Extracellular vesicles involved in growth regulation and metabolic modulation in Haematococcus pluvialis
Abstract Background Microalgae-derived extracellular vesicles (EVs), which transfer their cargos to the extracellular environment to affect recipient cells, play important roles in microalgal growth and environmental adaptation. And, they are also considered as sustainable and renewable bioresources...
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| Format: | Article |
| Language: | English |
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BMC
2024-01-01
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| Series: | Biotechnology for Biofuels and Bioproducts |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13068-024-02462-z |
| _version_ | 1827328270867103744 |
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| author | Qunju Hu Zhangli Hu Xiaojun Yan Jun Lu Chaogang Wang |
| author_facet | Qunju Hu Zhangli Hu Xiaojun Yan Jun Lu Chaogang Wang |
| author_sort | Qunju Hu |
| collection | DOAJ |
| description | Abstract Background Microalgae-derived extracellular vesicles (EVs), which transfer their cargos to the extracellular environment to affect recipient cells, play important roles in microalgal growth and environmental adaptation. And, they are also considered as sustainable and renewable bioresources of delivery nanocarrier for bioactive molecules and/or artificial drug molecules. However, their molecular composition and functions remain poorly understood. Results In this study, isolation, characterization, and functional verification of Haematococcus pluvialis-derived EVs (HpEVs) were performed. The results indicated that HpEVs with typical EV morphology and size were secreted by H. pluvialis cells during the whole period of growth and accumulated in the culture medium. Cellular uptake of HpEVs by H. pluvialis was confirmed, and their roles in regulation of growth and various physiological processes of the recipient cells were also characterized. The short-term inhibition of HpEV secretion results in the accumulation of functional cellular components of HpEVs, thereby altering the biological response of these cells at the molecular level. Meanwhile, continuously inhibiting the secretion of HpEVs negatively influenced growth, and fatty acid and astaxanthin accumulation in H. pluvialis. Small RNA high-throughput sequencing was further performed to determine the miRNA cargoes and compelling details in HpEVs in depth. Comparative analysis revealed commonalities and differences in miRNA species and expression levels in three stages of HpEVs. A total of 163 mature miRNAs were identified with a few unique miRNAs reveal the highest expression levels, and miRNA expression profile of the HpEVs exhibited a clear stage-specific pattern. Moreover, a total of 12 differentially expressed miRNAs were identified and their target genes were classified to cell cycle control, lipid transport and metabolism, secondary metabolites biosynthesis and so on. Conclusion It was therefore proposed that cargos of HpEVs, including miRNA constituents, were suggested potential roles in modulate cell physiological state of H. pluvialis. To summarize, this work uncovers the intercellular communication and metabolism regulation functions of HpEVs. |
| first_indexed | 2024-03-07T15:15:32Z |
| format | Article |
| id | doaj.art-dcf7c8b6dc51443da70c0198c77ee4c9 |
| institution | Directory Open Access Journal |
| issn | 2731-3654 |
| language | English |
| last_indexed | 2024-03-07T15:15:32Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Biotechnology for Biofuels and Bioproducts |
