Abstract
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.
Highlights
The physical arrangement of soil particles, aggregates, and pores; root and microbial growth; and burrowing activities of animals, together with external inputs of such particulate organic residues as plant litter, animal excreta, and dead bodies, all create a soil environment highly heterogeneous in both space and time and at a range of scales (Facelli and Facelli, 2002; Watt et al, 2006)
We consider our results to be robust because we used two independent approaches to quantify the development of Arbuscular mycorrhizal (AM) fungi in soil, namely the traditional microscopy and the quantitative real-time PCR (qPCR)
Using two independent approaches (454-sequencing of pooled soil samples per soil amendment treatment and qPCR using all individual soil samples), we demonstrated that the hyphal developmental responses of both AM fungi to soil amendments strongly correlated with the abundance of Nitrosospira sp., an ammonium oxidizer, and few other bacterial taxa in the soil including an obligate Acanthamoeba endosymbiont
Summary
The physical arrangement of soil particles, aggregates, and pores; root and microbial growth; and burrowing activities of animals, together with external inputs of such particulate organic residues as plant litter, animal excreta, and dead bodies, all create a soil environment highly heterogeneous in both space and time and at a range of scales (Facelli and Facelli, 2002; Watt et al, 2006). Adaptations of roots to heterogeneously distributed organic and inorganic nutrients in soil have been studied for decades (Robson et al, 1992; Robinson, 1996; Hodge, 2004). The root is not the only – and possibly not even the main – organ for primary acquisition of such poorly mobile nutrients as phosphorus (P) from the soil solution. This function is often fulfilled by the plants’ mycorrhizal symbionts. The nutrients taken up by AM fungal hyphae from the soil solution are passed on to the host plants at the root–mycorrhizal interface in the root cortex (Fitter, 1991; Smith et al, 2004). The importance of AM symbiosis for P acquisition by many plant species is firmly established (Cox and Tinker, 1976; Jakobsen et al, 1992), whereas its role in plant nitrogen (N) acquisition, repeatedly demonstrated (Mäder et al, 2000; Hodge et al, 2001; Fellbaum et al, 2012), is broadly accepted as being lower than that in plant P acquisition (Johnson et al, 2015)
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