Resource seeking strategies of zoosporic true fungi in heterogeneous soil habitats at the microscale level

Soil Biology and Biochemistry

Volumn 45, Issue , 2012, Pages 79-88

  Gleason, Frank H ^a   Crawford, John W ^a   Neuhauser, Sigrid ^b   Henderson, Linda E ^a   Lilje, Osu ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

Adaptations to soil environment; Chytrids; Soil structure; Three dimensional visualisation; Zoosporic true fungi

Indexed keywords

ADHESION TO SUBSTRATE; CHYTRIDS; ENVIRONMENTAL SAMPLE; FRESHWATER ECOSYSTEM; HETEROGENEOUS SOILS; MICROSCALE LEVELS; MOLECULAR TECHNIQUES; PHYSICAL CHARACTERISTICS; PRECISE METHOD; RAPID GROWTH; SOIL ENVIRONMENT; SOIL HABITATS; SOIL STRUCTURE; SPECIFIC ADAPTATIONS; TEMPORAL GRADIENTS; THREE DIMENSIONAL SPACE; THREE-DIMENSIONAL STRUCTURE;

ADHESION; FUNGI; MICROORGANISMS; SOILS; THREE DIMENSIONAL; VISUALIZATION;

ECOSYSTEMS;

ADAPTATION; FUNGUS; GROWTH RATE; HETEROGENEITY; MOLECULAR ANALYSIS; NUTRITIONAL REQUIREMENT; PHYSICAL PROPERTY; RESOURCE AVAILABILITY; SOIL ECOSYSTEM; SOIL MICROORGANISM; SOIL STRUCTURE; SPORE; VISUALIZATION;

FUNGI;

EID: 81155148587     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2011.10.011     Document Type: Review

References (109)

