Makoto Kimura
Hiromi Nishida2
Masashi Kato
Masatoshi Goto
Tomoyuki Nakagawa- 1Department of Applied Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi, Japan
- 2Department of Food and Life Sciences, Toyo University, Itakura, Gunma, Japan
- 3Faculty of Agriculture, Meijo University, Nagoya, Aichi, Japan
- 4Department of Applied Biochemistry and Food Science, Faculty of Agriculture, Saga University, Saga, Japan
- 5Faculty of Applied Biological Sciences, Gifu University, Gifu, Japan
Editorial on the Research Topic
Microorganisms and their metabolism affecting quality, safety and functionality of agricultural products
Microorganisms are closely associated with agriculture and food industries in both beneficial and detrimental ways. As the beneficial use of microorganisms, humans have taken advantage of their activities for preserving, flavoring, and enriching the agricultural products through fermentation. Since the early ages of crop cultivation, yeasts and molds inhabiting raw materials in the environment have been used for processing, which has led to the emergence of indigenous food cultures with unique tastes and odors. Despite the long history of traditional fermentation, it was not until the mid-19th century, when Louis Pasteur elucidated the chemical processes associated with life and structural integrity of yeast cells, that alcoholic fermentation has come to be recognized as the result of microbial activity (Barnett, 2003). In contrast to the positive impact of fermentation, the metabolic activities of some microorganisms can adversely affect human health by poisoning agricultural products. The description of such a negative impact was made by Louis René Tulasne in 1853, belonging to the same era as when Pasteur established the concept of fermentation, who showed that toxic ergot sclerotia were produced by a fungus, but not by the rye itself (Haarmann et al., 2009). The pathogenic Claviceps fungus was later shown to synthesize ergot alkaloid mycotoxins in the sclerotia, after which time the control of mycotoxins in agricultural products has become an important issue for ensuring food safety. In the light of the importance of microbial metabolism in such double-edged ways, the present Research Topic accepted five original research papers and one perspective paper (from a total of 13 submissions), which have expanded the scientific knowledge of the relevant microorganisms by using advanced modern technology, as outlined below.
Sake is a traditional Japanese rice wine made by advanced parallel double fermentation that involves starch saccharification of steamed rice grains by Aspergillus oryzae (known as the koji mold; the solid rice culture is called koji) and simultaneous alcoholic fermentation by the yeast Saccharomyces cerevisiae. Other than the common eukaryotic fermenting microorganisms used in sake production, bacteria inhabiting the sake breweries (described as kuratsuki in Japanese) have been identified by using massive parallel DNA sequencing, revealing the diversity of microbial flora during sake production in different breweries. This finding has led to the hypothesis that the specific flavor and taste of sake products possibly arose from interactions between brewery-specific kuratsuki bacteria and yeasts (Nishida, 2021). Indeed, functional studies of such recently isolated and characterized kuratsuki bacteria have provided insights into their involvement in making the flavor and taste of sake during the brewing process (Yazaki and Nishida, 2023). In close connection with this theory, Ito et al. describe the diversity and dynamics of the microbiome during the production process of sake at a local brewery in Kawaba village, a relatively isolated mountainous area bordering north of the Kanto Plain in Japan. By comparing the amplicon sequence variants of the 16S rRNA gene in the fermentation starter moto vs. the external environment, they demonstrated that autochthonous bacteria in the built environments, equipment surfaces, and raw materials have moved into moto in the brewery. It is also noteworthy that the relative abundances of microbes from the external environment have changed during moto fermentation.
