The Role of the Microbiome of Truffles in Aroma Formation: a Meta-Analysis Approach

Abstract

dTruffles (Tuber spp.) are ascomycete subterraneous fungi that form ectomycorrhizas in a symbiotic relationship with plant roots. Their fruiting bodies are appreciated for their distinctive aroma, which might be partially derived from microbes. Indeed, truffle fruiting bodies are colonized by a diverse microbial community made up of bacteria, yeasts, guest filamentous fungi, and viruses. The aim of this minireview is two-fold. First, the current knowledge on the microbial community composition of truffles has been synthesized to highlight similarities and differences among four truffle (Tuber) species (T. magnatum, T. melanosporum, T. aestivum, and T. borchii) at various stages of their life cycle. Second, the potential role of the microbiome in truffle aroma formation has been addressed for the same four species. Our results suggest that on one hand, odorants, which are common to many truffle species, might be of mixed truffle and microbial origin, while on the other hand, less common odorants might be derived from microbes only. They also highlight that bacteria, the dominant group in the microbiome of the truffle, might also be the most important contributors to truffle aroma not only in T. borchii, as already demonstrated, but also in T. magnatum, T. aestivum, and T. melanosporum. Microbes can be found almost everywhere on our planet. They colonize many different types of habitats, among them living organisms, such as plant roots or insect and human guts. Classical microbiological methods have long offered a spotlight view on microbial diversity. Recent high-throughput molecular techniques have revolutionized the field of microbial ecology by unraveling an enormous microbial diversity in numerous organisms and highlighting the deep impact of microbiomes of their host physiology and behavior (1, 2). Truffle fungi are no exception, since they are colonized by a complex microbial community made up of bacteria, yeasts, guest filamentous fungi, and viruses (3-14).Truffles are subterranean ascomycete fungi that form ectomycorrhizas in symbiotic relationship with plant roots (15). Their fruiting bodies are appreciated for their distinctive aroma, which is partially derived from microbes (6,14,16). The aim of this minireview is to synthesize the current knowledge on the composition of the microbial community of truffles and discuss their potential role in truffle aroma formation, specifically focusing on volatiles that are responsible for human-perceived truffle aroma (defined as odorants). TRUFFLE MICROBIOMESTruffles are colonized by microbes at all stages of their life cycle, which include a symbiotic stage in association with a host plant (ectomycorrhiza), a sexual stage (fruiting bodies), and a free-living mycelial stage, which might serve an exploratory purpose in the soil. To date, microbes and microbial communities have been characterized in truffles with culture-dependent and -independent techniques in Ͼ15 papers (3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(17)(18)(19)(20)(21). Various life cycle stages of four...

Growing edible mushrooms: a conversation between bacteria and fungi

“…Among cultivated Ascomycetes, truffles are colonized by microbes at all stages of their life cycle: symbiotic stage (ectomycorrhiza), fruiting bodies and mycelia (Vahdatzadeh et al, 2015). Black truffle ascocarps provide an habitat to complex bacterial communities, which is dynamic and evolves during the maturation of the ascocarps (Antony-Babu et al, 2014).…”

“…Black truffle ascocarps provide an habitat to complex bacterial communities, which is dynamic and evolves during the maturation of the ascocarps (Antony-Babu et al, 2014). Interestingly, bacteria, the dominant kingdom among truffle-associated microorganisms, have been postulated to be the most important contributors to truffle aromas (Vahdatzadeh et al, 2015). This raises the intriguing possibility that in a natural setting, the VOCs released by the bacterial microbiome of truffles play an important role in attracting the mammals and insects that act as vectors for truffle dispersal.…”

Root‐tip cutting and uniconazole treatment improve the colonization rate of Tuber indicum on Pinus armandii seedlings in the greenhouse

“…Alphaproteobacteria and Deltaproteobacteria (both in the phylum Proteobacteria) were found to be more abundant in the rhizosphere soil of root tip‐cut or 10 mg l −1 uniconazole‐treated colonized seedlings than in control rhizosphere soil. Previous studies also found that α‐Proteobacteria and γ‐Proteobacteria comprised the predominant components of the bacterial communities of truffles (Barbieri et al , ; Vahdatzadeh et al , ; Li et al , ). Previous studies have demonstrated that Pseudomonas fluorescens (Proteobacteria) improved the establishment and functioning of ectomycorrhizal symbiosis (Dominguez et al , ).…”

“…They can promote the growth of plants, increase the uptake of mineral elements and enhance the tolerance of plants to stress including drought stress, high salinity stress and disease stress (Abiala et al , ; Bell et al , ; Alegria Terrazas et al , ; Baldrian, ). Bacteria in the soil or associated with truffle ascocarps were found to play important roles in truffle maturation and production of volatile organic compounds (Barbieri et al , ; Antony‐Babu et al , ; Splivallo et al , ; Vahdatzadeh et al , ). Mycorrhiza helper bacteria (MHB) are a group of organisms that could stimulate the formation of mycorrhizal symbiosis (Deveau and Labbé, ).…”

Component features, odor‐active volatiles, and acute oral toxicity of novel white‐colored truffle Tuber japonicum native to Japan

“…Therefore, the odor characteristics of T. magnatum and T. japonicum had obvious differences. Many reports have shown that truffle aroma varies depending on the ripening stage (Saltarelli et al, 2008;Zeppa et al, 2004), with some assessing the microorganisms involved in forming the truffle aroma (Splivallo et al, 2015;Vahdatzadeh, Deveau, & Splivallo, 2015). Many reports have shown that truffle aroma varies depending on the ripening stage (Saltarelli et al, 2008;Zeppa et al, 2004), with some assessing the microorganisms involved in forming the truffle aroma (Splivallo et al, 2015;Vahdatzadeh, Deveau, & Splivallo, 2015).…”