The Cultivation Method Affects the Transcriptomic Response of Aspergillus niger to Growth on Sugar Beet Pulp
ABSTRACT In nature, filamentous fungi are exposed to diverse nutritional sources and changes in substrate availability. Conversely, in submerged cultures, mycelia are continuously exposed to the existing substrates, which are depleted over time. Submerged cultures are the preferred choice for experi...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2021-09-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/Spectrum.01064-21 |
| _version_ | 1818755177979576320 |
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| author | Sandra Garrigues Roland S. Kun Mao Peng Birgit S. Gruben Isabelle Benoit Gelber Miia Mäkelä Ronald P. de Vries |
| author_facet | Sandra Garrigues Roland S. Kun Mao Peng Birgit S. Gruben Isabelle Benoit Gelber Miia Mäkelä Ronald P. de Vries |
| author_sort | Sandra Garrigues |
| collection | DOAJ |
| description | ABSTRACT In nature, filamentous fungi are exposed to diverse nutritional sources and changes in substrate availability. Conversely, in submerged cultures, mycelia are continuously exposed to the existing substrates, which are depleted over time. Submerged cultures are the preferred choice for experimental setups in laboratory and industry and are often used for understanding the physiology of fungi. However, to what extent the cultivation method affects fungal physiology, with respect to utilization of natural substrates, has not been addressed in detail. Here, we compared the transcriptomic responses of Aspergillus niger grown in submerged culture and solid culture, both containing sugar beet pulp (SBP) as a carbon source. The results showed that expression of CAZy (Carbohydrate Active enZyme)-encoding and sugar catabolic genes in liquid SBP was time dependent. Moreover, additional components of SBP delayed the A. niger response to the degradation of pectin present in SBP. In addition, we demonstrated that liquid cultures induced wider transcriptome variability than solid cultures. Although there was a correlation regarding sugar metabolic gene expression patterns between liquid and solid cultures, it decreased in the case of CAZyme-encoding genes. In conclusion, the transcriptomic response of A. niger to SBP is influenced by the culturing method, limiting the value of liquid cultures for understanding the behavior of fungi in natural habitats. IMPORTANCE Understanding the interaction between filamentous fungi and their natural and biotechnological environments has been of great interest for the scientific community. Submerged cultures are preferred over solid cultures at a laboratory scale to study the natural response of fungi to different stimuli found in nature (e.g., carbon/nitrogen sources, pH). However, whether and to what extent submerged cultures introduce variation in the physiology of fungi during growth on plant biomass have not been studied in detail. In this study, we compared the transcriptomic responses of Aspergillus niger to growth on liquid and solid cultures containing sugar beet pulp (a by-product of the sugar industry) as a carbon source. We demonstrate that the transcriptomic response of A. niger was highly affected by the culture condition, since the transcriptomic response obtained in a liquid environment could not fully explain the behavior of the fungus in a solid environment. This could partially explain the differences often observed between the phenotypes on plates compared to liquid cultures. |
| first_indexed | 2024-12-18T05:35:01Z |
| format | Article |
| id | doaj.art-f8a7a37eaf554cc4b24d650eb4bb13d6 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-12-18T05:35:01Z |
| publishDate | 2021-09-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-f8a7a37eaf554cc4b24d650eb4bb13d62022-12-21T21:19:21ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972021-09-019110.1128/Spectrum.01064-21The Cultivation Method Affects the Transcriptomic Response of Aspergillus niger to Growth on Sugar Beet PulpSandra Garrigues0Roland S. Kun1Mao Peng2Birgit S. Gruben3Isabelle Benoit Gelber4Miia Mäkelä5Ronald P. de Vries6Fungal Physiology, Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology, Utrecht University, Utrecht, The NetherlandsFungal Physiology, Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology, Utrecht University, Utrecht, The NetherlandsFungal Physiology, Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology, Utrecht