Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists

Abstract

Bacteria and fungi can form a range of physical associations that depend on various modes of molecular communication for their development and functioning. These bacterial-fungal interactions often result in changes to the pathogenicity or the nutritional influence of one or both partners toward plants or animals (including humans). They can also result in unique contributions to biogeochemical cycles and biotechnological processes. Thus, the interactions between bacteria and fungi are of central importance to numerous biological questions in agriculture, forestry, environmental science, food production, and medicine. Here we present a structured review of bacterial-fungal interactions, illustrated by examples sourced from many diverse scientific fields. We consider the general and specific properties of these interactions, providing a global perspective across this emerging multidisciplinary research area. We show that in many cases, parallels can be drawn between different scenarios in which bacterial-fungal interactions are important. Finally, we discuss how new avenues of investigation may enhance our ability to combat, manipulate, or exploit bacterial-fungal complexes for the economic and practical benefit of humanity as well as reshape our current understanding of bacterial and fungal ecology.

Fig. 1.

Relevance of BFIs to different areas of scientific study.

Fig. 2.

The BFI equation. The combination of physical associations and molecular interactions between bacteria and fungi can result in a variety of different outcomes for each partner. In turn, these changes may affect the influence of the bacterial-fungal complex on their biotic and abiotic environment.

Fig. 3.

Role of autotrophic versus heterotrophic endobacteria in promoting fungal nutrition. (Left) Cartoon illustrating the nutritional relationship between Nostoc cyanobacteria and the lichenous fungus Geosiphon pyriforme during their BFI. Fungal cell structures such as vacuoles, nuclei, lipid bodies, and mitochondria are omitted for clarity. Carbon fixation occurs in photosynthetic cyanobacterial cells, while Nostoc heterocysts are able to fix atmospheric nitrogen (197, 198). Bacteria benefit from micronutrients supplied by the fungus, such as phosphate (356). Other nonphotosynthetic endobacteria living within the bladder may also supply fixed nitrogen to the fungus (355). (Right) Cartoon illustrating the role of Burkholderia rhizoxinica in the nutrition of Rhizopus microcarpus. In contrast to the cyanolichen example, the bacterium is not a primary producer of organic carbon or nitrogen for the fungus (208). However, the bacterial biosynthesis of the toxin rhizoxin is crucial for fungal pathogenicity toward rice seedlings and therefore to the fungal exploitation of plant-derived carbon and nitrogen (298). R. microcarpus also requires B. rhizoxinica for vegetative reproduction (299).

Fig. 4.

Interactions of pseudomonads with Agaricus bisporus lead to both positive and negative outcomes for the fungus, depending on the bacterial isolate and the developmental stage of the fungus. The toxin tolaasin is the primary factor responsible for brown blotch disease caused by P. tolaasii; other contributing factors are a secreted protease, lipase, and exopolysaccharide. *, mechanism unknown.

Fig. 5.

Coexistence and impact of bacteria and fungi in contrasting microbial ecosystems. Bacterial and fungal communities occupy overlapping niches in soil or when associated with plants and humans or other animals. Disturbing the communities that occupy these niches, for example, by the introduction or removal of key members, may alter the balance that exists between them. This can cause changes to the influences of bacteria and fungi on their niche, with consequences for the functioning of the ecosystem. BFIs may also result in novel effects in niches that do not occur in their absence.

Fig. 6.

Role of BFIs in ant-fungus mutualism. Nutrient flows and inhibitory interactions between organisms are indicated by arrows and blocked arrowheads, respectively. Major inputs of carbon (plant biomass) and nitrogen (plant biomass and nitrogen-fixing bacteria) provide the raw materials to support the web of interactions and are indicated with bold arrows. Ants transfer pathogenic Escovopsis fungi to their infrabuccal pocket during sanitization of the fungus garden.

Fig. 7.

Examples of some parallels among BFIs in different settings (22, 39, 56, 136, 141, 183, 188, 223, 283, 357, 371, 374).