Oxygen and the spatial structure of microbial communities

Biological Reviews

Volumn 83, Issue 4, 2008, Pages 553-569

  Fenchel, Tom ^a   Finlay, Bland ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Bacteria; Chemosensory behaviour; Meiofauna; Oxygen gradients; Oxygen requirements; Oxygen toxicity; Protozoa

Indexed keywords

HYDROXYL RADICAL; OXYGEN; PEROXIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

ACANTHAMOEBA CASTELLANII; AQUATIC ENVIRONMENT; CELL SIZE; DIFFUSION COEFFICIENT; ENDOSYMBIOSIS; ENERGY METABOLISM; MEIOFAUNA; MICROBIAL COMMUNITY; MICROBIAL RESPIRATION; NONHUMAN; OXYGEN CONSUMPTION; OXYGEN SENSING; OXYGEN TENSION; OXYGEN TOXICITY; OXYGEN TRANSPORT; PROTOZOON; REVIEW;

AEROBIOSIS; ANAEROBIOSIS; ANIMALS; ATMOSPHERE; ECOSYSTEM; GEOLOGIC SEDIMENTS; OXYGEN; OXYGEN CONSUMPTION;

ACANTHAMOEBA CASTELLANII; AMOEBA (GENUS); ANIMALIA; BACTERIA (MICROORGANISMS); CILIOPHORA; EUKARYOTA; METAZOA; PROKARYOTA; PROTISTA; PROTOZOA;

EID: 54849424343     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/j.1469-185X.2008.00054.x     Document Type: Review

References (103)

