The Mycobiota: Fungi Take Their Place Between Plants and Bacteria

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The Mycobiota: Fungi Take Their Place Between Plants and Bacteria Available online at www.sciencedirect.com ScienceDirect The mycobiota: fungi take their place between plants and bacteria Paola Bonfante, Francesco Venice and Luisa Lanfranco Eukaryotes host numerous intracellular and associated Mycobiota: fungi of the plant microbiota microbes in their microbiota. Fungi, the so-called Mycobiota, The knowledge that fungi live strictly associated with are important members of both human and plant microbiota. plants in diverse niches, particularly in the rhizosphere, Moreover, members of the plant mycobiota host their own dates back more than 100 years [3]. However, only a microbiota on their surfaces and inside their hyphae. The minor part of the mycobiome is cultivable, in line with microbiota of the mycobiota includes mycorrhizal helper what is known about fungal diversity, where only a small bacteria (for mycorrhizal fungi) and fungal endobacteria, which portion of the estimated 3.8 million species [4] are in are critical for the fungal host and, as such, likely affect the collections (http://www.wfcc.info/ccinfo/home/). Most of plant. This review discusses the contribution that these often- our knowledge of plant-associated fungi therefore comes overlooked members make to the composition and from molecular analysis, where the internal transcribed performance of the plant microbiota. spacer (ITS) of the nuclear rRNA operon is used as the official taxonomic barcode for fungi [5], providing Address species-level taxonomic delineation for most groups. Department of Life Sciences and Systems Biology, University of Torino, 10125, Torino, TO, Italy Emerging ‘omics’ techniques, as well as the concept of the microbiota as an additional plant genome (alongside Corresponding author: Bonfante, Paola ([email protected]) the nuclear and organellar genomes), offer new views of fungal diversity. The numbers of operational taxonomic units (OTUs) units increase with sequencing and sam- pling depth [6 ], suggesting that many members of the mycobiota remain to be discovered. Fungi proliferate in Current Opinion in Microbiology 2019, 49:18–25 different environments (soil, air, water) and with different This review comes from a themed issue on Environmental microbiology nutritional strategies (saprotrophic, biotrophic, parasitic), but the highest numbers of fungi are found to be plant- Edited by Roeland Berendsen and Klaus Schlaeppi associated and in the soil. These findings suggested a For a complete overview see the Issue and the Editorial remarkable fungal/plant species ratio of 17/1. Moreover, Available online 22nd October2019 these approaches revealed a variety of fungal communi- https://doi.org/10.1016/j.mib.2019.08.004 ties associated with myriad plants in diverse environ- ments [7]. 1369-5274/ã 2019 Elsevier Ltd. All rights reserved. Pioneering reports on the plant microbiota focused on identifying Arabidopsis thaliana bacterial assemblages [8], but recent papers consider eukaryotic and prokaryotic components of the microbiota. For example, Bergelson et al. [9] grew a worldwide panel of A. thaliana accessions Introduction and found that fungi influence root microbiota structure. The Fungal kingdom encompasses a plethora of eukary- Ascomycota andBasidiomycota are more common in leaves otic species that proliferate in diverse environments; than in roots, whereas Mortierellomycota are moderately fungi also have important roles as components of the enriched in the root microbiota. Irrespective of their quali- tative differences, the leaf and root microbiotas had similar microbiota, where they act as symbionts, endophytes, parasites, or saprotrophs. Characterizing the microbiota fungal richness. Moving from identity to functions, Almario of diverse species across kingdoms has revealed an unex- et al. [10] identified 15 fungal taxa consistently present in the root of Arabis alpina, including a Helotiales taxon that pected double nature of the fungi in the microbiome: they colonize higher eukaryotes from humans to plants [1,2 ]. colonizes the root endosphere and transfers phosphate to the plant. Similar functions have been described for the In the mean time, as with all other eukaryotes, fungi host endophyte Colletotrichum tofieldiae [11 ] and an endophytic their own microbiota, consisting of microbial communi- ties that adhere to the hyphal surface, develop among the strain of Fusarium solani was found to protect against root pseudotissues produced by hyphal aggregation, or colo- and foliar pathogens [12]. Emerging work is therefore discovering novel, beneficial members of the mycobiota nize the fungal cytoplasm. In this review, we illustrate the double role played by fungi in the microbiota (Figure 1). in addition to long-standing