Organic Nitrogen-Driven Stimulation of Arbuscular Mycorrhizal Fungal Hyphae Correlates with Abundance of Ammonia Oxidizers

. 2016 ; 7 () : 711. [epub] 20160512

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid27242732

Large fraction of mineral nutrients in natural soil environments is recycled from complex and heterogeneously distributed organic sources. These sources are explored by both roots and associated mycorrhizal fungi. However, the mechanisms behind the responses of arbuscular mycorrhizal (AM) hyphal networks to soil organic patches of different qualities remain little understood. Therefore, we conducted a multiple-choice experiment examining hyphal responses to different soil patches within the root-free zone by two AM fungal species (Rhizophagus irregularis and Claroideoglomus claroideum) associated with Medicago truncatula, a legume forming nitrogen-fixing root nodules. Hyphal colonization of the patches was assessed microscopically and by quantitative real-time PCR (qPCR) using AM taxon-specific markers, and the prokaryotic and fungal communities in the patches (pooled per organic amendment treatment) were profiled by 454-amplicon sequencing. Specific qPCR markers were then designed and used to quantify the abundance of prokaryotic taxa showing the strongest correlation with the pattern of AM hyphal proliferation in the organic patches as per the 454-sequencing. The hyphal density of both AM fungi increased due to nitrogen (N)-containing organic amendments (i.e., chitin, DNA, albumin, and clover biomass), while no responses as compared to the non-amended soil patch were recorded for cellulose, phytate, or inorganic phosphate amendments. Abundances of several prokaryotes, including Nitrosospira sp. (an ammonium oxidizer) and an unknown prokaryote with affiliation to Acanthamoeba endosymbiont, which were frequently recorded in the 454-sequencing profiles, correlated positively with the hyphal responses of R. irregularis to the soil amendments. Strong correlation between abundance of these two prokaryotes and the hyphal responses to organic soil amendments by both AM fungi was then confirmed by qPCR analyses using all individual replicate patch samples. Further research is warranted to ascertain the causality of these correlations and particularly which direct roles (if any) do these prokaryotes play in the observed AM hyphal responses to organic N amendment, organic N utilization by the AM fungus and its (N-unlimited) host plant. Further, possible trophic dependencies between the different players in the AM hyphosphere needs to be elucidated upon decomposing the organic N sources.

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Alberton O., Kuyper T. W., Gorissen A. (2005). Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO PubMed DOI

Bago B., Cano C., Azcón-Aguilar C., Samson J., Coughlan A. P., Piché Y. (2004). Differential morphogenesis of the extraradical mycelium of an arbuscular mycorrhizal fungus grown monoxenically on spatially heterogeneous culture media. PubMed DOI

Bago B., Vierheilig H., Piché Y., Azcón-Aguilar C. (1996). Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus PubMed DOI

Baldrian P., Kolařík M., Štursová M., Kopecký J., Valášková V., Větrovský T., et al. (2012). Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. PubMed DOI PMC

Baltruschat H. (1987). Field inoculation of maize with vesicular-arbuscular mycorrhizal fungi by using expanded clay as carrier material for mycorrhiza.

Beier S., Bertilsson S. (2013). Bacterial chitin degradation-mechanisms and ecophysiological strategies. PubMed DOI PMC

Bonkowski M. (2004). Protozoa and plant growth: the microbial loop in soil revisited. PubMed DOI

Calvet C., Camprubi A., Perez-Hernandez A., Lovato P. E. (2013). Plant growth stimulation and root colonization potential of in vivo versus in vitro arbuscular mycorrhizal inocula.

Cavagnaro T. R., Smith F. A., Smith S. E., Jakobsen I. (2005). Functional diversity in arbuscular mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species. DOI

Cheng L., Booker F. L., Tu C., Burkey K. O., Zhou L. S., Shew H. D., et al. (2012). Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO PubMed DOI

Couillerot O., Ramirez-Trujillo A., Walker V., von Felten A., Jansa J., Maurhofer M., et al. (2013). Comparison of prominent Azospirillum strains in Azospirillum- PubMed DOI

Cox G., Tinker P. B. (1976). Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. I. The arbuscule and phosphorus transfer: a quantitative ultrastructural study. DOI

Cruz C., Egsgaard H., Trujillo C., Ambus P., Requena N., Martins-Loucao M. A., et al. (2007). Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. PubMed DOI PMC

Drigo B., Pijl A. S., Duyts H., Kielak A., Gamper H. A., Houtekamer M. J., et al. (2010). Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO PubMed DOI PMC

Facelli E., Facelli J. M. (2002). Soil phosphorus heterogeneity and mycorrhizal symbiosis regulate plant intra-specific competition and size distribution. PubMed DOI