In addition to the metagenomics studies of traditional sake manufacturing process, this Research Topic includes two papers, in which the authors sought to improve fermentation and microbial products for industrial applications. Liu et al. describe their efforts to improve the quality of cider, a widely consumed alcoholic beverage produced by the fermentation of apple juice. It has been known that wild microbes present in the pericarps and stems often interfere with natural fermentation by autochthonous yeasts, thereby preventing high-quality cider production on an industrial scale (Lorenzini et al., 2019). With the ultimate goal of improving the quality and style of ciders, they screened and selected yeast starter strains with diverse characteristics by using a conventional olfactory test. Several candidate strains were characterized in terms of sugar utilization, methanol production, and volatile profiles, which could be explained by the relative transcription levels of genes associated with sugar metabolism, stress tolerance, and/or aroma production. The application of new strains that complement the conventional natural fermentation by autochthonous yeasts is expected to satisfy consumer demand and promote cider industry development. Another study by Wang et al. deals with polyunsaturated fatty acids (PUFAs), such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), which have numerous health benefits throughout human life. For the production of PUFAs, Schizochytrium is considered as one of the alternative sources to fish oils, as this eukaryotic heterotrophic microalagae can produce high levels of such functional food ingredients (Chang et al., 2013). As a first step toward achieving an industrial-level of PUFA production by Schizochytrium, the authors explored the possibility of using chemical modulators. Consequently, they found an increased ratio of PUFAs to saturated fatty acids, as well as increased production of PUFAs, by the addition of 1,3-propanediol. In cultures of Schizochytrium amended with varying doses and ratios of propanol and 1,3-propanediol, total fatty acid synthesis was synergistically enhanced at optimized concentrations.
Apart from the applied aspects of microorganisms used for the production of fermented foods and beverages, two basic studies on the cell structure and gene functions of A. oryzae have expanded the knowledge of this important food-fermentation fungus. One problem that hampers the breeding of the koji mold is its inability to cross genetically, as sexual reproduction has not yet been discovered. To enhance its potential applications in the industry, it is important to develop breeding techniques and increase its genetic diversity so that strains with beneficial traits can be selected. Toward this end, Katayama and Maruyama investigated the regulatory mechanisms of sclerotia formation, because this asexual structure serves as a repository for sexual development in closely related Aspergillus flavus (Kwon-Chung and Sugui, 2009). They showed inhibition of sclerotia formation and conidia induction by trace amounts of copper, and elucidated that the mechanism is mediated via transcriptional activation of AobrlA, a critical transcription factor gene for conidiation. Molecular genetic analyses have established epistatic relationships among the genes encoding AoSod1 (copper-dependent superoxide dismutase), AoCcsA (a copper chaperone that introduces copper ions into AoSod1), and EcdR (a transcription factor for AobrlA expression) in the copper regulation of these reproductive structures. In addition to the molecular mechanism underlying sterility, the presumed occurrence of galactofuranose (Galf )-containing glycans in A. oryzae cell walls (Nakajima and Ichishima, 1994) led to investigations by Kadooka et al., who identified the related UDP-galactofuranose mutase gene (ugmA) and showed the UgmA-dependent synthesis of Galf-containing glycoproteins in the koji mold. Although the amount of the Galf-containing glycoproteins in the cell wall fraction was significantly smaller than that in other Aspergillus species, the incorporation of Galf side chains into the core mannan backbone was required for the maintenance of cell wall integrity; i.e., as revealed by the temperature and calcofluor white sensitivities of the A. oryzae ΔugmA disruptant. Given that such fungal-type galactomannan (FTGM) is a remnant of the ancestral pathogenic Aspergillus species and is antigenic in humans, it is intriguing to assume that some health-promoting benefits, such as immunostimulatory effects and intestinal eubiosis, occur through habitual ingestion of koji-fermented foods (Kitagaki, 2021). These findings provide a theoretical basis for innovative industrial developments.
Fusarium graminearum and other closely related Fusarium phytopathogenic fungi infect wheat and barley, and accumulate trichothecene mycotoxins in the grains (Kimura et al., 2007). This group of mycotoxins inhibits protein translation in eukaryotes and causes moldy-grain toxicoses through ingestion of contaminated agricultural products. These Fusarium species have recently been found to have a potential ability to glucosylate the side chains of the trichothecene skeleton, raising the possibility of producing diverse variations of “masked” mycotoxins (Matsui et al., 2021). Thus, the mechanism of regulation of trichothecene biosynthesis by F. graminearum has been the subject of intensive studies, and several hypotheses and models have been proposed. Liew et al. discuss several issues that previous researchers had not noticed, presenting original unpublished results, and proposing a revision of the current understanding of the mechanism of trichothecene biosynthesis regulation. Finally, the perspective paper shares a strategy for establishing a regulatory model of transcription of Tri6 and Tri10 in F. graminearum, which are trichothecene transcription factor and regulatory protein genes, respectively, located at the core region of the gene cluster (Maeda et al., 2018). Overall, the information is highly suggestive for research on the roles of various genetic and environmental factors involved in the regulation of secondary metabolism.