1. Bärlocher F., Brendelberger H. Clearance of aquatic hyphomycete spores by a benthic suspension feeder. Limnology and Oceanography 2004, 49:2292-2296.
2. Baker K., Langenheder S., Nicol G., Ricketts D., Killham K., Campbell C., Prosser J. Environmental and spatial characterisation of bacterial community composition in soil to inform sampling strategies. Soil Biology and Biochemistry 2009, 41:2292-2298.
3. Barr D.J.S. Studies on Rhizophydium and Phlyctochytrium (Chytridiales). I. Comparative morphology. Canadian Journal of Botany 1969, 47:991-997.
4. Barr D.J.S. Studies on Rhizophydium and Phlyctochytrium (Chytridiales). II. Comparative physiology. Canadian Journal of Botany 1969, 47:999-1005.
5. Barr D.J.S. Phlyctochytrium reinboldtae (Chytridiales): morphology and physiology. Canadian Journal of Botany 1970, 48:479-484.
6. Barr D.J.S. The classification of Spizellomyces, Gaertneriomyces, Triparticalcar, and Kochiomyces (Spizellomycetales, Chytridiomycetes). Canadian Journal of Botany 1984, 62:1171-1201.
7. Barr D.J.S. Isolation, culture and identification of Chytridiales, Spizellomycetales and Hyphochytriales. Zoosporic Fungi in Teaching and Research 1987, 118-120. Southeastern Publishing Corporation, Athens, GA. M.S. Fuller, A. Jaworski (Eds.).
8. Barr D.J.S. 5. Chytridiomycota. The Mycota, Part A 2001, vol. VII:93-112. Springer-Verlag, New York, NY.
9. Barstow W.E., Pommerville J. The ultrastructure of cell wall formation and of gamma particles during encystment of Allomyces macrogynus zoospores. Archives of Microbiology 1980, 128:179-189.
10. Beakes G.W., Canter H.M., Jaworski G.H.M. Comparative ultrastructural ontogeny of zoosporangia of Zygorhizidium affluens and Z. planktonicum, chytrid parasites of the diatom Asterionellla formosa. Mycological Research 1992, 96:1047-1059.
11. Bernstein L.B. A biosystematic study of Rhizophlyctis rosea with emphasis on zoospore variability. Journal of the Elisha Mitchell Scientific Society 1968, 84:84-93.
12. Bonkowski M. Protozoa and plant growth: the microbial loop in soil revisited. New Phytologist 2004, 162:617-631.
13. Bostick L.R. Studies of the morphology of Chytriomyces hyalinus. Journal of the Elisha Mitchell Scientific Society 1968, 84:94-99.
14. Cantino E.C., Mills G.L. 12. Form and function in chytridiomycete spores, with emphasis upon Blastocladiella emersonii. The Fungal Spore, Form and Function 1976, 501-557. John Wiley & Sons, New York. D.J. Weber, W.M. Hess (Eds.).
15. Carson J.K., Gonzalez-Quinones V., Murphy D.V., Hinz C., Shaw J.A., Gleeson D.B. Low pore connectivity increases bacterial diversity in soil. Applied and Environmental Microbiology 2010, 76:3936-3942.
16. Couch J.N. Technic for collection, isolation and culture of chytrids. Journal of the Elisha Mitchell Scientific Society 1939, 55:208-214.
17. Czeczuga B., Muszyńska E. Aquatic zoosporic fungi from baited spores of cryptogams. Fungal Diversity 2004, 16:11-22.
18. Davies D.R., Theodorou M.K., Brooks A.E., Trinci A.P.J. Influence of drying on the survival of anaerobic fungi in rumen digesta and faeces of cattle. FEMS Microbiology Letters 1993, 106:59-64.
19. Deacon J.W., Saxena G. Oriented zoospore attachment and cyst germination in Catenaria anguillulae, a facultative endoparasite of nematodes. Mycological Research 1997, 101:513-522.
20. Deacon L.J., Grinev D.V., Crawford J.W., Harris J., Ritz K., Young I.M. Simultaneous preservation of soil structural properties and phospholipid profiles: a comparison of three drying techniques. Pedosphere 2008, 18:284-287.
21. Dessaux Y., Hinsinger P., Lemanceau P. Rhizosphere: so many achievements and even more challenges. Plant and Soil 2009, 312:1-3.
22. Digby A.L., Gleason F.H., McGee P.A. Some fungi in the Chytridiomycota can assimilate both inorganic and organic sources of nitrogen. Fungal Ecology 2010, 3:261-266.
23. Dix N.J., Webster J. Fungal Ecology 1995, Chapman & Hall, London.
24. Dogma I.J. Isolation and pure culture techniques for monocentric chytridiomycetes. Nova Hedwigia 1973, 24:379-392.
25. Evans T.A., Dawes T.K., Ward P.R., Lo N. Ants and termites increase crop yield in a dry climate. Nature Communications 2011, 2:262. 10.1038/ncomms1257.
26. Feeney D.S., Crawford J.W., Daniell T., Halllet P.D., Nunan N., Ritz K., Rivers M., Young I.M. Three-dimensional microorganization of the soil-root-microbe system. Microbial Ecology 2006, 52:151-158.
27. Feltham D.L., Chaplain M.A.J., Young I.M., Crawford J.W. A mathematical analysis of a minimal model of nematode migration in soil. Journal of Biological Systems 2002, 10:15-32.
