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Transcriptomic Analysis Reveals the Response of the Bacterium Priestia Aryabhattai SK1-7 to Interactions and Dissolution with Potassium Feldspar

Potassium feldspar (K(2)O·Al(2)O(3)·6SiO(2)) is considered to be the most important source of potash fertilizer. The use of microorganisms to dissolve potassium feldspar is a low-cost and environmentally friendly method. Priestia aryabhattai SK1-7 is a strain with a strong ability to dissolve potass...

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Autores principales: Yang, Hui, Lu, Lanxiang, Chen, Yifan, Ye, Jianren
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10231193/
https://www.ncbi.nlm.nih.gov/pubmed/37154709
http://dx.doi.org/10.1128/aem.02034-22
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author Yang, Hui
Lu, Lanxiang
Chen, Yifan
Ye, Jianren
author_facet Yang, Hui
Lu, Lanxiang
Chen, Yifan
Ye, Jianren
author_sort Yang, Hui
collection PubMed
description Potassium feldspar (K(2)O·Al(2)O(3)·6SiO(2)) is considered to be the most important source of potash fertilizer. The use of microorganisms to dissolve potassium feldspar is a low-cost and environmentally friendly method. Priestia aryabhattai SK1-7 is a strain with a strong ability to dissolve potassium feldspar; it showed a faster pH drop and produced more acid in the medium with potassium feldspar as the insoluble potassium source than in the medium with K(2)HPO(4) as the soluble potassium source. We speculated whether the cause of acid production was related to one or more stresses, such as mineral-induced generation of reactive oxygen species (ROS), the presence of aluminum in potassium feldspar, and cell membrane damage due to friction between SK1-7 and potassium feldspar, and analyzed it by transcriptome. The results revealed that the expression of the genes related to pyruvate metabolism, the two-component system, DNA repair, and oxidative stress pathways in strain SK1-7 was significantly upregulated in potassium feldspar medium. The subsequent validation experiments revealed that ROS were the stress faced by strain SK1-7 when interacting with potassium feldspar and led to a decrease in the total fatty acid content of SK1-7. In the face of ROS stress, strain SK1-7 upregulated the expression of the maeA-1 gene, allowing malic enzyme (ME2) to produce more pyruvate to be secreted outside the cell using malate as a substrate. Pyruvate is both a scavenger of external ROS and a gas pedal of dissolved potassium feldspar. IMPORTANCE Mineral-microbe interactions play important roles in the biogeochemical cycling of elements. Manipulating mineral-microbe interactions and optimizing the consequences of such interactions can be used to benefit society. It is necessary to explore the black hole of the mechanism of interaction between the two. In this study, it is revealed that P. aryabhattai SK1-7 faces mineral-induced ROS stress by upregulating a series of antioxidant genes as a passive defense, while overexpression of malic enzyme (ME2) secretes pyruvate to scavenge ROS as well as to increase feldspar dissolution, releasing K, Al, and Si into the medium. Our research provides a theoretical basis for improving the ability of microorganisms to weather minerals through genetic manipulation in the future.
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spelling pubmed-102311932023-06-01 Transcriptomic Analysis Reveals the Response of the Bacterium Priestia Aryabhattai SK1-7 to Interactions and Dissolution with Potassium Feldspar Yang, Hui Lu, Lanxiang Chen, Yifan Ye, Jianren Appl Environ Microbiol Geomicrobiology Potassium feldspar (K(2)O·Al(2)O(3)·6SiO(2)) is considered to be the most important source of potash fertilizer. The use of microorganisms to dissolve potassium feldspar is a low-cost and environmentally friendly method. Priestia aryabhattai SK1-7 is a strain with a strong ability to dissolve potassium feldspar; it showed a faster pH drop and produced more acid in the medium with potassium feldspar as the insoluble potassium source than in the medium with K(2)HPO(4) as the soluble potassium source. We speculated whether the cause of acid production was related to one or more stresses, such as mineral-induced generation of reactive oxygen species (ROS), the presence of aluminum in potassium feldspar, and cell membrane damage due to friction between SK1-7 and potassium feldspar, and analyzed it by transcriptome. The results revealed that the expression of the genes related to pyruvate metabolism, the two-component system, DNA repair, and oxidative stress pathways in strain SK1-7 was significantly upregulated in potassium feldspar medium. The subsequent validation experiments revealed that ROS were the stress faced by strain SK1-7 when interacting with potassium feldspar and led to a decrease in the total fatty acid content of SK1-7. In the face of ROS stress, strain SK1-7 upregulated the expression of the maeA-1 gene, allowing malic enzyme (ME2) to produce more pyruvate to be secreted outside the cell using malate as a substrate. Pyruvate is both a scavenger of external ROS and a gas pedal of dissolved potassium feldspar. IMPORTANCE Mineral-microbe interactions play important roles in the biogeochemical cycling of elements. Manipulating mineral-microbe interactions and optimizing the consequences of such interactions can be used to benefit society. It is necessary to explore the black hole of the mechanism of interaction between the two. In this study, it is revealed that P. aryabhattai SK1-7 faces mineral-induced ROS stress by upregulating a series of antioxidant genes as a passive defense, while overexpression of malic enzyme (ME2) secretes pyruvate to scavenge ROS as well as to increase feldspar dissolution, releasing K, Al, and Si into the medium. Our research provides a theoretical basis for improving the ability of microorganisms to weather minerals through genetic manipulation in the future. American Society for Microbiology 2023-05-08 /pmc/articles/PMC10231193/ /pubmed/37154709 http://dx.doi.org/10.1128/aem.02034-22 Text en Copyright © 2023 Yang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Geomicrobiology
Yang, Hui
Lu, Lanxiang
Chen, Yifan
Ye, Jianren
Transcriptomic Analysis Reveals the Response of the Bacterium Priestia Aryabhattai SK1-7 to Interactions and Dissolution with Potassium Feldspar
title Transcriptomic Analysis Reveals the Response of the Bacterium Priestia Aryabhattai SK1-7 to Interactions and Dissolution with Potassium Feldspar
title_full Transcriptomic Analysis Reveals the Response of the Bacterium Priestia Aryabhattai SK1-7 to Interactions and Dissolution with Potassium Feldspar
title_fullStr Transcriptomic Analysis Reveals the Response of the Bacterium Priestia Aryabhattai SK1-7 to Interactions and Dissolution with Potassium Feldspar
title_full_unstemmed Transcriptomic Analysis Reveals the Response of the Bacterium Priestia Aryabhattai SK1-7 to Interactions and Dissolution with Potassium Feldspar
title_short Transcriptomic Analysis Reveals the Response of the Bacterium Priestia Aryabhattai SK1-7 to Interactions and Dissolution with Potassium Feldspar
title_sort transcriptomic analysis reveals the response of the bacterium priestia aryabhattai sk1-7 to interactions and dissolution with potassium feldspar
topic Geomicrobiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10231193/
https://www.ncbi.nlm.nih.gov/pubmed/37154709
http://dx.doi.org/10.1128/aem.02034-22
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