Acid adaptive response of Alicyclobacillus acidoterrestris: A strategy to survive lethal heat and acid stresses

Alicyclobacillus acidoterrestris causes the spoilage of pasteurized acidic fruit juice, seriously decreasing quality and posing a significant safety concern. We previously discovered that acid adaptation could induce stress adaptive responses of A. acidoterrestris, however, the underlying mechanisms of this induction have not been fully elucidated. In this work, the effects of acid adaptation (pH = 3.0, 1 h) on intracellular pH (pHi) and the morphophysiological properties of A. acidoterrestris under lethal heat and acid stresses were investigated, and gene expression profiles after acid adaptation were measured by transcriptomic analysis. The results showed that acid adaptation increased the pHi of A. acidoterrestris cells in response to lethal stresses, enhanced membrane integrity, decreased surface shrinkage and roughness, and altered the Fourier transform infrared spectra profiles. After acid adaptation of A. acidoterrestris, 517 differentially expressed genes (DEGs) were detected. Consistent with resistance phenotypes, DEGs included genes related to cell surface modification and pHi homeostasis. Specifically, the barrier function of cell membrane was strengthened during acid adaptation by increasing fatty acid (FA) chain length, promoting unsaturated FA biosynthesis, and maintaining balanced synthesis of zwitterionic and acidic phospholipids. To reduce excessive intracellular protons, cells upregulated glutamate decarboxylation, urease system, and branched-chain amino acid synthesis. Additionally, the nucleotide salvage pathway was activated, and homologous recombination, UvrD-mediated transcription-coupled, and ribonucleotide excision repair pathways were applied to repair DNA lesions. Sporulation metabolism was also induced. The findings of this study provide insight into the multiple layers of acid adaptive response strategies of A. acidoterrestris, with implications for the formulation of improved control measures in the fruit juice industry.