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Diurnal patterns of productivity of arbuscular mycorrhizal fungi revealed with the Soil Ecosystem Observatory.

ABSTRACT: Arbuscular mycorrhizal (AM) fungi are the most abundant plant symbiont and a major pathway of carbon sequestration in soils. However, their basic biology, including their activity throughout a 24-h day : night cycle, remains unknown. We employed the in situ Soil Ecosystem Observatory to quantify the rates of diurnal growth, dieback and net productivity of extra-radical AM fungi. AM fungal hyphae showed significantly different rates of growth and dieback over a period of 24 h and paralleled the circadian-driven photosynthetic oscillations observed in plants. The greatest rates (and incidences) of growth and dieback occurred between noon and 18:00 h. Growth and dieback events often occurred simultaneously and were tightly coupled with soil temperature and moisture, suggesting a rapid acclimation of the external phase of AM fungi to the immediate environment. Changes in the environmental conditions and variability of the mycorrhizosphere may alter the diurnal patterns of productivity of AM fungi, thereby modifying soil carbon sequestration, nutrient cycling and host plant success.

SUBMITTER: Hernandez RR

PROVIDER: S-EPMC4288973 | biostudies-literature | 2013 Oct

REPOSITORIES: biostudies-literature

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Diurnal patterns of productivity of arbuscular mycorrhizal fungi revealed with the Soil Ecosystem Observatory.

Hernandez Rebecca R RR Allen Michael F MF

The New phytologist 20130712 2

Arbuscular mycorrhizal (AM) fungi are the most abundant plant symbiont and a major pathway of carbon sequestration in soils. However, their basic biology, including their activity throughout a 24-h day : night cycle, remains unknown. We employed the in situ Soil Ecosystem Observatory to quantify the rates of diurnal growth, dieback and net productivity of extra-radical AM fungi. AM fungal hyphae showed significantly different rates of growth and dieback over a period of 24 h and paralleled the c ...[more]

PMID: 23844990

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Project description:Soil bacteria and fungi are known to form niche-specific communities that differ between actively growing and decaying roots. Yet almost nothing is known about the cross-kingdom interactions that frame these communities and the environmental filtering that defines these potentially friendly or competing neighbors. We explored the temporal and spatial patterns of soil fungal (mycorrhizal and nonmycorrhizal) and bacterial cooccurrence near roots of wild oat grass, Avena fatua, growing in its naturalized soil in a greenhouse experiment. Amplicon sequences of the fungal internal transcribed spacer (ITS) and bacterial 16S rRNA genes from rhizosphere and bulk soils collected at multiple plant growth stages were used to construct covariation-based networks as a step toward identifying fungal-bacterial associations. Corresponding stable-isotope-enabled metagenome-assembled genomes (MAGs) of bacteria identified in cooccurrence networks were used to inform potential mechanisms underlying the observed links. Bacterial-fungal networks were significantly different in rhizosphere versus bulk soils and between arbuscular mycorrhizal fungi (AMF) and nonmycorrhizal fungi. Over 12 weeks of plant growth, nonmycorrhizal fungi formed increasingly complex networks with bacteria in rhizosphere soils, while AMF more frequently formed networks with bacteria in bulk soils. Analysis of network-associated bacterial MAGs suggests that some of the fungal-bacterial links that we identified are potential indicators of bacterial breakdown and consumption of fungal biomass, while others intimate shared ecological niches.IMPORTANCE Soils near living and decomposing roots form distinct niches that promote microorganisms with distinctive environmental preferences and interactions. Yet few studies have assessed the community-level cooccurrence of bacteria and fungi in these soil niches as plant roots grow and senesce. With plant growth, we observed increasingly complex cooccurrence networks between nonmycorrhizal fungi and bacteria in the rhizosphere, while mycorrhizal fungal (AMF) and bacterial cooccurrence was more pronounced in soil further from roots, in the presence of decaying root litter. This rarely documented phenomenon suggests niche sharing of nonmycorrhizal fungi and bacteria, versus niche partitioning between AMF and bacteria; both patterns are likely driven by C substrate availability and quality. Although the implications of species cooccurrence are fiercely debated, MAGs matching the bacterial nodes in our networks possess the functional potential to interact with the fungi that they are linked to, suggesting an ecological significance of fungal-bacterial cooccurrence patterns.

Project description:In the Mediterranean, long-term impact of typical land uses on soil fertility have not been quantified yet on replicated mixed crop-livestock farms and considering the variability of soil texture. Here, we report the effects, after 15 years of practice, of two legume-winter cereal rotations, olive orchards and vineyards on microbiological and chemical indicators of soil fertility and the communities of arbuscular mycorrhizal fungi (AMF). We compare the changes among these four agricultural land-use types to woodland reference sites. Root colonization by AMF of English ryegrass (Lolium perenne L.), a grass that occurred under all land use types, was only half as heavy in biannual berseem clover (Trifolium alexandrinum L.)-winter cereal rotations than in 4-year alfalfa (Medicago sativa L.)-winter cereal rotations. In olive (Olea europaea L.) orchards and vineyards (Vitis vinifera L.), where weeds are controlled by frequent surface tillage, the AMF root colonization of ryegrass was again much lower than in the legume-cereal rotations and at the woodland reference sites. All the microbial parameters and soil organic carbon correlated most strongly with differences in occurrence and relative abundance (β-diversity) of AMF genera in soil. The soil pH and mineral nutrients in soil strongly correlated with differences in AMF root colonization and AMF genus richness (α-diversity) in soil. Diversity of AMF was much less affected by soil texture than land use, while the opposite was true for microbial and chemical soil fertility indicators. Land uses that guaranteed a continuous ground cover of herbaceous plants and that involved only infrequent tillage, such as multiyear alfalfa-winter cereal rotation, allowed members of the AMF genus Scutellospora to persist and remain abundant. On the contrary, under land uses accompanied by frequent tillage and hence discontinuous presence of herbaceous plants, such as tilled olive orchard and vineyard, members of the genus Funneliformis dominated. These results suggest that multiyear alfalfa-winter cereal rotation with active plant growth throughout the year is the least detrimental agricultural land use in soil carbon and AMF abundance and diversity, relative to the woodland reference.

Dataset Information

Diurnal patterns of productivity of arbuscular mycorrhizal fungi revealed with the Soil Ecosystem Observatory.

Publications

Diurnal patterns of productivity of arbuscular mycorrhizal fungi revealed with the Soil Ecosystem Observatory.

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