1. Alexandre, G., Greer-Phillis, S. Zhulin, I. B 2004). Ecological role of energy taxis in microorganisms. FEMS Microbiology Reviews 28, 113 126.
2. Aller, R. C 1983). The importance of the diffusive permeability of animal burrows linings in determining sediment chemistry. Journal of marine Research 41, 299 322.
3. Alongi, D. M 1985). Microbes, meiofauna and bacterial productivity in tubes constructed by the polychaete Capitella capitata. Marine Ecology Progress Series 23, 207 208.
4. Alve, E. Bernhard, J. M 1995). Vertical migratory response of benthic formaminifera to controlled oxygen concentrations in an experimental mesocosm. Marine Ecology Progress Series 116, 137 151.
5. Armitage, J. P 1997). Behavioural responses of bacteria to light and oxygen. Archives of Microbiology 168, 249 261.
6. Barbara, G. M. Mitchell, J. G 1996). Formation of a 30-40-micrometer- thick laminations by high-speed marine bacteria in microbial mats. Applied and Environmental Microbiology 62, 3985 3990.
7. Berg, H. C 1983). Random Walks in Biology. Princeton University Press, Princeton.
8. Bernard, C. Fenchel, T 1994). Chemosensory behaviour of Strombidium purpureum an anaerobic oligotrich ciliate with endosymbiotic purple nonsulfur bacteria. Journal of Eukaryotic Microbiology 41, 391 396.
9. Bernard, C. Fenchel, T 1996). Some microaerobic ciliates are facultative anaerobes. European Journal of Protistology 32, 293 297.
10. Bernard, C., Simpson, A. G. B. Patterson, D. J 2000). Some free-living flagellates (Protista) from anoxic habitats. Ophelia 52, 113 142.
11. Bernhard, J. M. Bowser, S. S 2008). Peroxisome proliferation in foramnifera inhabiting the chemocline: an adaptation to reactive oxygen species exposure? J. Eukaryote Microbiol. 55, 135 144.
12. Bernhard, J. M., Visscher, P. T. Bowser, S. S 2003). Sub-milimeter life positions of bactreia, protists, and metazoans in laminated sediments of the Santa Barbara Basin. Limnol. Oceanogr. 48 : 813 828.
13. Bilinski, T 1991). Oxygen toxicity and microbial evolution. BioSystems 24, 305 312.
14. Blackburn, N. Fenchel, T 1999a). Influence of bacteria, diffusion and shear on micro-scale nutrient patches, and implications for bacterial chemotaxis. Marine Biology Progress Series 189, 1 7.
15. Blackburn, N. Fenchel, T 1999b). Modelling of microbial patch encounter by chemotactic protozoa. Protist 150, 337 343.
16. Blakemore, R. P 1982). Magnetotactic bacteria. Annual Review of Microbiology 36, 217 238.
17. Canfield, D. E 2005). The early history of atmospheric oxygen: homage to Robert M. Garrels. Annual Review of Earth and Planetary Science 33, 1 36.
18. Crenshaw, H. C 1996). A new look on locomotion in microorganisms. American Zoologist 36, 608 618.
19. Cronkite, D. van den Brink, S 1981). The role of oxygen and light in guiding "photoaccumulation" in the Paramecium bursaria-Chlorella symbiosis. Journal of Experimental Zoology 217, 171 177
20. Dusenbery, D. B 1998). Spatial sensing of stimulus gradients can be superior to temporal sensing for free-swimming bacteria. Biophysical Journal 74, 2272 2277.
21. Edgecomb, V. P., Kysela, D. T., Teske, A., Gomez, de V., Sogin, M. L 2002). Benthic eukryotic diversity in the Guaymas Basin hydrothermal vent envirronmnet. PNAS 99, 7658 7662.
22. Engelmann, T. W 1881). Zur Biologie der Scizomyceten. Pflügers Archiv Gesamte Physiologie 26, 537 545.
23. Engelmann, T. W 1883). Bacterium photometricum: Ein Beitrag zur vergleichnende Physiologie und Farbensinnes. Archiev für Gesamte physiologie der Menchen und Tieres. Bonn, 30, 95 124.
24. Fenchel, T 1969). The ecology of marine microbenthos IV. Ophelia 6, 1 182.
25. Fenchel, T 1994). Motility and chemosensory behaviour of the sulphur bacterium Thiovulum majus. Microbiology 140, 3109 3116.
26. Fenchel, T 1996a). Worm burrows and oxic microniches in marine sediments. 1. Spatial and temporal scales. Marine Biology 127, 289 295.
27. Fenchel, T 1996b). Worm burrows and oxic microniches in marine sediments. 2. Distribution patterns of ciliated protozoa. Marine Biology 127, 297 301.
