Most cited article - PubMed ID 36190238
Arbuscular Mycorrhiza and Nitrification: Disentangling Processes and Players by Using Synthetic Nitrification Inhibitors
While largely depending on other microorganisms for nitrogen (N) mineralization, arbuscular mycorrhizal fungi (AMF) can transfer N from organic sources to their host plants. Here, we compared N acquisition by the AMF hyphae from chitin and protein sources and assessed the effects of microbial interactions in the hyphosphere. We employed in vitro compartmented microcosms, each containing three distinct hyphosphere compartments amended with different N sources (protein, chitin, or ammonium chloride), one of which was enriched with 15N isotope. All hyphosphere compartments were supplied with Paenibacillus bacteria, with or without the protist Polysphondylium pallidum. We measured the effect of these model microbiomes on the efficiency of 15N transfer to roots via the AMF hyphae. We found that the hyphae efficiently took up N from ammonium chloride, competing strongly with bacteria and protists. Mobilization of 15N from chitin and protein was facilitated by bacteria and protists, respectively. Notably, AMF priming significantly affected the abundance of bacteria and protists in hyphosphere compartments and promoted mineralization of protein N by protists. Subsequently, this N was transferred into roots. Our results provide the first unequivocal evidence that roots can acquire N from proteins present in the AMF hyphosphere and that protists may play a crucial role in protein N mineralization.
- Keywords
- arbuscular mycorrhizal fungus, hyphosphere, multitrophic interactions, organic nitrogen, quantitative real‐time PCR, stable isotopes, temporal dynamics,
- MeSH
- Chitin metabolism MeSH
- Nitrogen * metabolism MeSH
- Eukaryota * metabolism MeSH
- Hyphae metabolism MeSH
- Nitrogen Isotopes MeSH
- Plant Roots microbiology metabolism MeSH
- Mycorrhizae * metabolism MeSH
- Plant Proteins metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Chitin MeSH
- Nitrogen * MeSH
- Nitrogen Isotopes MeSH
- Plant Proteins MeSH
Differences in functioning among various genotypes of arbuscular mycorrhizal (AM) fungi can determine their fitness under specific environmental conditions, although knowledge of the underlying mechanisms still is very fragmented. Here we compared seven homokaryotic isolates (genotypes) of Rhizophagus irregularis, aiming to characterize the range of intraspecific variability with respect to hyphal exploration of organic nitrogen (N) resources, and N supply to plants. To this end we established two experiments (one in vitro and one in open pots) and used 15N-chitin as the isotopically labeled organic N source. In Experiment 1 (in vitro), mycelium of all AM fungal genotypes transferred a higher amount of 15N to the plants than the passive transfer of 15N measured in the non-mycorrhizal (NM) controls. Noticeably, certain genotypes (e.g., LPA9) showed higher extraradical mycelium biomass production but not necessarily greater 15N acquisition than the others. Experiment 2 (in pots) highlighted that some of the AM fungal genotypes (e.g., MA2, STSI) exhibited higher rates of targeted hyphal exploration of chitin-enriched zones, indicative of distinct N exploration patterns from the other genotypes. Importantly, there was a high congruence of hyphal exploration patterns between the two experiments (isolate STSI always showing highest efficiency of hyphal exploration and isolate L23/1 being consistently the lowest), despite very different (micro) environmental conditions in the two experiments. This study suggests possible strategies that AM fungal genotypes employ for efficient N acquisition, and how to measure them. Implications of such traits for local mycorrhizal community assembly still need to be understood.
- Keywords
- Hyphosphere microbiome, Intraspecific differences, Mycorrhizal hyphal networks, Quantitative real-time PCR (qPCR), Soil nitrogen exploration, Stable isotopic labeling and tracing,
- MeSH
- Chitin metabolism MeSH
- Nitrogen metabolism MeSH
- Genotype * MeSH
- Glomeromycota physiology genetics MeSH
- Fungi MeSH
- Hyphae * genetics growth & development MeSH
- Mycorrhizae * physiology genetics MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Chitin MeSH
- Nitrogen MeSH
Arbuscular mycorrhizal (AM) fungi are supposedly competing with ammonia-oxidizing microorganisms (AO) for soil nitrogen in form of ammonium. Despite a few studies directly addressing AM fungal and AO interactions, mostly in artificial cultivation substrates, it is not yet clear whether AM fungi can effectively suppress AO in field soils containing complex indigenous microbiomes. To fill this knowledge gap, we conducted compartmentalized pot experiments using four pairs of cropland and grassland soils with varying physicochemical properties. To exclude the interference of roots, a fine nylon mesh was used to separate the rhizosphere and mesh bags, with the latter being filled with unsterile field soils. Inoculation of plants with AM fungus Rhizophagus irregularis LPA9 suppressed AO bacteria (AOB) but not archaea (AOA) in the soils, indicating how soil nitrification could be suppressed by AM fungal presence/activity. In addition, in rhizosphere filled with artificial substrate, AM inoculation did suppress both AOB and AOA, implying more complex interactions between roots, AO, and AM fungi. Besides, we also observed that indigenous AM fungi contained in the field soils eventually did colonize the roots of plants behind the root barrier, and that the extent of such colonization was higher if the soil has previously been taken from cropland than from grassland. Despite this, the effect of experimental AM fungal inoculation on suppression of indigenous AOB in the unsterile field soils did not vanish. It seems that studying processes at a finer temporal scale, using larger buffer zones between rhizosphere and mesh bags, and/or detailed characterization of indigenous AM fungal and AO communities would be needed to uncover further details of the biotic interactions between the AM fungi and indigenous soil AO.
