARÓDI, L., P. BURJÁN, AND F. ROZGONYI. 1990. Opsonic requirements and surface hydrophobicity of novobiocin-resistant, coagulase-negative Staphylococci. J. Med. Microbiol. 32: 19-24.
39. MCELDOWNEY, S., AND M. FLETCHER. 1986. Effect of growth conditions and surface characteristics of aquatic bacteria on their attachment to solid surfaces. J. Gen. Microbiol. 132: 513-523.
40. MONGER, B. C. 1993. The physical basis of prey capture by heterotrophic marine nanoflagellates. Ph.D. dissertation, Univ. Hawaii Manoa.
41. _, AND M. R. LANDRY. 1990. Direct-interception feeding by marine zooflagellates: The importance of surface forces and hydrodynamic forces. Mar. Ecol. Prog Ser. 65: 123-140.
42. _, AND _. 1991. Prey-size dependency of grazing by free-living marine flagellates. Mar. Ecol. Prog. Ser. 74: 239-248.
43. _, AND _. 1992. Size-selective grazing by heterotrophic nanoflagellates: An analysis using live-stained bacteria and dual-beam flow cytometry. Arch. Hydrobiol. Beih. 37: 173-185.
44. _, AND _. 1993. Flow cytometric analysis of marine bacteria using Hoechst 33342. Appl. Environ. Microbiol. 59: 905-911.
45. _, C. MCCLAIN, AND R. MURTUGUDDE. 1997. Seasonal phytoplankton dynamics in the Eastern Tropical Atlantic. J. Geophys. Res. 102: 12,389-12,411.
46. MURRAY, W., R. T. BARBER, M. R. ROMAN, M. P. BACON, AND R. A. FEELY. 1994. Physical and biological controls on carbon cycling in the equatorial Pacific. Science 266: 58-64.
47. NINHAM, B. W. 1980. Long-range vs. short-range forces. The present state of play. J. Phys. Chem. 84: 1423-1430.
48. PARNTHALER, J., T. POSCH, K. SIMEK, J. VRBA, R. AMANN, AND R. PSENNER. 1997. Contrasting bacterial strategies to coexist with a flagellate predator in an experimental microbial assemblage. Appl. Environ. Microbiol. 63: 569-601.
49. PARTENSKY, F., W. R. HESS, AND D. VAULOT. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance, Microbiol. Mol. Biol. Rev. 63: 106-127.
50. PASHLEY, R. M., P. M. MCGUIGGAN, B. W. NINHAM, AND D. F. EVANS. 1985. Attractive forces between uncharged hydrophobic surfaces: Direct measurements in aqueous solution. Science 229: 1088-1089.
51. PATTERSON, D. J., AND J. LARSEN. 1991. General introduction, p. 1-5. In D. J. Patterson and J. Larsen [eds.], The biology of free-living heterotrophic flagellates. Systematics Assoc. Special V. 45. Clarendon.
52. PLATT, T., D. V. SUBBA RAO, AND B. IRWIN. 1983. Photosynthesis of picoplankton in the oligotrophic ocean. Nature 301: 702-704.
53. ROSNER, B. 1982. Fundamentals of biostatistics. Duxbury.
54. SHERR, E. B., AND B. F. SHERR. 1994. Bacterivory and herbivory: Key roles of phagotrophic protists in pelagic food webs. Microb. Ecol. 28: 223-235.
55. SHIMETA, J., P. A. JUMARS, AND E. J. LESSARD. 1995. Influence of turbulence on suspension-feeding by protozoa - experiments in laminar shear fields. Limnol. Oceanogr. 40: 845-859.
56. SIBBALD, M. J., L. J. ALBRIGHT, AND P. R. SIBBALD. 1987. Chemosensory responses of a heterotrophic microflagellate to bacteria and several nitrogen compounds. Mar. Ecol. Prog. Ser. 36: 201-204.
57. SMYTH, C. J., P. JONSSON, E. OLSSON, O. SODERLIND, J. ROSENGREN, S. HJERTEN, AND T. WADSTROM. 1978. Differences in hydrophobic surface characteristics of porcine enteropathogenic Escherichia coli with or without K88 antigen as revealed by hydrophobic interaction chromatography. Infect. Immun. 22: 462-472.
58. STENSTRÖM, T. A. 1989. Bacterial hydrophobicity, an overall parameter for the measurement of adhesion potential to soil particles. Appl. Environ. Microbiol. 55: 143-147.
59. STRICKLAND, J. D. H., AND T. R. PARSONS. 1972. A practical handbook of seawater analysis. Fisheries Research Board of Canada.
60. TAYLOR, G. T., D. ZHENG, M. LEE, P. J. TROY, G. GYANANATH, AND S. K. SHARMA. 1997. Influence of surface properties on accumulation of conditioning films and marine bacteria on substrata exposed to oligotrophic waters. Biofouling 11: 31-57.
61. VAN HANNEN, E. J., M. VENINGA, J. BLOEM, H. J. GONS, AND H. J. LAANBROEK. 1999. Genetic changes in the bacterial community structure associated with protistan grazers. Arch. Hydrobiol. 145: 25-38.
62. VAN LOOSDRECHT, M. C. M., J. LYKLEMA, W. NORDE, G. SCHRAA, AND A. J. B. ZEHNDER. 1987. Electrophoretic mobility and hydrophobicity as a measure to predict the initial steps of bacterial adhesion. Appl. Environ. Microbiol. 53: 1898-1901.
63. VAN OSS, C. J. 1978. Phagocytosis as a surface phenomenon. Annu. Rev. Microbiol. 32: 19-39.
64. VAULOT, D., D. MARIE, R. J. OLSON, AND S. W. CHISHOLM. 1995. Growth of Prochlorococcus, a photosynthetic prokaryote, in the equatorial Pacific ocean. Science 268: 1480-1482.
65. YAMADA, S., AND A. MATSUMOTO. 1990. Surface properties of Staphylococcus aureus affecting chemiluminescence response of human phagocytes. Microbiol. Imunol. 34: 809-817.
66. YAMADA, T., N. MURAMATSU, AND T. KONDO. 1993. Phagocytosis of monosaccharide-binding latex particles by guinea-pig polymorphonuclear leucocytes. J. Biomat. Sci. Polymer Ed. 4: 347-355.
67. YASKOVICH, G. A., AND E. P. YAKOVLEVA. 1996. Strain-specific variations in the hydrophobicity of the bacterial cell surface. Microbiologia 65: 501-503.
68. ZANG, Y., AND R. M. MILLER. 1994. Effect of Pseudomonas rhamnolipid biosurfactant on cell hydrophobicity and biodegradation of octadecane. Appl. Environ. Microbiol. 60: 2101-2106.