University, Utrecht, The NetherlandsFungal Physiology, Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology, Utrecht University, Utrecht, The NetherlandsFungal Physiology, Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology, Utrecht University, Utrecht, The NetherlandsDepartment of Microbiology, University of Helsinki, Helsinki, FinlandFungal Physiology, Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology, Utrecht University, Utrecht, The NetherlandsABSTRACT In nature, filamentous fungi are exposed to diverse nutritional sources and changes in substrate availability. Conversely, in submerged cultures, mycelia are continuously exposed to the existing substrates, which are depleted over time. Submerged cultures are the preferred choice for experimental setups in laboratory and industry and are often used for understanding the physiology of fungi. However, to what extent the cultivation method affects fungal physiology, with respect to utilization of natural substrates, has not been addressed in detail. Here, we compared the transcriptomic responses of Aspergillus niger grown in submerged culture and solid culture, both containing sugar beet pulp (SBP) as a carbon source. The results showed that expression of CAZy (Carbohydrate Active enZyme)-encoding and sugar catabolic genes in liquid SBP was time dependent. Moreover, additional components of SBP delayed the A. niger response to the degradation of pectin present in SBP. In addition, we demonstrated that liquid cultures induced wider transcriptome variability than solid cultures. Although there was a correlation regarding sugar metabolic gene expression patterns between liquid and solid cultures, it decreased in the case of CAZyme-encoding genes. In conclusion, the transcriptomic response of A. niger to SBP is influenced by the culturing method, limiting the value of liquid cultures for understanding the behavior of fungi in natural habitats. IMPORTANCE Understanding the interaction between filamentous fungi and their natural and biotechnological environments has been of great interest for the scientific community. Submerged cultures are preferred over solid cultures at a laboratory scale to study the natural response of fungi to different stimuli found in nature (e.g., carbon/nitrogen sources, pH). However, whether and to what extent submerged cultures introduce variation in the physiology of fungi during growth on plant biomass have not been studied in detail. In this study, we compared the transcriptomic responses of Aspergillus niger to growth on liquid and solid cultures containing sugar beet pulp (a by-product of the sugar industry) as a carbon source. We demonstrate that the transcriptomic response of A. niger was highly affected by the culture condition, since the transcriptomic response obtained in a liquid environment could not fully explain the behavior of the fungus in a solid environment. This could partially explain the differences often observed between the phenotypes on plates compared to liquid cultures.https://journals.asm.org/doi/10.1128/Spectrum.01064-21gene expressionsubmerged culturesolid cultureAspergillus nigersugar beet pulp |
| spellingShingle | Sandra Garrigues Roland S. Kun Mao Peng Birgit S. Gruben Isabelle Benoit Gelber Miia Mäkelä Ronald P. de Vries The Cultivation Method Affects the Transcriptomic Response of Aspergillus niger to Growth on Sugar Beet Pulp Microbiology Spectrum gene expression submerged culture solid culture Aspergillus niger sugar beet pulp |
| title | The Cultivation Method Affects the Transcriptomic Response of Aspergillus niger to Growth on Sugar Beet Pulp |
| title_full | The Cultivation Method Affects the Transcriptomic Response of Aspergillus niger to Growth on Sugar Beet Pulp |
| title_fullStr | The Cultivation Method Affects the Transcriptomic Response of Aspergillus niger to Growth on Sugar Beet Pulp |
| title_full_unstemmed | The Cultivation Method Affects the Transcriptomic Response of Aspergillus niger to Growth on Sugar Beet Pulp |
| title_short | The Cultivation Method Affects the Transcriptomic Response of Aspergillus niger to Growth on Sugar Beet Pulp |
| title_sort | cultivation method affects the transcriptomic response of aspergillus niger to growth on sugar beet pulp |
| topic | gene expression submerged culture solid culture Aspergillus niger sugar beet pulp |
| url | https://journals.asm.org/doi/10.1128/Spectrum.01064-21 |
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