28. Fenchel, T. Bernard, C 1993). Endosymbiotic purple non-sulphur bacteria in an anaerobic ciliated protozoon. FEMS Microbiology Letters 110, 21 25.
29. Fenchel, T., Bernard, C., Esteban, G., Finlay, B. J., Hansen, P. J. Iversen, N 1995). Microbial diversity and activity in a Danish fjord with anoxic deep water. Ophelia 43, 45 100.
30. Fenchel, T. Bernard C 1996). Behavioural responses in oxygen gradients of ciliates from microbial mats. European Journal of Protistology 32, 55 63.
31. Fenchel, T. Blackburn, N 1999). Motile chemosensory behaviour of phagotrophic protists: mechanisms for and efficiency of congregating at food patches. Protist 150, 325 336.
32. Fenchel, T. Finlay, B. J 1984). Geotaxis in the ciliated protozoon Loxodes. Journal of experimental Biology 110, 17 33.
33. Fenchel T. Finlay, B. J 1986a). The structure and function of Müller vesicles in loxodid ciliates, Journal of Protozoology 33, 69 76.
34. Fenchel, Y. Finlay, B. J 1986b). Photobehavior of the ciliated protozoon Loxodes: taxic, transient, and kinetic responses in the presence and absence of oxygen. Journal of Protozoology 33, 139 145.
35. Fenchel, T. Finlay, B. J 1989). Kentrophoros: A mouthless ciliate with a symbiotic kitchen garden. Ophelia 30, 75 93.
36. Fenchel, T. Finlay, B. J 1990). Oxygen toxicity, respiration and behavioural responses to oxygen in free-living anaerobic ciliates. Journal of General Microbiology 136, 1953 1959.
37. Fenchel, T. Finlay, B. J 1995). Ecology and Evolution in Anoxic Worlds. Oxford University Press, Oxford.
38. Fenchel, T., Finlay, B. J. Giannì, A 1989). Microaerophily in ciliates: responses of an Euplotes species (Hypotrichida) to oxygen tension. Archiev für Protistenkunde 137, 317 330.
39. Fenchel, T. Glud, R 1998). Veil architechture in a sulphide-oxidizing bacterium enhances countercurrent flux. Nature 394, 367 369.
40. Fenchel, T. Thar, R 2004). "Candidatus Ovobacter propellens": a large conspicuous prokaryote with an unusual motility behaviour. FEMS Microbiology Ecology 48, 231 238.
41. Finlay, B. J 1981). Oxygen availability and seasonal migrations of ciliated protozoa in a freshwater lake. Journal of General Microbiology 123, 173 178.
42. Finlay, B. J 1985). Nitrate respiration by protozoa (Loxodes spp.) in the hypolimnetic nitrite maximum of a productive freshwater pond. Freshwater Biology 15, 333 346.
43. Finlay, B. J., Berninger, U. G., Stewart, L. J., Hindle, R. M. Davison, W 1987). Some factors controlling the distribution of two pond-dwelling ciliates with algal symbionts (Frontonia vernalis and Euplotes daidaleos). Journal of Protozoology 34, 349 356
44. Finlay, B. J. Esteban, G. F 1998). Planktonic ciliate species diversity as an integral component of ecosystem function in a freshwater pond. Protist 149, 155 165.
45. Finlay, B. J. Fenchel T 1986). Photosensivity in the ciliated protozoon Loxodes: pigment granules, absorption and action spectra, blue light perception and ecological significance. Journal of Protozoology 33, 534 542.
46. 2 toxicity in the freshwater ciliated protozoon Loxodes. Journal of Protozoology 33, 157 165.
47. Finlay, B. J., Maberly, S. C. Esteban, G 1996). Spectacular abundance of ciliates in anoxic pond water: contribution of symbiont photosynthesis to host respiratory oxygen requirements. FEMS Microbiology Ecology 20, 229 235.
48. Finlay, B. J., Maberly, S. C. Cooper, J. I 1997). Microbial diversity and ecosystem function. Oikos 80, 209 213.
49. Finlay, B. J., Span, A. S. W. Harman, J. M. P 1983). Nitrate respiration in primitive eukaryotes. Nature 303, 333 336.
50. Fisher, J. P. Cypionka, H 2006). Analysis of aerotactic band formation by Desulfovibrio desulfuricans in a stopped-flow diffusion chamber. FEMS Micobiology Ecology 55, 186 194.
51. Giere, O 1993). Meiobenthology. Springer-Verlag, Berlin
52. Giere, O., Liebezeit, G. Dawson, R 1982). Habitat conditions and distribution pattern of the gutess oligochaete Phallodrius leukodermatus. Marine Ecology Progress Series 8, 291 299.
53. + sensing. Trends Biochem. Sci. 9, 397 400.
54. Glud, R. N 2008). Oxygen dynamics of marine sediments. Marine Biology Research 4, 243 389.
