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.

Bacterial-Fungal Interactions: Hyphens between Agricultural, Clinical, Environmental, and Food Microbiologists

Fungi of the genus Trichoderma are soilborne, green-spored ascomycetes that can be found all over the world. They have been studied with respect to various characteristics and applications and are known as successful colonizers of their habitats, efficiently fighting their competitors. Once established, they launch their potent degradative machinery for decomposition of the often heterogeneous substrate at hand. Therefore, distribution and phylogeny, defense mechanisms, beneficial as well as deleterious interaction with hosts, enzyme production and secretion, sexual development, and response to environmental conditions such as nutrients and light have been studied in great detail with many species of this genus, thus rendering Trichoderma one of the best studied fungi with the genome of three species currently available. Efficient biocontrol strains of the genus are being developed as promising biological fungicides, and their weaponry for this function also includes secondary metabolites with potential applications as novel antibiotics. The cellulases produced by Trichoderma reesei, the biotechnological workhorse of the genus, are important industrial products, especially with respect to production of second generation biofuels from cellulosic waste. Genetic engineering not only led to significant improvements in industrial processes but also to intriguing insights into the biology of these fungi and is now complemented by the availability of a sexual cycle in T. reesei/Hypocrea jecorina, which significantly facilitates both industrial and basic research. This review aims to give a broad overview on the qualities and versatility of the best studied Trichoderma species and to highlight intriguing findings as well as promising applications.

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Biology and biotechnology of Trichoderma

This review focuses on bacteria-fungi interactions mediated by secondary metabolites that occur in the environment and have implications for medicine and biotechnology Bipartite interactions that affect agriculture as well as relationships involving additional partners (plants and animals) are discussed The advantages of microbial interplay for food production and the risks regarding food safety are presented Furthermore, recent developments in decoding the impact of bacteria-fungi interactions on infection processes and their implications for human health are highlighted In addition, this reviews aims to demonstrate how the understanding of complex microbial interactions found in nature can be exploited for the discovery of new therapeutics

Molecular bacteria-fungi interactions: effects on environment, food, and medicine.

Trichoderma spp. are effective biocontrol agents for many plant pathogens, thus the mechanism of Trichoderma-induced plant resistance is not fully understood. In this study, a novel Trichoderma strain was identified, which could promote plant growth and reduce the disease index of gray mold caused by Botrytis cinerea in cucumber. To assess the impact of Trichoderma inoculation on the plant response, a multi-omics approach was performed in the Trichoderma-inoculated cucumber plants through the analyses of the plant transcriptome, proteome, and phytohormone content. A novel Trichoderma strain was identified by morphological and molecular analysis, here named T. longibrachiatum H9. Inoculation of T. longibrachiatum H9 to cucumber roots promoted plant growth in terms of root length, plant height, and fresh weight. Root colonization of T. longibrachiatum H9 in the outer layer of epidermis significantly inhibited the foliar pathogen B. cinerea infection in cucumber. The plant transcriptome and proteome analyses indicated that a large number of differentially expressed genes (DEGs) and differentially expressed proteins (DEPs) were identified in cucumber plants 96 h post T. longibrachiatum H9 inoculation. Up-regulated DEGs and DEPs were mainly associated with defense/stress processes, secondary metabolism, and phytohormone synthesis and signaling, including jasmonic acid (JA), ethylene (ET) and salicylic acid (SA), in the T. longibrachiatum H9-inoculated cucumber plants in comparison to untreated plants. Moreover, the JA and SA contents significantly increased in cucumber plants with T. longibrachiatum H9 inoculation. Application of T. longibrachiatum H9 to the roots of cucumber plants effectively promoted plant growth and significantly reduced the disease index of gray mold caused by B. cinerea. The analyses of the plant transcriptome, proteome and phytohormone content demonstrated that T. longibrachiatum H9 mediated plant systemic resistance to B. cinerea challenge through the activation of signaling pathways associated with the phytohormones JA/ET and SA in cucumber.

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Involvement of jasmonic acid, ethylene and salicylic acid signaling pathways behind the systemic resistance induced by Trichoderma longibrachiatum H9 in cucumber.

