Fungi and bacteria are found living together in a wide variety of environments. Their interactions are significant drivers of many ecosystem functions and are important for the health of plants and animals. A large number of fungal and bacterial families engage in complex interactions that lead to critical behavioural shifts of the microorganisms ranging from mutualism to antagonism. The importance of bacterial-fungal interactions (BFI) in environmental science, medicine and biotechnology has led to the emergence of a dynamic and multidisciplinary research field that combines highly diverse approaches including molecular biology, genomics, geochemistry, chemical and microbial ecology, biophysics and ecological modelling. In this review, we discuss recent advances that underscore the roles of BFI across relevant habitats and ecosystems. A particular focus is placed on the understanding of BFI within complex microbial communities and in regard of the metaorganism concept. We also discuss recent discoveries that clarify the (molecular) mechanisms involved in bacterial-fungal relationships, and the contribution of new technologies to decipher generic principles of BFI in terms of physical associations and molecular dialogues. Finally, we discuss future directions for research in order to stimulate synergy within the BFI research area and to resolve outstanding questions.

Abstract:In the field of microbial biomineralization, much of the scientific attention is focused on processes carried out by prokaryotes, in particular bacteria, even though fungi are also known to be involved in biogeochemical cycles in numerous ways. They are traditionally recognized as key players in organic matter recycling, as nutrient suppliers via mineral weathering, as well as large producers of organic acids such as oxalic acid for instance, an activity leading to the genesis of various metal complexes such as metal-oxalate. Their implications in the transformation of various mineral and metallic compounds has been widely acknowledged during the last decade, however, currently, their contribution to the genesis of a common biomineral, calcite, needs to be more thoroughly documented. Calcite is observed in many ecosystems and plays an essential role in the biogeochemical cycles of both carbon (C) and calcium (Ca). It may be physicochemical or biogenic in origin and numerous organisms have been recognized to control or induce its biomineralization. While fungi have often been suspected of being involved in this process in terrestrial environments, only scarce information supports this hypothesis in natural settings. As a result, calcite biomineralization by microbes is still largely attributed to bacteria at present. However, in some terrestrial environments there are particular calcitic habits that have been described as being fungal in origin. In addition to this, several studies dealing with axenic cultures of fungi have demonstrated the ability of fungi to produce calcite. Examples of fungal biomineralization range from induced to organomineralization processes. More examples of calcite biomineralization related to direct fungal activity, or at least to their presence, have been described within the last decade. However, the peculiar mechanisms leading to calcite biomineralization by fungi remain incompletely understood and more research is necessary, posing new exciting questions linked to microbial biomineralization processes.

The maintenance of energetically costly flagella by bacteria in non-water-saturated media, such as soil, still presents an evolutionary conundrum. Potential explanations have focused on rare flooding events allowing dispersal. Such scenarios, however, overlook bacterial dispersal along mycelia as a possible transport mechanism in soils. The hypothesis tested in this study is that dispersal along fungal hyphae may lead to an increase in the fitness of flagellated bacteria and thus offer an alternative explanation for the maintenance of flagella even in unsaturated soils. Dispersal along fungal hyphae was shown for a diverse array of motile bacteria. To measure the fitness effect of dispersal, additional experiments were conducted in a model system mimicking limited dispersal, using Pseudomonas putida KT2440 and its nonflagellated (⌬fliM) isogenic mutant in the absence or presence of Morchella crassipes mycelia. In the absence of the fungus, flagellar motility was beneficial solely under conditions of water saturation allowing dispersal, while under conditions limiting dispersal, the nonflagellated mutant exhibited a higher level of fitness than the wild-type strain. In contrast, in the presence of a mycelial network under conditions limiting dispersal, the flagellated strain was able to disperse using the mycelial network and had a higher level of fitness than the mutant. On the basis of these results, we propose that the benefit of mycelium-associated dispersal helps explain the persistence of flagellar motility in non-water-saturated environments.

The origin of soil mineralized nanofibres remains controversial. It is attributed to either biogenic factors or physicochemical processes. Scanning electron microscope and transmission electron microscope observations show that nanofibres could originate from the breakdown of fungal hyphae, especially its cell wall. It is hypothesized that during the decay of organic matter, cell wall microfibrils are released in the soil where they are exposed to mineralizing pore fluids, leading to their calcitic pseudomorphosis and/or are used as a template for calcite precipitation. When associated with needle fibre calcite bundles, nanofibres could indicate the relict of an organic sheath in which calcite has precipitated. This paper emphasizes the important roles of both organic matter and fungi in carbonatogenesis, and consequently in the soil carbon cycle.

The interactions between bacteria and fungi, the main actors of the soil microbiome, remain poorly studied. Here, we show that the saprotrophic and ectomycorrhizal soil fungus Morchella crassipes acts as a bacterial farmer of Pseudomonas putida, which serves as a model soil bacterium. Farming by M. crassipes consists of bacterial dispersal, bacterial rearing with fungal exudates, as well as harvesting and translocation of bacterial carbon. The different phases were confirmed experimentally using cell counting and 13 C probing. Common criteria met by other non-human farming systems are also valid for M. crassipes farming, including habitual planting, cultivation and harvesting. Specific traits include delocalization of food production and consumption and separation of roles in the colony (source versus sink areas), which are also found in human agriculture. Our study evidences a hitherto unknown mutualistic association in which bacteria gain through dispersal and rearing, while the fungus gains through the harvesting of an additional carbon source and increased stress resistance of the mycelium. This type of interaction between fungi and bacteria may play a key role in soils.

Fungi and bacteria form various associations that are central to numerous environmental processes. In the so-called fungal highway, bacteria disperse along fungal mycelium. We developed a novel tool for the in situ isolation of bacteria moving along fungal hyphae as well as for the recovery of fungi potentially involved in dispersal, both of which are attracted towards a target culture medium. We present the validation and the results of the first in situ test. Couples of fungi and bacteria were isolated from soil. Amongst the enriched organisms, we identified several species of fast-growing fungi (Fusarium sp. and Chaetomium sp.), as well as various potentially associated bacterial groups, including Variovorax soli, Olivibacter soli, Acinetobacter calcoaceticus, and several species of the genera Stenotrophomonas, Achromobacter and Ochrobactrum. Migration of bacteria along fungal hyphae across a discontinuous medium was confirmed in most of the cases. Although the majority of the bacteria for which migration was confirmed were also positive for flagellar motility, not all motile bacteria dispersed using their potential fungal partner. In addition, the importance of hydrophobicity of the fungal mycelial surface was confirmed. Future applications of the columns include targeting different types of microorganisms and their interactions, either by enrichment or by state of the art molecular biological methods.

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