Abstract
Bacterial-feeding nematodes constitute one of the primary grazers of soil bacteria. We investigated the effects of selective grazing of a representative nematode (Zeldia punctata, Cephalobidae) on nematode life history and population biology and on the soil microbial community. Firstly, we measured (i) the effect of five different bacterial strains on the nematode life cycle using petri dishes and (ii) the impact of bacterial inoculation on nematode population growth in a soil microcosm. Selection of the five bacterial strains was based on morphology, cell-wall characteristics and mucus production. Z. punctata development was strongly affected by the type of bacteria ingested, independent of experimental design. Bacterial cell-wall characteristics seemed to directly affect Z. punctata development since high nematode densities were only reached with gram-negative strains (Pseudomonas monteilii and Methylobacterium nodulans). In petri dishes, the filamentous organisms (Actinomyces sp.) and mucus-producing bacteria (Bradyrhizobium sp.) led to the least reproduction. Duration of the various nematode life phases (egg, juvenile, reproductive stage and non-reproductive stage) was significantly affected by the bacterial food source. Total life span varied from 12.5 days (Bradyrhizobium sp.) to 40 days (Pseudomonas monteilii). Secondly, we monitored the influence of Z. punctata on the indigenous soil microbial community in the presence or absence of a maize plantlet. Nematode inoculation led to an increase in bacterial activity (as measured by alkaline phosphatase activity) but did not significantly influence bacterial biomass. The genetic fingerprint (DGGE) of soil bacteria was more influenced by plant presence than by nematode inoculation. Nematode activity has important repercussions on N flux in the soil since inoculation of Z. punctata in the absence of plants resulted in a net increase of N mineralization (2 mg N per pot) while a decrease of mineral N (0.5 mg N per pot) was observed in the absence of the nematodes, due to bacterial immobilization. This study underscores the close relationship between selective bacterial grazing and nematode development. Nevertheless, the impact of nematode grazing on the overall soil microbial community seems to primarily affect microbial activity and relative dominance rather than microbial diversity.
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References
Alexander M 1977 Introduction to Soil Microbiology. John Wiley, New York.
Amato M and Ladd J N 1988 Assay for microbial biomass based on ninhydrin-reactive nitrogen extracts fumigated soil. Soil Biol. Biochem. 20, 107-114.
Anderson R V and Coleman D C 1981 Population development and interactions between two species of bacteriophagic nematodes. Nematologica 27, 6-19.
Andrassy I 1956 Die Rauminhalts-und Gewichtsbestimmung der Fadenwürmer (Nematoden). Acta Zoologica, Budapest 2, 1-15.
Andrew P A and Nicholas W L 1976 Effect of bacteria on dispersal of Caenorhabditis elegans(Rhabditidae). Nematologica 22, 451-461.
Baath E, Lohm U, Lundgren B, Rosswall and Soderstrom E A 1981 Impact of microbial-feeding animals on soil activity and nitrogen dynamics: a soil microcosm experiment. Oikos 37, 257-264.
Bardgett R D, Cook R, Yeates G W and Denton C S 1999 The influence of nematodes on below-ground processes in grassland ecosystems. Plant Soil 212, 23-33.
Bird A F and Ryder M H 1993 Feeding of the nematode Acrobeloides nanuson bacteria. J. Nematol. 25, 493-499.
Bonkowski M and Brandt F 2002 Do soil protozoa enhance plant growth by hormonal effects. Soil Boil. Biochem. 34, 1709-1715.
Bremner J 1965 Inorganic forms of nitrogen. InMethods of Soil Analysis, Ed Black CA et al., Madison WI. pp. 1179-1237.
de Ley P 1991 The nematode community of a marginal soil at Camberene, Senegal, with special attention to functional morphology and niche partitioning in the family Cephalobidae. Academiae Ana Leda 53, 109-153.
Djigal D, Brauman A, Diop A, Chotte J-L and Villenave C 2004 Influence of some bacterial-feeding nematodes (Cephalobidae) on soil microbial comunity during mays growth. Soil Biol. Biochem. 36, in press.
Duponnois R, Ba A M and Mateille T 1998 Effects of some rhizosphere bacteria for the biocontrol of nematodes of the genus Meloidogynewith Arthrobotrys oligospora. Fundam. Appl. Nematol. 21, 157-163.
Ekschmitt K, Bakonyi G, Bongers M, Bongers T, Boström S, Dogan H, Harrison A, Kallimanis A, Nagy P, O'Donnell A G, Sohlenius B, Stamou G P and Wolters V 1999 Effects of the nematofauna on microbial energy and matter transformation rates in European grassland soils. Plant Soil 212, 45-61.
Ferris H, Venette R C and Lau S S 1997 Population energetics of bacterial-feeding nematodes: carbon and nitrogen budgets. Soil Biol. Biochem. 29, 1183-1194.
Ferris H, Venette R C, vanderMeulen H R and Lau S S 1998 Nitrogen mineralization by bacterial-feeding nematodes: verification and measurement. Plant Soil 203, 159-171.
Founoune H, Duponnois R, Bâ A M, Sall S, Branget I, Lorquin J, Neyra M and Chotte J-L 2001 Mycorrhiza helper bacteria stimulate ectomycorrhizal symbiosis of Acacia holosericeawith Pisoluthus alba. New Phytol. 153, 81-89.
Galiana A, Alabarce J and Duhoux E 1990 Nodulation in vitro d'Acacia mangiumWild (leguminosae). Ann. Sci. For. 47, 451-460.
Griffiths B S and Bardgett R D 1997 Interactions between microbefeeding invertebrates and soil microorganisms. InModern Soil Microbiology. Eds. J D van Elsas, E Wellington and J T Trevors. Dekker, M., New York. pp. 165-182.