28. Freeman K.R., Martin A.P., Karki D., Lynch R.C., Mitter M.S., Meyer M.S., Longcore J.E., Simmons D.R., Schmidt S.K. Evidence that chytrids dominate fungal communities at high-elevation soils. Proceedings of the National Academy of Sciences 2009, 106:18315-18320.
29. Gleason F.H., Letcher P.M., McGee P.A. Some aerobic Blastocladiomycota and Chytridiomycota can survive but cannot grow under anaerobic conditions. Australasian Mycologist 2007, 26:57-64.
30. Gleason F.H., Kagami M., Lefèvre E., Sime-Ngando T. The ecology of chytrids in aquatic ecosystems: roles in food web dynamics. Fungal Biology Reviews 2008, 2:17-25.
31. Gleason F.H., Lilje O. Structure and function of fungal zoospores: ecological implications. Fungal Ecology 2009, 2:53-59.
32. Gleason F.H., Schmidt S.K., Marano A.V. Can zoosporic true fungi grow or survive in extreme or stressful environments?. Extremophiles 2010, 14:417-425.
33. Gleason F.H., Marano A.V., Johnson P., Martin W.W. Blastocladian parasites of invertebrates. Fungal Biology Reviews 2010, 24:56-67.
34. Gleason F.H., Marano A.V., Digby A.L., Al-Shugairan N., Lilje O., Steciow M.M., Barrera M.D., Inaba S., Nakagiri A. Patterns of utilization of different carbon sources by some Chytridiomycota. Hydrobiologia 2011, 659:55-64.
35. Goldstein S. Degradation of pollen by phycomycetes. Ecology 1960, 41:543-545.
36. Grose M.J., Gilligan C.A., Spencer D., Goddard B.V.D. Spatial heterogeneity of soil water around single roots: use of CT-scanning to predict fungal growth in the rhizosphere. New Phytologist 1996, 133:261-272.
37. Gutman J., Zarka A., Boussiba S. The host-range of Paraphysoderma sedebokerensis, a chytrid that infects Haematococcus fluvialis. European Journal of Phycology 2009, 44:509-514.
38. Hallett P.D., Feeney D.S., Bengough A.G., Rillig M.C., Scrimgeour C.M., Young I.M. Disentangling the impact of AM fungi versus roots on soil structure and water transport. Plant and Soil 2009, 314:183-196.
39. Hansel C.M., Fendorf S., Jardine P.M., Francis C.A. Changes in bacterial and archael community structure and functional diversity along a geochemically variable soil profile. Applied and Environmental Microbiology 2008, 74:1620-1633.
40. Hapca S.M., Budha P., Crawford J.W., Young I.M. Movement of the nematode, Phasmarhabditis hermaphrodita, in a structurally heterogeneous environment. Nematology 2007, 9:731-738.
41. Hartwright L.M., Hunter P.J., Walsh J.A. A comparison of Olpidium isolates from a range of host plants using internal transcribed spacer sequence analysis and host range studies. Fungal Biology 2010, 114:26-33.
42. Held A.A. Attraction and attachment of zoospores of the parasitic chytrid Rozellla allomyces in response to host-dependent factors. Archives of Microbiology 1974, 95:97-114.
43. Held A.A. Rozella and Rozellopsis: naked endoparasitic fungi which dress-up as their hosts. Botanical Review 1981, 47:451-515.
44. Hinsinger P., Bengough A.G., Vetterlein D., Young I.M. Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant and Soil 2009, 321:117-152.
45. Hoffland E., Giesler R., Jongman A.G., van Breemen N. Feldspar tunneling by fungi along natural productivity gradients. Ecosystems 2003, 6:739-745.
46. James T.Y., Letcher P.M., Longcore J.E., Mozley-Standridge S.E., Porter D., Powell M.J., Griffith G.W., Vilgalys R. A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 2006, 98:860-871.
47. Jobard M., Rasconi S., Sime-Ngando T. Fluorescence in situ hybridization of uncultured zoosporic fungi: testing with clone-FISH and application to freshwater samples using CARD-FISH. Journal of Microbiological Methods 2010, 83:236-243.
48. Joblin K.N. Physical disruption of plant fibre by rumen fungi of the Sphaeromonas group. The Role of Protozoa and Fungi in Ruminant Digestion 1989, 259-260. Penambul Books, Armidale, NSW. J.V. Nolan, R.A. Leng, D.I. Demeyer (Eds.).
49. Jones D.L., Nguyen C., Finlay R.D. Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant and Soil 2009, 321:5-33.
50. Jones M.D.M., Forn I., Gadelha C., Egan M.J., Bass D., Massana R., Richards T.A. Discovery of novel intermediate forms redefines the fungal tree of life. Nature 2011, 474:200-203.
51. Karling J.S. Parasitism among the chytrids. American Journal of Botany 1942, 29:24-35.
52. Kagami M., de Bruin A., Ibelings B.W., van Donk E. Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 2007, 578:113-129.
53. Koch W.J. Studies with the motile cells of chytrids. IV. Planonts in the experimental taxonomy of aquatic phycomycetes. Journal of the Elisha Mitchell Scientific Society 1968, 84:69-83.
