Different Effects of Soil Fertilization on Bacterial Community Composition in the Penicillium canescens Hyphosphere and in Bulk Soil

Abstract

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.

Hyphae move matter and microbes to mineral microsites: Integrating the hyphosphere into conceptual models of soil organic matter stabilization

“…The composition of the hyphal microbiome varies phylogenetically across fungal taxa, as well as across fungal guilds (i.e., mycorrhizal vs. saprotrophic), reflecting different needs for resource acquisition (e.g., organic matter decomposition vs. mineral nutrient acquisition; Pent et al, 2020). Bacterial community composition in the hyphosphere varies with nutritional demand in both mycorrhizal (Gorka et al, 2019; Wang et al, 2019); and saprotrophic fungi (Zhang et al, 2020), and the functional genomics of bacteria residing on a single fungal taxon can be experimentally altered based on nutrient addition (Zhang et al, 2020). Multiple lines of evidence suggest that the presence of individual fungal taxa can structure the composition and function of soil bacterial communities (Jeewani et al, 2021; Liu et al, 2018; Nuccio et al, 2013; Yuan et al, 2021; Zagryadskaya et al, 2011), which can subsequently impact organo‐mineral interactions (Jeewani et al, 2021).…”

“…For instance, soil structure affects not only the number of mineral sites available for MAOM formation, but also the extent of hyphal exploration (Ritz & Young, 2004; Witzgall et al, 2021), with some proportion of soil volume often inaccessible to hyphae due to small pore sizes. Moreover, emerging evidence suggests that different fungal and bacterial taxa may preferentially colonize different mineral types (Finley et al, 2021; Sun et al, 2020; Zhang et al, 2020), implying complex interactions between soil mineralogy and the microbes responsible for depositing the organic substrates at mineral surfaces (Jilling et al, 2018; Kleber et al, 2015). Understanding of these microbe–mineral interactions and their effects on the formation and cycling of MAOM is rapidly evolving, and will remain an important research driver for the foreseeable future.…”

Succession of the wheat seed-associated microbiome as affected by soil fertility level and introduction ofPenicilliumandBacillusinoculants in the field

“… 2018 , Zhang et al . 2020 ). Some of the dominating seed-associated taxa ( Erwinia , Pseudomonas , Salinibacterium and Sphingomonas ) might come with the seeds as endophytes (Özkurt et al .…”

Impact of Norway spruce pre-degradation stages induced by G. trabeum on fungal and bacterial communities

“…The abundance of several bacterial families ( Burkholderiaceaea , Microbacteriaceae and Acetobacteraceae ) showed a positive correlation with two fungal genera ( Penicillium and Trichoderma ) in all environments. In the context of wood degradation, bacteria could potentially take up carbon from fungal hyphae exudates or lignocellulose degradation products, while at the same time also supplying the fungi with essential nutrients such as nitrogen, phosphorus or zinc (Zhang et al ., 2020; Saravanan et al ., 2007; Schellenberger et al ., 2009; Kirker et al, 2017; Zelinka et al, 2021). Moreover, some bacteria can detoxify antifungal compounds and therefor they may also help to synergistically protect fungal species in the same environment (Nazir et al ., 2014).…”