INTRODUCTION: The hyphosphere of arbuscular mycorrhizal (AM) fungi is teeming with microbial life. Yet, the influence of nutrient availability or nutrient forms on the hyphosphere microbiomes is still poorly understood. METHODS: Here, we examined how the microbial community (prokaryotic, fungal, protistan) was affected by the presence of the AM fungus Rhizophagus irregularis in the rhizosphere and the root-free zone, and how different nitrogen (N) and phosphorus (P) supplements into the root-free compartment influenced the communities. RESULTS: The presence of AM fungus greatly affected microbial communities both in the rhizosphere and the root-free zone, with prokaryotic communities being affected the most. Protists were the only group of microbes whose richness and diversity were significantly reduced by the presence of the AM fungus. Our results showed that the type of nutrients AM fungi encounter in localized patches modulate the structure of hyphosphere microbial communities. In contrast we did not observe any effects of the AM fungus on (non-mycorrhizal) fungal community composition. Compared to the non-mycorrhizal control, the root-free zone with the AM fungus (i.e., the AM fungal hyphosphere) was enriched with Alphaproteobacteria, some micropredatory and copiotroph bacterial taxa (e.g., Xanthomonadaceae and Bacteroidota), and the poorly characterized and not yet cultured Acidobacteriota subgroup GP17, especially when phytate was added. Ammonia-oxidizing Nitrosomonas and nitrite-oxidizing Nitrospira were significantly suppressed in the presence of the AM fungus in the root-free compartment, especially upon addition of inorganic N. Co-occurrence network analyses revealed that microbial communities in the root-free compartment were complex and interconnected with more keystone species when AM fungus was present, especially when the root-free compartment was amended with phytate. CONCLUSION: Our study showed that the form of nutrients is an important driver of prokaryotic and eukaryotic community assembly in the AM fungal hyphosphere, despite the assumed presence of a stable and specific AM fungal hyphoplane microbiome. Predictable responses of specific microbial taxa will open the possibility of using them as co-inoculants with AM fungi, e.g., to improve crop performance.
- Keywords
- arbuscular mycorrhizal (AM) fungi/al, extraradical hyphae, hyphosphere, inorganic and organic, microbiome, networks, nutrient cycling, nutrient mobilization,
- Publication type
- Journal Article MeSH
Plant-plant interactions and coexistence can be directly mediated by symbiotic arbuscular mycorrhizal (AM) fungi through asymmetric resource exchange between the plant and fungal partners. However, little is known about the effects of AM fungal presence on resource allocation in mixed plant stands. Here, we examined how phosphorus (P), nitrogen (N) and carbon (C) resources were distributed between coexisting con- and heterospecific plant individuals in the presence or absence of AM fungus, using radio- and stable isotopes. Congeneric plant species, Panicum bisulcatum and P. maximum, inoculated or not with Rhizophagus irregularis, were grown in two different culture systems, mono- and mixed-species stands. Pots were subjected to different shading regimes to manipulate C sink-source strengths. In monocultures, P. maximum gained more mycorrhizal phosphorus uptake benefits than P.bisulcatum. However, in the mixed culture, the AM fungus appeared to preferentially transfer nutrients (33P and 15N) to P.bisulcatum compared to P. maximum. Further, we observed higher 13C allocation to mycorrhiza by P.bisulcatum in mixed- compared to the mono-systems, which likely contributed to improved competitiveness in the mixed cultures of P.bisulcatum vs. P. maximum regardless of the shading regime. Our results suggest that the presence of mycorrhiza influenced competitiveness of the two Panicum species in mixed stands in favor of those with high quality partner, P. bisulcatum, which provided more C to the mycorrhizal networks. However, in mono-species systems where the AM fungus had no partner choice, even the lower quality partner (i.e., P.maximum) could also have benefitted from the symbiosis. Future research should separate the various contributors (roots vs. common mycorrhizal network) and mechanisms of resource exchange in such a multifaceted interaction.