54. Kropp D.L., Harold M.H. Selective transport of nutrients via the rhizoids of the water mold Blastocladiella emersonii. Journal of Bacteriology 1982, 151:429-437.
55. Lara E., Moreira D., Lopez-Garcia P. The environmental clade LKM11 and Rozella from the deepest branching clade of fungi. Protist 2010, 161:116-121.
56. Lee E.-J. Chytrid distribution in diverse boreal Manitoba sites. Korean Journal of Biological Sciences 2000, 4:57-62.
57. Lefèvre E., Bardot C., Noel C., Carrias J.-F., Viscogliosi E., Amblard C., Sime-Ngando T. Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environmental Microbiology 2007, 9:61-71.
58. Letcher P.M., Powell M.J. Distribution of zoosporic fungi in forest soils of the Blue Ridge and Appalachian Mountains of Virginia. Mycologia 2001, 93:1029-1041.
59. Letcher P.M., Powell M.J. Frequency and distribution patterns of zoosporic fungi from moss-covered and exposed forest soils. Mycologia 2002, 94:761-771.
60. Liggenstoffer A.S., Youssef N.H., Couger M.B., Elshahed M.S. Phylogenetic diversity and community structure of anaerobic gut fungi (phylum Neocallimastigomycota) in ruminant and non-ruminant herbivores. The ISME Journal 2010, 4:1225-1235.
61. Lilje O., Lilje E. Fluctuation in Rhizophydium sp. (AUS 6) zoospore production and biomass during colony formation. Australasian Mycologist 2008, 27:20-32.
62. Lozupone C.A., Klein D.A. Molecular and cultural assessment of chytrid and Spizellomyces populations in grassland soils. Mycologia 2002, 94:411-420.
63. Machlis L. Zoospore chemotaxis in the watermold Allomyces. Physiologia Plantarum 1969, 22:126-139.
64. Marano A.V., Gleason F.H., Barrera M.D., Steciow M.M., Daynes C.N., McGee P.A. Rhizophlyctis rosea in soil: frequency, abundance and density of colonization of baits under different temperature treatments in the laboratory. Nova Hedwigia 2011, 93:73-84.
65. Midgley D.J., Letcher P.M., McGee P.A. Access to organic and insoluble sources of phosphorus varies among soil Chytridiomycota. Archives of Microbiology 2006, 186:211-217.
66. Mitchell R.T., Deacon J.W. Selective accumulation of zoospores of Chytridiomycetes and Oomycetes on cellulose and chitin. Transactions British Mycological Society 1986, 86:219-223.
67. Mooney S.J., Morris C., Berry P.M. Visualization and quantification of the effects of cereal root lodging on three-dimensional soil macrostructure using X-ray computed tomography. Soil Science 2006, 171:706-718.
68. Moss A.S., Reddy N.S., Dortaj I.M., San Francisco M.J. Chemotaxis of the amphibian pathogen Batrachochytrium dendrobatidis and its response to a variety of attractants. Mycologia 2008, 100:1-5.
69. Nikolcheva L.G., Bärlocher F. Taxon-specific fungal primers reveal unexpectedly high diversity during leaf decomposition in a stream. Mycological Progress 2004, 3:41-49.
70. Nunan N., Ritz K., Rivers M., Feeney D.S., Young I.M. Investigating microbial micro-habitat structure using X-ray computed tomography. Geoderma 2006, 133:398-407.
71. Old K.M., Darbyshire J.F. Soil fungi as food for giant amoebae. Soil Biology and Biochemistry 1978, 10:93-100.
72. Orpin C.G., Bountiff L. Zoospore chemotaxis in the rumen phycomycete Neocallimastix frontalis. Journal of General Microbiology 1978, 104:113-122.
73. Ottow J.C.G., von Klopotek A. Enzymatic reduction of iron oxide by fungi. Applied Microbiology 1969, 18:41-43.
74. Paterson R.A. Benthic and planktonic phycomycetes from northern Michigan. Mycologia 1967, 59:405-416.
75. Phuphumirat W., Gleason F.H., Phongpaichit S., Mildenhall D.C. The infection of pollen by zoosporic fungi in tropical soils and its impact on pollen preservation: a preliminary study. Nova Hedwigia 2011, 92:233-244.
76. Perrier E., Bird N., Rieu M. Generalizing the fractal model of soil structure: the pore-solid fractal approach. Geoderma 1999, 88:137-164.
77. Powell M.J. Looking at mycology with a janus face: a glimpse at Chytridiomycetes active in the environment. Mycologia 1993, 85:1-20.
78. Powell M.J. Production and modifications of extracellular structures during development of chytridiomycetes. Protoplasma 1994, 181:123-141.
79. Powell M.J., Blackwell W.H. A proposed dispersal mechanism for Septosperma rhizophydii. Mycologia 1991, 83:673-680.
80. Purcell E.M. Life at low Reynolds-number. American Journal of Physics 1977, 45:3-11.
81. Rasconi S., Jobard M., Sime-Ngando T. Parasitic fungi of phytoplankton: ecological roles and implications for microbial food webs. Aquatic Microbial Ecology 2011, 62:123-137.
