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Fungal-Bacterial Cooccurrence Patterns Differ between Arbuscular Mycorrhizal Fungi and Nonmycorrhizal Fungi across Soil Niches.

ABSTRACT: 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.

SUBMITTER: Yuan MM

PROVIDER: S-EPMC8092305 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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.

Project description:UnlabelledWe investigated communities of arbuscular mycorrhizal fungi (AMF) in the roots and the rhizosphere soil of Brachypodium retusum in six different natural soils under field conditions. We explored phylogenetic patterns of AMF composition using indicator species analyses to find AMF associated with a given habitat (root versus rhizosphere) or soil type. We tested whether the AMF characteristics of different habitats or contrasting soils were more closely related than expected by chance. Then we used principal-component analysis and multivariate analysis of variance to test for the relative contribution of each factor in explaining the variation in fungal community composition. Finally, we used redundancy analysis to identify the soil properties that significantly explained the differences in AMF communities across soil types. The results pointed out a tendency of AMF communities in roots to be closely related and different from those in the rhizosphere soil. The indicator species analyses revealed AMF associated with rhizosphere soil and the root habitat. Soil type also determined the distribution of AMF communities in soils, and this effect could not be attributed to a single soil characteristic, as at least three soil properties related to microbial activity, i.e., pH and levels of two micronutrients (Mn and Zn), played significant roles in triggering AMF populations.ImportanceCommunities of arbuscular mycorrhizal fungi (AMF) are main components of soil biota that can determine the productivity of ecosystems. These fungal assemblages vary across host plants and ecosystems, but the main ecological processes that shape the structures of these communities are still largely unknown. A field study in six different soil types from semiarid areas revealed that AMF communities are significantly influenced by habitat (soil versus roots) and soil type. In addition, three soil properties related to microbiological activity (i.e., pH and manganese and zinc levels) were the main factors triggering the distribution of AMF. These results contribute to a better understanding of the ecological factors that can shape AMF communities, an important soil microbial group that affects multiple ecosystem functions.

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Fungal-Bacterial Cooccurrence Patterns Differ between Arbuscular Mycorrhizal Fungi and Nonmycorrhizal Fungi across Soil Niches.

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