studies on mycorrhizal fungi. Current Opinion in Microbiology 2019, 49:18–25 www.sciencedirect.com Fungi, plants, bacteria Bonfante, Venice and Lanfranco 19 Figure 1 Endobacteria End obacteria Endobacteria Fungal Associated Associated Associated (Mycoavidus (Ca. Glomer ibacter (Burkolderia microbiota bacteria cysteinexigens) bacteria gigas porarum) bacteria rhizoxinica) Symbi onts/ Saprotrophs Beneficial endophytes Pathogens (Mortierella, Endogone) (Arbu scular mycorrhizal (Rhizopus) fungi; Serendipita) MYCOBIOTA Fun gal commun ities Plant Microbiota Bacterial commun ities Saprotroph s Symbionts Pathogens Current Opinion in Microbiology The flow chart offers a map to the Mycobiota as a component of the more complex Plant Microbiota. The fungal communities consist of saprotrophic, symbiotic and pathogenic fungi. On their own, these fungi may associate with soil bacteria or host endobacteria, which represent the more intimate form of interaction. These bacterial communities in their whole add a further level of complexity to the microbial component of the Plant Microbiota. Living in association with plants and exploring the soil with with ecto- and arbuscular mycorrhizal fungi (AMF), and their network of extraradical hyphae make mycorrhizal belongto very diverse taxa including Proteobacteria such as fungi a perfect example of the plant microbiota. Their Pseudomonas and Oxalobacteracea, Actinomycetes such as diversity in the most different environments has been Streptomyces, and Firmicutes such as Bacillus [16,17]. MHB deeply investigated [13]. may enhance mycorrhizal functions, provide nutrients to the fungus and plant, and promote defenses. For example, Notwithstanding some pitfalls and potential biases when the fructose exuded by the AMF Rhizophagus irregularis applied to fungal communities [7], high-throughput stimulates phosphatase expression and secretion in the sequencing has shown that fungi are unexpectedly MHB Rahnella aquatilis, thus promoting the mineralization diverse, important members of the plant microbiota. of organic phosphorus (i.e. phytate) into inorganic phos- The challenge for the future will be to unravel phorus [18].Even if establishedinfully artificial conditions, the complex interactions among fungi and neighboring this system reveals an interesting cooperation between bacteria, and their effects on host physiology and metab- AMF and bacteria. olism [14]. High-throughput sequencing gave a wider description of From nutrient transfer to truffles: fungal- MHB communities: Iffis et al. [19] identified the domi- associated bacterial communities nant AMF-associated bacterial OTUs in the roots of Mycobiota-associated bacteria have diverse effects on their plants growing in hydrocarbon-polluted soils. Vik et al. interacting fungi and plants, from nutrient transfer to [20] explored the bacterial community composition of the production of aromatic metabolites. Mycorrhiza helper ectomycorrhizal roots of Bistorta vivipara and concluded bacteria (MHB) were the first to be acknowledged for their that Actinobacteria were significantly more abundant in positive effects; identified by Garbaye [15 ], they interact ectomycorrhizas than in soil. A detailed profile of bacterial www.sciencedirect.com Current Opinion in Microbiology 2019, 49:18–25 20 Environmental microbiology communities associated with Pinus sylvestris roots colonized health, as well as drug, food, and toxin production by different fungi demonstrated that each ectomycorrhizal (reviewed in Deveau et al. [25]). In the fungal microbiota, root harboured distinct bacterial communities [21]. ‘fungiphiles’ explore soil niches using saprotrophic fungi as substrates [26] while others use mycorrhizal fungi as a Other root-associated fungi have their own microbiota. highway to reach plant organs [27]. The phyllosphere Glancing at a truffle under an electron microscope in the microbial community is also strongly influenced by the pre-microbiota era was a shocking experience that interaction between microorganisms: particular taxa, revealed diverse bacteria proliferating around the aggre- including fungi, act as ‘hub microbes’ due to their rele- gating hyphae forming the fruiting body (Figure 2). The vance in shaping the plant microbiota [28]. In another existence of this complex system of bacteria and fungi special environment, cheese rinds, Serratia isolates dis- opened the question of whether we are smelling and perse on fungal networks by swimming in the liquid tasting bacteria or the precious truffles. Indeed, the Tuber layers formed on Mucor hyphae [29]. Indeed, by mecha- borchii bacterial communities are dominated by a-proteo- nisms including flagella-mediated motility, fungal- bacteria and b-proteobacteria [22], which produce sul- associated bacterial dispersal can shift the cheese rind phur-containing volatiles such
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