55. 2- optode measuremets at benthic interfaces. Limnology and Oceanography 46, 2073 2080.
56. Gooday, A. J., Bernhard, J. M., Levin, L. A. Suhr, S. B 2000). Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas. Deep Sea Research Part II 47, 25 54.
57. Gonzales, C., Agapito, M. T., Rocher, A., Gonzales-Martib, M. C., Vega-Agapito, V., Gomez-Nino, A., Rigual, R., Casatafieda, J. Obeso, A 2007). Chemoreception in the context of the general biology of ROS. Respiratory Physiology & Neurobiology 157, 30 44.
58. Head, I. M., Gray, N. D., Babenzien, H. Glöckner, F. O 2000). Uncultured giant sulphur bacteria of the genus Achromatium. FEMS Mcrobiology Ecoogy 33, 171 180.
59. Hou, S., Larson, R. W., Boudko, D., Riley, C. W., Karatan, E., Ordal, G. W. Alam, M 2000). Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 403, 540 544.
60. Jennings, H. S 1906). Behavior of Lower Organisms. Bloomington, Indiana.
61. Jensen, P 1987). Differences in microhabitat, abundance and body size between oxybiotic and thiobiotic free-living marine nematodes. Oecologia (Berlin) 71, 564 567.
62. Jørgensen, B. B 1977). Bacterial sulphate reduction within rediced microniches of oxiized marine sediments. Marine Biology 41, 7 17.
63. Jørgensen, B. B 1982). Ecology of the bacteria of the sulphur cycle with special reference to anaoxic-oxic environments. Philosophical Transactions of the Royal Society London, B 298, 543 564.
64. Kamykowski, D. Zentara, S.-J 1990). Hypoxia in the world ocean as recorded in the historical data set. Deep Sea Res. 37, 219 241.
65. Klimant, I., Kühl, M., Glud. R. N. Holst, G 1997). Optical measurements of oxygen and temperature in microscale: strategies and biological applications. Sensors and Actuators B 38-39, 29 37.
66. Krieg, N. R. Hoffman, P. S 1986). Microaerophily and oxygen toxicity. Annual Review of Microbiology 40, 107 130.
67. Kühl, M., Rockelt, L. F. Thar, R 2007). Combined imaging of bacteria and oxygen in biofilms. Applied and Environmental Microbiology 73, 6289 6295.
68. Lane, N 2002). Oxygen. The Molecule that made the World. Oxford University Press, Oxford.
69. Levin, L. A 2003). Oxygen minimum zone benthos: adaptation and community response to hypozia. Ocenogr. Mar. Biol. Ann. Rev., 38, 219 241.
70. Lloyd, D., Williams J. M., Yarlett, N. Williams A. G 1982). Oxygen affinities of the hydrogenosome containing protozoa Tritrichomonmas foetus and Dasytrichia ruminantium and two aerobic protozoa determined by bacterial bioluminescence. Journal of General Microbiology 128, 1019 1022.
71. Macnab, R. M. Koshland, D. E 1972). The gradient-sensing mechanism in bacterial chemotaxis. Proceedings of the National Academy of Science, 69, 2509 2512.
72. Massaro, F. L 1980). Oxygen toxicity. American Journal of Medicine 69, 117 126.
73. Meyers, M. B., Fossing, H. Powell, E. N 1988). Movement of oxybiotic and thiobiotic meiofauna in response to changes in pore-water oxygen and sulfide gradients around macroinfaunal tubes. Marine Biology 98, 395 414.
74. Milsom, W. K. Burleson, M. L 2007). Peripheral arterial chemoreceptors and the evolution of the carotid body. Respiratory Physiology & Neurobiology 157, 4 11.
75. Møller, M. M., Nielsen, N. P. Jørgensen, B. B 1985). Oxygen responses and mat formation by Beggiatoa spp. Applied and Environmental Microbiology 50, 373 382.
76. Morris, J. G 1979). Nature of oxygen toxicity in anaerobic organisms. In Strategies of Microbial Life in Extreme Environments (ed. M Shilo pp. 149 162. Dahlem Conferences, Berlin.
77. Muyzer, G., Yildirim, Y., van Dongen, U., Kühl, M. Thar, R 2005). Indentification of "Candidatus Thioturbo danicus", a microaerophilic bacterium that builds conspicuous veils on sulfidic sediments. Applied and Environmental Microbiology 71, 8929 8933.
78. Nedwell, P. B. Gray, T. R. G 1987). Soils and sediments as materials for microbial growth. In Ecology of Microbial Communities (ed. M. Fletcher, T. R. G Gray J. G Jones pp. 21 54. Cambridge University Press, Cambridge.