In summary, this Research Topic highlights recent advances that explore applied aspects of microorganisms for the production of fermented foods and beverages, as well as basic research into the genetic and biochemical mechanisms underlying the growth, development, and metabolism of microorganisms that affect the quality, safety, and functionality of agricultural products.
Author contributions
All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.
Acknowledgments
Topic editors would like to thank all the authors contributed to the Research Topic as well as the Frontiers team.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Barnett, J. A. (2003). Beginnings of microbiology and biochemistry: the contribution of yeast research. Microbiology 149, 557–567. doi: 10.1099/mic.0.26089-0
Chang, G., Gao, N., Tian, G., Wu, Q., Chang, M., and Wang, X. (2013). Improvement of docosahexaenoic acid production on glycerol by Schizochytrium sp. S31 with constantly high oxygen transfer coefficient. Bioresour. Technol. 142, 400–406. doi: 10.1016/j.biortech.2013.04.107
Haarmann, T., Rolke, Y., Giesbert, S., and Tudzynski, P. (2009). Ergot: from witchcraft to biotechnology. Mol. Plant Pathol. 10, 563–577. doi: 10.1111/j.1364-3703.2009.00548.x
Kimura, M., Tokai, T., Takahashi-Ando, N., Ohsato, S., and Fujimura, M. (2007). Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci. Biotechnol. Biochem. 71, 2105–2123. doi: 10.1271/bbb.70183
Kitagaki, H. (2021). Medical application of substances derived from non-pathogenic fungi Aspergillus oryzae and A. luchuensis-containing koji. J. Fungi. 7, 243. doi: 10.3390/jof7040243
Kwon-Chung, K. J., and Sugui, J. A. (2009). Sexual reproduction in Aspergillus species of medical or economical importance: why so fastidious? Trends Microbiol. 17, 481–487. doi: 10.1016/j.tim.2009.08.004
Lorenzini, M., Simonato, B., Slaghenaufi, D., Ugliano, M., and Zapparoli, G. (2019). Assessment of yeasts for apple juice fermentation and production of cider volatile compounds. LWT 99, 224–230. doi: 10.1016/j.lwt.2018.09.075
Maeda, K., Ichikawa, H., Nakajima, Y., Motoyama, T., Ohsato, S., Kanamaru, K., et al. (2018). Identification and characterization of small molecule compounds that modulate trichothecene production by Fusarium graminearum. ACS Chem. Biol. 13, 1260–1269. doi: 10.1021/acschembio.8b00044
Matsui, K., Takeda, H., Shinkai, K., Kakinuma, T., Koizumi, Y., Kase, M., et al. (2021). 4-O-Glucosylation of trichothecenes by Fusarium species: a phase II xenobiotic metabolism for t-type trichothecene producers. Int. J. Mol. Sci. 22, 13542. doi: 10.3390/ijms222413542
Nakajima, T., and Ichishima, E. (1994). Chemical structure of the galactomannan moiety in the cell wall glycoproteins of Aspergillus oryzae. J. Ferment. Bioeng. 78, 472–475. doi: 10.1016/0922-338X(94)90050-7
Nishida, H. (2021). Sake brewing and bacteria inhabiting sake breweries. Front. Microbiol. 12, 602380. doi: 10.3389/fmicb.2021.602380
Keywords: Aspergillus oryzae (the koji mold), fermented foods and beverages, Fusarium graminearum, microbiome analysis, mycotoxin biosynthesis, polyunsaturated fatty acids (PUFAs), trichothecene gene regulation, yeasts
Citation: Kimura M, Nishida H, Kato M, Goto M and Nakagawa T (2023) Editorial: Microorganisms and their metabolism affecting quality, safety and functionality of agricultural products. Front. Microbiol. 14:1215112. doi: 10.3389/fmicb.2023.1215112
Received: 01 May 2023; Accepted: 04 May 2023;
Published: 17 May 2023.
Edited and reviewed by: Aldo Corsetti, University of Teramo, Italy
Copyright © 2023 Kimura, Nishida, Kato, Goto and Nakagawa. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Makoto Kimura, bWtpbXVyYSYjeDAwMDQwO2Fnci5uYWdveWEtdS5hYy5qcA==