Felderer B., Jansa J., Schulin R. (2013). Interaction between root growth allocation and mycorrhizal fungi in soil with patchy P distribution. DOI

Feldmann F., Idczak E. (1992). “Inoculum production of vesicular-arbuscular mycorrhizal fungi for use in tropical nurseries,” in

Fellbaum C. R., Gachomo E. W., Beesetty Y., Choudhari S., Strahan G. D., Pfeffer P. E., et al. (2012). Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. PubMed DOI PMC

Feng G., Song Y. C., Li X. L., Christie P. (2003). Contribution of arbuscular mycorrhizal fungi to utilization of organic sources of phosphorus by red clover in a calcareous soil. DOI

Feng H., Feng G., Wang J., Li X. (2004). Effect of sodium phytate on alkaline phosphatase (ALP) activity in intraradical hyphae of AM fungi and development of its extraradical hyphae. PubMed

Fitter A. H. (1991). Costs and benefits of mycorrhizas - Implications for functioning under natural conditions. DOI

Gavito M. E., Olsson P. A. (2003). Allocation of plant carbon to foraging and storage in arbuscular mycorrhizal fungi. PubMed DOI

Gavito M. E., Olsson P. A. (2008). Foraging strategies of the external mycelium of the arbuscular mycorrhizal fungi DOI

George T., Singleton P. W., Vankessel C. (1993). The use of 15N natural abundance and nitrogen yield of nonnodulating isolines to estimate nitrogen fixation by soybeans ( DOI

Govindarajulu M., Pfeffer P. E., Jin H. R., Abubaker J., Douds D. D., Allen J. W., et al. (2005). Nitrogen transfer in the arbuscular mycorrhizal symbiosis. PubMed DOI

Gryndler M., Hršelová H., Stříteská D. (2000). Effect of soil bacteria on hyphal growth of the arbuscular mycorrhizal fungus PubMed DOI

Gryndler M., Jansa J., Hršelová H., Chvátalová I., Vosátka M. (2003). Chitin stimulates development and sporulation of arbuscular mycorrhizal fungi. DOI

Gryndler M., Vejsadová H., Vančura V. (1992). The effect of magnesium ions on the vesicular arbuscular mycorrhizal infection of maize roots. PubMed DOI

Gryndler M., Vosátka M., Hršelová H., Chvátalová I., Jansa J. (2002). Interaction between arbuscular mycorrhizal fungi and cellulose in growth substrate. DOI

Herman D. J., Firestone M. K., Nuccio E., Hodge A. (2012). Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition. PubMed DOI

Hodge A. (2004). The plastic plant: root responses to heterogeneous supplies of nutrients. DOI

Hodge A., Campbell C. D., Fitter A. H. (2001). An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. PubMed DOI

Hodge A., Fitter A. H. (2010). Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. PubMed DOI PMC

Hodge A., Robinson D., Fitter A. H. (2000). Arbuscular mycorrhizal inoculum enhances root proliferation in, but not nitrogen capture from, nutrient-rich patches in soil. PubMed DOI

Hodge A., Storer K. (2015). Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. DOI

Jakobsen I., Abbott L. K., Robson A. D. (1992). External hyphae of vesicular-arbuscular mycorrhizal fungi associated with DOI

Jansa J., Bukovská P., Gryndler M. (2013). Mycorrhizal hyphae as ecological niche for highly specialized hypersymbionts - or just soil free-riders? PubMed DOI PMC

Jansa J., Gryndler M. (2010). “Biotic environment of the arbuscular mycorrhizal fungi in soil,” in DOI

Jansa J., Mozafar A., Frossard E. (2003). Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. DOI

Jansa J., Mozafar A., Frossard E. (2005). Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. DOI

Johnson N. C., Wilson G. W. T., Wilson J. A., Miller R. M., Bowker M. A. (2015). Mycorrhizal phenotypes and the law of the minimum. PubMed DOI

Joner E. J., Jakobsen I. (1995). Growth and extracellular phosphatase activity of arbuscular mycorrhizal hyphae as influenced by soil organic matter. DOI

Joner E. J., van Aarle I. M., Vosátka M. (2000). Phosphatase activity of extra-radical arbuscular mycorrhizal hyphae: a review. DOI

Koide R. T., Kabir Z. (2000). Extraradical hyphae of the mycorrhizal fungus PubMed DOI

Koller R., Scheu S., Bonkowski M., Robin C. (2013). Protozoa stimulate N uptake and growth of arbuscular mycorrhizal plants. DOI

Konvalinková T., Püschel D., Janoušková M., Gryndler M., Jansa J. (2015). Duration and intensity of shade differentially affects mycorrhizal growth- and phosphorus uptake responses of PubMed DOI PMC