79. Nelson, D. C., Revsbech, N. P. Jørgensen, B. B 1986). Microoxic-anoxic niche of Beggiatoa spp.: microelectrode survey of marine and freshwater strains. Applied and Environmental Microbiology 52, 161 168.
80. Ott, J. A. Novak, R 1989). Living at an interface: meiofauna at the oxygen/sulfide boundary of marine sediments. In Reproduction, Genetics and Distribution of Marine Organisms (ed. J. S. Ryland P. A. Tyler) pp. 415 422. Olsen & Olsen, Frederiksborg, Denmark.
81. Penard, E 1917). Le genre Loxodes. Revue Suisse de Zoologie 25, 453 489.
82. Ploug, H. Jørgensen, B. B 1999). A net-jet flow system for mass transfer and microsensor studies of sinking aggregates. Marine Ecology Progress Series 176, 279 290.
83. Preisler, A., De Beer, D., Lichtschlag, A., Lavik. G. Boetius, A. Jørgensen, B. B 2007). Biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment. The ISME Journal 1, 1 13.
84. Reise, K 1981). High abundance of small zoobenthos around biogenic structures in tidal sediments of the Waddensea. Helgoländer wissenschaftliche Meeresuntersuchungen 34, 413 425.
85. Revsbech, N. P. Jørgensen, B. B 1986). Microelectrodes: their use in microbial Ecology. Advances in Microbial Ecology 9, 293 352.
86. Risgaard-Petersen, N., Langezaal, A. M., Ingvardsen, S., Schmid, M. C., Jetten, M. S. M., Op den Camp, H. J. M, Derksen, J. W. M., Piña-Ochoa, E., Eriksson, S. P., Nielsen, L. P. Revsbech, N. P., Cedhagen, T. van der Zwaan, G. J 2006). Evidence for complete denitrification in a benthic foraminifer. Nature 443, 93 96.
87. Roberts, A. M 1970). Geotaxis in motile micro-organisms. Journal of Experimental Biology 53, 687 699.
88. Rodgers, K. R 1999). Heme-based sensors in biological systems. Current Opinion in Chemical Biology 3, 158 167.
89. Sass, A. M., Eschemann, A., Kühl, M., Thar, R., Sass, H. Cypionka, H 2002). Growth and chemosensory behaviour of sulphate-reducing bacteria in oxygen-sulfide gradients. FEMS Microbiology Ecology 40, 47 54.
90. Scherer, B 1985). Annual dynamics of a meiofauna community from the "sulphide layer" of a North Sea sand flat. Microfauna Marina 2, 117 161.
91. Schnitzer, M. J., Block, S. M., Berg, H. C. Purcell, E. M 1990). Strategies for chemotaxis. In Biology of the Chemotactic Response (ed. Armitage, J. P. Lackie, J. M. pp. 15 34. Cambridge University Press, Cambridge.
92. Scott, C., Lyons, T. W., Bekker, A., Shen, Y., Poulton, S. W., Chu, X. Anbar, A. D 2008). Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452, 456 459.
93. Semenza, G. L 2007). Life with oxygen. Science 318, 62 64.
94. Shioi, J., Chuan, V. D. Taylor, B. L 1987). Oxygen as attractant and repellent in bacterial chemotaxis. Journal of Bacteriology 169, 3118 3123.
95. Tachezy, J., Sánchez, L. B. Müller, M 2001). Mitochondrial type iron-sulfur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of IscS. Mol. Biol. Evol. 18, 1919 1928.
96. Taylor, B. L 1983). Role of proton motive force in sensory transduction in bacteria. Ann. Rev. Microbiol. 37, 551 573.
97. Thar, R. Fenchel, T 2001). True chemotaxis in oxygen gradients of the sulfur-oxidizing bacterium Thiovulum majus. Applied and Environmental Microbiology 67, 3299 3303.
98. Thar, R. Fenchel, T 2005). Survey of motile microaerophilic bacterial morphotypes in the oxygen gradient above a marine sulfidic sediment. Applied and Environmental Microbiology 71, 3682 3691.
99. Thar, R. Kühl, M 2001). Motility of Marichromatium gracile in response to light, oxygen, and sulphide. Applied and Environmental Microbiology 67, 5410 5419.
100. Thar, R. Kühl, M 2002). Conspicuous veils formed by vibrioid bacteria on sulfidic marine sediments. Applied and Environmental Microbiology 68, 6310 6320.
101. Thar, R. Kühl, M 2003). Bacteria are not too small for spatial sensing of chemical gradients: an experimental evidence. Proceedings of the National Academy of Science 100, 5748 5753.
102. Tyson, R. V. Pearson, T. H eds 1991). Modern and Ancient Continental Shelf Anoxia. The Geological Society, London.
103. Wetzel, M. A., Jensen, P. Giere, O 1995). Oxygen/sulfide regime and nematode fauna associated with Arenicola marina burrows: new insight in the thiobios case. Marine Biology 124, 3901 312.