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Genomic Plasticity of Acid-Tolerant Phenotypic Evolution in Acetobacter pasteurianus

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Abstract

Acetic acid bacteria have a remarkable capacity to cope with elevated concentrations of cytotoxic acetic acid in their fermentation environment. In particular, the high-level acetate tolerance of Acetobacter pasteurianus that occurs in vinegar industrial settings must be constantly selected for. However, the improved acetic acid tolerance is rapidly lost without a selection pressure. To understand genetic and molecular biology of this acquired acetic acid tolerance in A. pasteurianus, we evolved three strains A. pasteurianus CICIM B7003, CICIM B7003-02, and ATCC 33,445 over 960 generations (4 months) in two initial acetic acids of 20 g·L−1 and 30 g·L−1, respectively. An acetic acid-adapted strain M20 with significantly improved specific growth rate of 0.159 h−1 and acid productivity of 1.61 g·L−1·h−1 was obtained. Comparative genome analysis of six evolved strains revealed that the genetic variations of adaptation were mainly focused on lactate metabolism, membrane proteins, transcriptional regulators, transposases, replication, and repair system. Among of these, lactate dehydrogenase, acetolactate synthase, glycosyltransferase, ABC transporter ATP-binding protein, two-component regulatory systems, the type II toxin-antitoxin system (RelE/RelB/StbE), exodeoxyribonuclease III, type I restriction endonuclease, tRNA-uridine 2-sulfurtransferase, and transposase might collaboratively contribute to the improved acetic acid tolerance in A. pasteurianus strains. The balance between repair factors and transposition variations might be the basis for genomic plasticity of A. pasteurianus strains, allowing the survival of populations and their offspring in acetic acid stress fluctuations. These observations provide important insights into the nature of acquired acetic acid tolerance phenotype and lay a foundation for future genetic manipulation of these strains.

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Data Availability

All data generated or analyzed during this study are included in this published article and its Supplementary material.

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Funding

This work is financially supported by the National Natural Science Foundation of China (grant nos. 31901671) and the Fundamental Research Funds for the Central Universities (JUSRP121016).

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Authors and Affiliations

  1. The Key Laboratory of Industrial Biotechnology, Ministry of Education, School of Biotechnology, Jiangnan University, 1800 Lihu Road, Wuxi, People’s Republic of China

    Ling Gao, Wei Shi & Xiaole Xia

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  1. Ling Gao
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  2. Wei Shi
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  3. Xiaole Xia
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Contributions

L. Gao and X.L. Xia conceived and designed the experiments. L. Gao and W. Shi carried out the experiments and analyzed the data. L. Gao and X.L. Xia wrote and revised the paper. All authors read and approved the final manuscript.

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Correspondence to Xiaole Xia.

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Gao, L., Shi, W. & Xia, X. Genomic Plasticity of Acid-Tolerant Phenotypic Evolution in Acetobacter pasteurianus. Appl Biochem Biotechnol 195, 6003–6019 (2023). https://doi.org/10.1007/s12010-023-04353-9

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