82. Read D.B., Bengough A.G., Gregory P.J., Crawford J.W., Robinson D., Scrimgeour C.M., Young I.M., Zhang K., Zhang X. Plant roots release phospholipid surfactants that modify the physical and chemical properties of soil. New Phytologist 2003, 157:315-326.
83. Richardson A.J., Stewart C.S., Gooday G.W. Attachment to cellulose and maturation of attached thalli in the anaerobic rumen fungus Neocallimastix frontalis strain RE1. Mycological Research 1998, 102:1119-1125.
84. Rillig M.C. Arbuscular mycorrhizae, glomalin and soil quality. Canadian Journal of Soil Science 2004, 84:355-363.
85. Ritz K., Young I.M. Interactions between soil structure and fungi. Mycologist 2004, 18:52-59.
86. Rodger S., Griffiths B.S., McNicol J.W., Wheatley R.W., Young I.M. The impact of bacterial diet on the migration and navigation of Caenorhabditis elegans. Microbial Ecology 2004, 48:358-365.
87. Sanz J.L., Köchling T. Molecular biology techniques used in wastewater treatment: an overview. Process Biochemistry 2007, 42:119-133.
88. Seena S., Wynberg N., Barlocher F. Fungal diversity during decomposition of oak, maple and linden leaves assessed through clone libraries. Fungal Diversity 2008, 30:1-14.
89. Shearer C.A., Descals E., Kohlmeyer B., Kohlmeyer J., Marvanová L., Padgett D., Porter D., Raja H.A., Schmit J.P., Thornton H.A., Voglmayr H. Fungal biodiversity in aquatic habitats. Biodiversity and Conservation 2007, 16:49-67.
90. Sime-Ngando T., Lefevre E., Gleason F.H. Hidden diversity among aquatic heterotrophic flagellates: ecological potentials of zoosporic fungi. Hydrobiologia 2011, 659:5-22.
91. Smits M.M. 13. Mineral tunnelling by fungi. Fungi in Biogeochemical Cycles 2006, 311-327. Cambridge University Press, Cambridge, UK. G.M. Gadd (Ed.).
92. Smits M.M. The fungal-mineral: challenges and considerations of micro-analytical developments. Fungal Biology Reviews 2009, 23:122-131.
93. Sparrow F.K. Aquatic Phycomycetes 1960, The University of Michigan Press, Ann Arbor, MI. second ed.
94. Steenwerth K.L., Drenovsky R.E., Lambert J.-J., Kluepfel D.A., Scow K.M., Smart D.R. Soil morphology, depth and grapevine root frequency influence microbial communities in a Pinot noir vineyard. Soil Biology and Biochemistry 2006, 40:1330-1340.
95. Sukop M.C., Perfect E., Bird N.R.A. Water retention of prefractal porous media generated with the homogeneous and heterogeneous algorithms. Water Resources Research 2001, 37:2631-2636.
96. Sutheimer S.H., Maurice P.A., Zhou Q. Dissolution of well and poorly crystallized kaolinites: Al speciation and effects of surface characteristics. American Mineralogist 1999, 84:620-628.
97. Thornton M.L. Transport of soil-dwelling aquatic phycomycetes by earthworms. Transactions British Mycological Society 1970, 55:391-397.
98. Timonin M.I., Illman W.I., Hartgerink T. Oxidation of manganous salts of manganese by soil fungi. Canadian Journal of Microbiology 1972, 18:793-799.
99. Tisdall J.M., Oades J.M. Organic matter and water-stable aggregates in soils. Journal of Soil Science 1982, 33:141-163.
100. Travland L.B. Structures of the motile cells of Coelomomyces psorophorae and functions of the zygote in encystment on a host. Canadian Journal of Botany 1979, 57:1021-1035.
101. Trinci A.P.J., Davies D.R., Gull K., Lawrence M., Nielsen B.B., Rickers A., Theodorou M.K. Anaerobic fungi in herbivorous animals. Mycological Research 1994, 98:129-152.
102. Tunlid A., Nivens D.E., Jansson H.-B., White D.C. Infrared monitoring of the adhesion of Catenaria anguillulae zoospores to solid surfaces. Experimental Mycology 1991, 15:206-214.
103. Turcotte D.L. Self-organized complexity in geomorphology: observations and models. Geomorphology 2007, 91:302-310.
104. van Schöll L., Kuyper T.W., Smits M.M., Landeweert R., Hoffland E., van Breemen N. Rock-eating mycorrhizas: their role in plant nutrition and biogeochemical cycles. Plant and Soil 2008, 303:35-47.
105. Wallace H.R. Observations on the emergence from cysts and the orientation of larvae of three species of the genus Heterodera in the presence of host plant roots. Nematologica 1958, 3:236-243.
106. Willoughby L.G. The ecology of some lower fungi at Esthwaite Water. Transactions British Mycological Society 1961, 44:305-332.
107. Young I.M., Crawford J.W., Rappoldt C. New methods and models for characterising structural heterogeneity of soil. Soil & Tillage Research 2001, 61:33-45.
108. Young I.M., Crawford J.W. Interactions and self-organization in the soil-microbe complex. Science 2004, 304:1634-1637.
109. Young I.M., Crawford J.W., Nunan N., Otten W., Spiers A. Microbial distribution in soils: physics and scaling. Advances in Agronomy 2008, 100:81-121.