Dataset Information

A novel baiting microcosm approach used to identify the bacterial community associated with Penicillium bilaii hyphae in soil.

ABSTRACT: It is important to identify and recover bacteria associating with fungi under natural soil conditions to enable eco-physiological studies, and to facilitate the use of bacterial-fungal consortia in environmental biotechnology. We have developed a novel type of baiting microcosm, where fungal hyphae interact with bacteria under close-to-natural soil conditions; an advantage compared to model systems that determine fungal influences on bacterial communities in laboratory media. In the current approach, the hyphae are placed on a solid support, which enables the recovery of hyphae with associated bacteria in contrast to model systems that compare bulk soil and mycosphere soil. We used the baiting microcosm approach to determine, for the first time, the composition of the bacterial community associating in the soil with hyphae of the phosphate-solubilizer, Penicillium bilaii. By applying a cultivation-independent 16S rRNA gene-targeted amplicon sequencing approach, we found a hypha-associated bacterial community with low diversity compared to the bulk soil community and exhibiting massive dominance of Burkholderia OTUs. Burkholderia is known be abundant in soil environments affected by fungi, but the discovery of this massive dominance among bacteria firmly associating with hyphae in soil is novel and made possible by the current bait approach.

SUBMITTER: Ghodsalavi B

PROVIDER: S-EPMC5659649 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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A novel baiting microcosm approach used to identify the bacterial community associated with Penicillium bilaii hyphae in soil.

Ghodsalavi Behnoushsadat B Svenningsen Nanna Bygvraa NB Hao Xiuli X Olsson Stefan S Nicolaisen Mette Haubjerg MH Al-Soud Waleed Abu WA Sørensen Søren J SJ Nybroe Ole O

PloS one 20171027 10

It is important to identify and recover bacteria associating with fungi under natural soil conditions to enable eco-physiological studies, and to facilitate the use of bacterial-fungal consortia in environmental biotechnology. We have developed a novel type of baiting microcosm, where fungal hyphae interact with bacteria under close-to-natural soil conditions; an advantage compared to model systems that determine fungal influences on bacterial communities in laboratory media. In the current appr ...[more]

PMID: 29077733

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Project description:This study investigated the effects of long-term soil fertilization on the composition and potential for phosphorus (P) and nitrogen (N) cycling of bacterial communities associated with hyphae of the P-solubilizing fungus Penicillium canescens Using a baiting approach, hyphosphere bacterial communities were recovered from three soils that had received long-term amendment in the field with mineral or mineral plus organic fertilizers. P. canescens hyphae recruited bacterial communities with a decreased diversity and an increased abundance of Proteobacteria relative to what was observed in soil communities. As core bacterial taxa, Delftia and Pseudomonas spp. were present in all hyphosphere samples irrespective of soil fertilization. However, the type of fertilization showed significant impacts on the diversity, composition, and distinctive taxa/operational taxonomic units (OTUs) of hyphosphere communities. The soil factors P (Olsen method), exchangeable Mg, exchangeable K, and pH were important for shaping soil and hyphosphere bacterial community compositions. An increased relative abundance of organic P metabolism genes was found in hyphosphere communities from soil that had not received P fertilizers, which could indicate P limitation near the fungal hyphae. Additionally, P. canescens hyphae recruited bacterial communities with a higher abundance of N fixation genes than found in soil communities, which might imply a role of hyphosphere communities for fungal N nutrition. Furthermore, the relative abundances of denitrification genes were greater in several hyphosphere communities, indicating an at least partly anoxic microenvironment with a high carbon-to-N ratio around the hyphae. In conclusion, soil fertilization legacy shapes P. canescens hyphosphere microbiomes and their functional potential related to P and N cycling.IMPORTANCE P-solubilizing Penicillium strains are introduced as biofertilizers to agricultural soils to improve plant P nutrition. Currently, little is known about the ecology of these biofertilizers, including their interactions with other soil microorganisms. This study shows that communities dominated by Betaproteobacteria and Gammaproteobacteria colonize P. canescens hyphae in soil and that the compositions of these communities depend on the soil conditions. The potential of these communities for N and organic P cycling is generally higher than that of soil communities. The high potential for organic P metabolism might complement the ability of the fungus to solubilize inorganic P, and it points to the hyphosphere as a hot spot for P metabolism. Furthermore, the high potential for N fixation could indicate that P. canescens recruits bacteria that are able to improve its N nutrition. Hence, this community study identifies functional groups relevant for the future optimization of next-generation biofertilizer consortia for applications in soil.

Project description:The rate, timing, and mode of species dispersal is recognized as a key driver of the structure and function of communities of macroorganisms, and may be one ecological process that determines the diversity of microbiomes. Many previous studies have quantified the modes and mechanisms of bacterial motility using monocultures of a few model bacterial species. But most microbes live in multispecies microbial communities, where direct interactions between microbes may inhibit or facilitate dispersal through a number of physical (e.g., hydrodynamic) and biological (e.g., chemotaxis) mechanisms, which remain largely unexplored. Using cheese rinds as a model microbiome, we demonstrate that physical networks created by filamentous fungi can impact the extent of small-scale bacterial dispersal and can shape the composition of microbiomes. From the cheese rind of Saint Nectaire, we serendipitously observed the bacterium Serratia proteamaculans actively spreads on networks formed by the fungus Mucor. By experimentally recreating these pairwise interactions in the lab, we show that Serratia spreads on actively growing and previously established fungal networks. The extent of symbiotic dispersal is dependent on the fungal network: diffuse and fast-growing Mucor networks provide the greatest dispersal facilitation of the Serratia species, while dense and slow-growing Penicillium networks provide limited dispersal facilitation. Fungal-mediated dispersal occurs in closely related Serratia species isolated from other environments, suggesting that this bacterial-fungal interaction is widespread in nature. Both RNA-seq and transposon mutagenesis point to specific molecular mechanisms that play key roles in this bacterial-fungal interaction, including chitin utilization and flagellin biosynthesis. By manipulating the presence and type of fungal networks in multispecies communities, we provide the first evidence that fungal networks shape the composition of bacterial communities, with Mucor networks shifting experimental bacterial communities to complete dominance by motile Proteobacteria. Collectively, our work demonstrates that these strong biophysical interactions between bacterial and fungi can have community-level consequences and may be operating in many other microbiomes.

Dataset Information

A novel baiting microcosm approach used to identify the bacterial community associated with Penicillium bilaii hyphae in soil.

Publications

A novel baiting microcosm approach used to identify the bacterial community associated with Penicillium bilaii hyphae in soil.

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