Microbially based biocontrol of plant diseases differs fundamentally from chemical control, but pesticide regulations for microbial and chemical pesticides remain similar. In the United States, the Food, Insecticide, Fungicide and Rodenticide Act (FIFRA) (19), like similar laws in other countries, requires any material making a pesticidal claim to be registered. The Act was in response to widespread concern regarding the safety and environmental effects of pesticides. Registration requires significant effort, time, and expense to conduct toxicological, environmental, and in some cases, efficacy testing. However, the nature and advantages of chemicals and microbials are quite different, especially between chemical fungicides and endophytic symbiotic microbes that act through changes in plant gene expression. Further, some organisms with pest control activities were never covered by FIFRA, including obligate symbionts such as rhizobia and mycorrhizal fungi and larger organisms such as nematodes and predatory insects. Furthermore, FIFRA and similar regulations are designed primarily for specific, individual agents, and not for complex mixtures such as composts, manures, and teas made from these largely unregulated sources, even though they have activity against plant pests and their active ingredients may be similar to those in registered pesticides. In addition, pesticide regulations cover only materials that make specific pesticidal claims, i.e., they do not cover agents that make claims for general improvement of plant health and plant quality. Finally, there is great potential for use of microbial agents in the developing world, although full-scale production, marketing, and registration are simply too expensive for these societies. To overcome this economic difficulty, some countries have substituted locally produced products for imported ones (2,55). There are numerous microbial products listed for the control of various pathogens, insects, or weeds. Copping (14) lists 17 species or strains of fungi or bacteria that have been commercialized for insect control, 37 for control of pathogens or nematodes, and 14 mycoherbicides. This must be an underestimate; Faria and Wraight (20) list 171 commercial mycoinsecticides and mycoacaricides over 12 species or subspecies of fungi. Even this is an underestimate because these authors did not include many nonregistered products or those produced by governmental agencies. In fact, many products or preparations with activity against plant pathogens or other pests are not registered pesticides. Instead, they may be marketed as plant inoculants or plant strengthening agents, which gives these products a marketplace advantage because the time and money necessary for registration are avoided. Moreover, because many microbial agents can be propagated easily, local distribution systems have been developed. As a consequence, biocontrol production, distribution, and methods of use have evolved in diverse ways, each of which has advantages and disadvantages. There are strong incentives to develop biological products that fall outside the registered pesticide model, and it is likely that more products with pesticidal activity will be sold outside this framework. Much of this paper will deal with biocontrol based on Trichoderma strains, but other systems will be discussed as well. Finally, there are safety implications for the different systems that have evolved, but modern taxonomic studies provide insight into this aspect and also will be discussed. It is important to consider the perceived benefits that microbial agents have in different parts of the world. In the United States and other developed countries, the agents are considered to be useful but not essential. However, in the developing world, as perceived by the Association of Asian Pacific Agricultural Research Institutions (AAPARI), biopesticides and biofertilizers are considered extremely important. Applicators in the developing world may not wear protective clothing (communication in AAPARI meeting cited in Acknowledgments), so there may be serious health hazards to the use of toxic chemical agents. In addition, fertilizers are rapidly becoming too expensive for use by smallholders in many parts of the world, and biofertilizers in their various forms are considered to be essential components of food security in many countries.

https://apsjournals.apsnet.org/doi/pdf/10.1094/PDIS-94-8-0928

Changing Models for Commercialization and Implementation of Biocontrol in the Developing and the Developed World

Green mold of Pleurotus ostreatus, caused by Trichoderma species, has recently resulted in crop losses worldwide. Therefore, there is an emerging need for rapid means of diagnosing the causal agents. A PCR assay was developed for rapid detection of Trichoderma pleurotum and Trichoderma pleuroticola, the two pathogens causing green mold of P. ostreatus. Three oligonucleotide primers were designed for identifying these species in a multiplex PCR assay based on DNA sequences within the fourth and fifth introns in the translation elongation factor 1α gene. The primers detected the presence of T. pleurotum and/or T. pleuroticola directly in the growing substrates of oyster mushrooms, without the need for isolating the pathogens. The assay was used to assess the presence of the two species in natural environments in which P. ostreatus can be found in Hungary, and demonstrated that T. pleuroticola was present in the growing substrates and on the surface of the basidiomes of wild oyster mushrooms. Other Trichoderma species detected in these substrates and habitats were Trichoderma harzianum, Trichoderma longibrachiatum and Trichoderma atroviride. Trichoderma pleurotum was not found in any of the samples from the forested areas tested in this study.

Molecular identification of Trichoderma species associated with Pleurotus ostreatus and natural substrates of the oyster mushroom.

Although oyster mushroom (Pleurotus spp.) is a valuable food, cultivated worldwide on an industrial scale, still very little is known about the microbial dynamics during oyster mushroom substrate preparation. Therefore, the characterization of the microbial dynamics by chemical and biological tools was the objective of this study. During substrate preparation, enzymatic digestibility of the substrate improved by 77%, whereas the cellulose and hemicellulose to lignin ratios decreased by 9% and 19%, respectively. Fluorescein diacetate hydrolysis reached its minimum value at the temperature maximum of the process during the composting phase and exceeded the initial level at the end of the process. Fungal species played part in the initial mesophilic phase of the substrate preparation process, but they disappeared after pasteurization in tunnels at constant elevated temperatures. Changes in the microbiota showed a marked bacterial community succession during substrate preparation investigated by 16S ribosomal deoxyribonucleic acid-based terminal restriction fragment length polymorphism (T-RFLP). Mature samples represented the least variance, which indicated the effect of the standardized preparation protocol. The relation between mushroom yield and the bacterial community T-RFLP fingerprints was investigated, but the uniformity of mushroom yields did not support any significant correlation.

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Papers

Molecular identification of Trichoderma species associated with Pleurotus ostreatus and natural substrates of the oyster mushroom.

Microbial community structure changes during oyster mushroom substrate preparation.

Characterization of pseudomonads isolated from decaying sporocarps of oyster mushroom