Koske R. E., Gemma J. N. (1989). A modified procedure for staining roots to detect VA mycorrhizas. DOI

Kowalchuk G. A., Stephen J. R., DeBoer W., Prosser J. I., Embley T. M., Woldendorp J. W. (1997). Analysis of ammonia-oxidizing bacteria of the beta subdivision of the class PubMed PMC

Leigh J., Fitter A. H., Hodge A. (2011). Growth and symbiotic effectiveness of an arbuscular mycorrhizal fungus in organic matter in competition with soil bacteria. PubMed DOI

Leigh J., Hodge A., Fitter A. H. (2009). Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. PubMed DOI

Li X. L., George E., Marschner H. (1991). Extension of the phosphorus depletion zone in VA mycorrhizal white clover in a calcareous soil. DOI

Mäder P., Vierheilig H., Streitwolf-Engel R., Boller T., Frey B., Christie P., et al. (2000). Transport of DOI

McGonigle T. P., Miller M. H., Evans D. G., Fairchild G. L., Swan J. A. (1990). A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. PubMed DOI

Nuccio E. E., Hodge A., Pett-Ridge J., Herman D. J., Weber P. K., Firestone M. K. (2013). An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. PubMed DOI

Ohno T., Zibilske L. M. (1991). Determination of low concentrations of phosphorus in soil extracts using Malachite green. DOI

Ravnskov S., Larsen J., Olsson P. A., Jakobsen I. (1999). Effects of various organic compounds growth and phosphorus uptake of an arbuscular mycorrhizal fungus. DOI

Robinson D. (1996). Resource capture by localized root proliferation: why do plants bother? DOI

Robson A. D., Longnecker N. E., Osborne L. D. (1992). Effects of heterogeneous nutrient supply on root growth and nutrient uptake in relation to nutrient supply on duplex soils. DOI

Rotthauwe J. H., Witzel K. P., Liesack W. (1997). The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. PubMed PMC

Scheublin T. R., Ridgway K. P., Young J. P. W., van der Heijden M. G. A. (2004). Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. PubMed DOI PMC

Šmilauer P., Lepš J. (2014).

Smith S. E., Smith F. A., Jakobsen I. (2004). Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. DOI

Somasegaran P., Hoben H. J. (1994).

St. John T., Coleman D., Reid C. (1983). Association of vesicular-arbuscular mycorrhizal hyphae with soil organic particles. DOI

Sulieman S., Van Ha C., Schulze J., Tran L. S. P. (2013). Growth and nodulation of symbiotic PubMed DOI PMC

Sylvia D. M., Norris J. R. (1992). “Quantification of external hyphae of vesicular-arbuscular mycorrhizal fungi,” in

Tarafdar J. C., Marschner H. (1994). Phosphatase activity in the rhizosphere and hyphosphere of VA mycorrhizal wheat supplied with inorganic and organic Posphorus. DOI

Ter Braak C. J. F., Šmilauer P. (2002).

Thonar C., Erb A., Jansa J. (2012). Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communities - marker design, verification, calibration and field validation. PubMed DOI

Thonar C., Schnepf A., Frossard E., Roose T., Jansa J. (2011). Traits related to differences in function among three arbuscular mycorrhizal fungi. DOI

Toljander J. F., Artursson V., Paul L. R., Jansson J. K., Finlay R. D. (2006). Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. PubMed DOI

Toljander J. F., Lindahl B. D., Paul L. R., Elfstrand M., Finlay R. D. (2007). Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. PubMed DOI

van der Heijden M. G. A., Martin F. M., Selosse M. A., Sanders I. R. (2015). Mycorrhizal ecology and evolution: the past, the present, and the future. PubMed DOI

Větrovský T., Baldrian P. (2013). Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. DOI

Wagg C., Bender S. F., Widmer F., van der Heijden M. G. A. (2014). Soil biodiversity and soil community composition determine ecosystem multifunctionality. PubMed DOI PMC

Watt M., Silk W. K., Passioura J. B. (2006). Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. PubMed DOI PMC

Webster G., Embley T. M., Freitag T. E., Smith Z., Prosser J. I. (2005). Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils. PubMed DOI

White T., Bruns T., Lee S., Taylor J. (1990). “Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics,” in

Zhang L., Fan J. Q., Ding X. D., He X. H., Zhang F. S., Feng G. (2014). Hyphosphere interactions between an arbuscular mycorrhizal fungus and a phosphate solubilizing bacterium promote phytate mineralization in soil. DOI

Zheng C., Chai M., Jiang S., Zhang S., Christie P., Zhang J. (2015). Foraging capability of extraradical mycelium of arbuscular mycorrhizal fungi to soil phosphorus patches and evidence of carry-over effect on new host plant. DOI

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