Griffiths B S, Welschen R, van Arendonk J J C M and Lambers H 1992 The effect of nitrate-nitrogen supply on bacteria and bacterial-feeding fauna in the rhizosphere of different grass species. Oecologia 91, 251-259.
Griffiths B S, Bonkowski M, Dobson G and Caul S 1999 Changes in soil microbial community structure in the presence of microbialfeeding nematodes and protozoa. Pedobiologia 43, 297-304.
Ingham R E, Trofymow J A, Ingham E R and Coleman D C 1985 Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecological Monographs 55, 119-140.
Jensen S, Ovreas L, Daae F L and Torsvik V 1998 Diversity in methane enrichments from agricultural soil revealed by DGGE separation of PCR amplified 16S rDNA fragments. FEMS Microbiology Ecology 26, 17-26.
Mikola J 1998 Effects of microbivore species composition and basal resource enrichment on trophic-level biomasses in an experimental microbial-based soil food web. Oecologia 117, 396-403.
Mikola J and Setälä H 1998 No evidence of trophic cascades in an experimental microbial-based soil food web. Ecology 153-164.
Muyzer G, De Waal E C and Uitterlinden A 1993 Profiling of complex microbial populations using denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59, 695-700.
Ovreas L, Forney L, Daae F L and Torsvik V 1997 Distribution of bacterioplankton in meromictic lake Saelevannet, as determined by denaturing gradient gel electrophoresis of PCRamplified genes fragments coding for 16S rRNA. Appl. Environ. Microbiol., 3367-3373.
Porteous L A, Seidler R J and Watrud L S 1997 An improved method for purifying DNA from soil for PCR amplification and molecular ecology applications. Molecular Ecology 6, 787-791.
Rønn R, McCaig A E, Griffiths B S and Prosser J I 2002 Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environ Microbiol 68, 6094-6105.
Ruess L, Zapata E J G and Dighton J 2000 Food preferences of a fungal-feeding Aphelenchoides species. Nematology 2, 223-230.
Sall S and Chotte J L 2002 Phosphatase and urease activities in a tropical sandy soil as affected by water holding capacity and assay conditions. Commun. Soil Plant Analysis 33, 2745-2755.
Samba R R, De Lajudie P, Gillis M, Neyra M, SpencerBaretto M and Dreyfus B 1999 Diversity of Rhyzobianodulating Crotalaria sppfrom Senegal. Symbiosis 27, 259-268.
Seinhorst J W 1962 Modifications of the elutriation method for extracting nematodes from soil. Nematologica 8, 117-128.
Slepecky R A and Hemphill E 1991 The genus Bacillus-non medical. InThe Prokaryotes: A Handbook on the Biology of Bacteria. Ecophysiology, Isolation, Identification, Applications, Eds. A Balows, H G Truper, M Dworkin, W Harder and K H Schleifer. Springer-Verlag, New York.
Sohlenius B 1990 Influence of cropping system and nitrogen input on soil fauna and microorganisms in a Swedish arable soil. Biol. Fert. Soils 9, 168-173.
Sohlenius B 1973 Influence of food supply on population structure and length distribution in Acrobeloides nanus(Nematoda: Cephalobidae). Pedobiologia 13, 205-213.
Sy A, Giraud E, Jourand P, Garcia N, Willems A, De Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C and Dreyfus B 2001 Methylotrophic M. nodulansbacteria nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 183, 214-220.
Tabatabai M A and Bremner J M 1969 Use of p-nitrophneyl phosphate for assay of soil phosphatase activity. Soil Biol. Biochem. 1, 301-307.
Traunspurger W, Bergtold M and Goedkoop W 1997 The effects of nematodes on bacterial activity and abundance in a freshwater sediment. Oecologia 112, 118-122.
Venette R C and Ferris H 1998 Influence of bacterial type and density on population growth of bacterial-feeding nematodes. Soil Biol. Biochem. 30, 949-960.
Villenave C, Bongers T, Ekschmitt K, Djigal D and Chotte J-L 2001 Changes in nematode communities following cultivation of soils after fallow periods of different length. Appl. Soil Ecol. 17, 43-52.
Villenave C, Bongers T, Ekschmitt K, Fernandes P and Oliver R 2003 Changes in nematode communities after manuring in millet fields in Senegal. Nematology 5, (in press).
Villenave C, Leye K, Chotte J L and Duponnois R 2003 Nematofauna associated with exotic and native leguminous plant species in West Africa: Effect of Glomus intaradicesarbuscular mycorrhizal symbiosis. Biol. Fertil. Soils 38, 161-169.
Vincent J M 1970 A Manual for the Pratictical Study of Root Nodule Bacteria. Blackwell Sci. Publ. Oxford.
Williams S J and Davies F L 1965 Use of antibiotics for selective isolation and enumeration of actinomycetes in soil. J. General Microbiol. 38.
Yeates G W 1979 Soil nematodes in terrestrial ecosystems. J. Nematol. 11, 213-229.
Yeates G W, Bongers T, de Goede R G M, Freckman D W and Georgieva S S 1993 Feeding habits in soil nematode families and genera-An outline for soil ecologists. J. Nematol. 25, 315-331.
Yeates G W 2003 Nematodes as soil indicators: functional and biodiversity aspects. Biol. Fertil. Soils 37, 199-210.
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Djigal, D., Sy, M., Brauman, A. et al. Interactions between Zeldia Punctata (Cephalobidae) and bacteria in the presence or absence of maize plants. Plant and Soil 262, 33–44 (2004). https://doi.org/10.1023/B:PLSO.0000037022.16822.75
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DOI: https://doi.org/10.1023/B:PLSO.0000037022.16822.75