| spelling | doaj.art-dcf7c8b6dc51443da70c0198c77ee4c92024-03-05T17:58:03ZengBMCBiotechnology for Biofuels and Bioproducts2731-36542024-01-0117112010.1186/s13068-024-02462-zExtracellular vesicles involved in growth regulation and metabolic modulation in Haematococcus pluvialisQunju Hu0Zhangli Hu1Xiaojun Yan2Jun Lu3Chaogang Wang4Shenzhen Key Laboratory of Marine Bioresource and Eco-Environmental Science, Shenzhen Engineering Laboratory for Marine Algal Biotechnology, Guangdong Provincial Key Laboratory for Plant Epigenetics, College of Life Sciences and Oceanography, Shenzhen UniversityShenzhen Key Laboratory of Marine Bioresource and Eco-Environmental Science, Shenzhen Engineering Laboratory for Marine Algal Biotechnology, Guangdong Provincial Key Laboratory for Plant Epigenetics, College of Life Sciences and Oceanography, Shenzhen UniversityCollege of Marine Science and Technology, Zhejiang Ocean UniversityAuckland Bioengineering Institute, University of AucklandShenzhen Key Laboratory of Marine Bioresource and Eco-Environmental Science, Shenzhen Engineering Laboratory for Marine Algal Biotechnology, Guangdong Provincial Key Laboratory for Plant Epigenetics, College of Life Sciences and Oceanography, Shenzhen UniversityAbstract Background Microalgae-derived extracellular vesicles (EVs), which transfer their cargos to the extracellular environment to affect recipient cells, play important roles in microalgal growth and environmental adaptation. And, they are also considered as sustainable and renewable bioresources of delivery nanocarrier for bioactive molecules and/or artificial drug molecules. However, their molecular composition and functions remain poorly understood. Results In this study, isolation, characterization, and functional verification of Haematococcus pluvialis-derived EVs (HpEVs) were performed. The results indicated that HpEVs with typical EV morphology and size were secreted by H. pluvialis cells during the whole period of growth and accumulated in the culture medium. Cellular uptake of HpEVs by H. pluvialis was confirmed, and their roles in regulation of growth and various physiological processes of the recipient cells were also characterized. The short-term inhibition of HpEV secretion results in the accumulation of functional cellular components of HpEVs, thereby altering the biological response of these cells at the molecular level. Meanwhile, continuously inhibiting the secretion of HpEVs negatively influenced growth, and fatty acid and astaxanthin accumulation in H. pluvialis. Small RNA high-throughput sequencing was further performed to determine the miRNA cargoes and compelling details in HpEVs in depth. Comparative analysis revealed commonalities and differences in miRNA species and expression levels in three stages of HpEVs. A total of 163 mature miRNAs were identified with a few unique miRNAs reveal the highest expression levels, and miRNA expression profile of the HpEVs exhibited a clear stage-specific pattern. Moreover, a total of 12 differentially expressed miRNAs were identified and their target genes were classified to cell cycle control, lipid transport and metabolism, secondary metabolites biosynthesis and so on. Conclusion It was therefore proposed that cargos of HpEVs, including miRNA constituents, were suggested potential roles in modulate cell physiological state of H. pluvialis. To summarize, this work uncovers the intercellular communication and metabolism regulation functions of HpEVs.https://doi.org/10.1186/s13068-024-02462-zExtracellular vesiclesHaematococcus pluvialisFunctional analysismicroRNAMetabolite biosynthesis |
| spellingShingle | Qunju Hu Zhangli Hu Xiaojun Yan Jun Lu Chaogang Wang Extracellular vesicles involved in growth regulation and metabolic modulation in Haematococcus pluvialis Biotechnology for Biofuels and Bioproducts Extracellular vesicles Haematococcus pluvialis Functional analysis microRNA Metabolite biosynthesis |
| title | Extracellular vesicles involved in growth regulation and metabolic modulation in Haematococcus pluvialis |
| title_full | Extracellular vesicles involved in growth regulation and metabolic modulation in Haematococcus pluvialis |
| title_fullStr | Extracellular vesicles involved in growth regulation and metabolic modulation in Haematococcus pluvialis |
| title_full_unstemmed | Extracellular vesicles involved in growth regulation and metabolic modulation in Haematococcus pluvialis |
| title_short | Extracellular vesicles involved in growth regulation and metabolic modulation in Haematococcus pluvialis |
| title_sort | extracellular vesicles involved in growth regulation and metabolic modulation in haematococcus pluvialis |
| topic | Extracellular vesicles Haematococcus pluvialis Functional analysis microRNA Metabolite biosynthesis |
| url | https://doi.org/10.1186/s13068-024-02462-z |
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