Effect of ammonium stress on phosphorus solubilization of a novel marine mangrove microorganism Bacillus aryabhattai NM1-A2 as revealed by integrated omics analysis

Abstract

Abstract Background Phosphorus (P) is one of the essential nutrients for plant growth. Phosphate-solubilizing microorganisms (PSMs) can alleviate P deficiency in an eco-friendly way. Ammonium toxicity is widespread, but is not very well known about the effect of ammonium stress on phosphorus solubilization (PS) of PSMs. Results In this study, seven PSMs were isolated from mangrove sediments. Among them, Bacillus aryabhattai NM1-A2 showed a high PS ability under ammonium stress, which reached a maximum of 196.96 mg/L at 250 mM (NH4)2SO4. Whole-genome analysis showed that B. aryabhattai NM1-A2 contained various genes related to ammonium transporter (amt), ammonium assimilation (i.e., gdhA, glnA, and gltD), organic acid synthesis (i.e., ackA, fdhD, and idh), and phosphate transport (i.e., pstB and pstS). Furthermore, transcriptome data showed that the expression level of amt was downregulated. This phenomenon contributed to reducing the intake of external ammonium. For ammonium assimilation under ammonium stress, accompanied by protons efflux, the glutamate dehydrogenase pathway was the main approach. The overall upregulated glycolysis and tricarboxylic acid cycle could provide abundant carbon skeletons. Among them, the upregulated expression of idh indicated that more 2-oxoglutarate (2-OG) was induced under NH4+ stress. High performance liquid chromatography results showed that the concentrations of formic acid and acetic acid were significantly increased under ammonium stress, while succinic acid was significantly decreased. Conclusions In conclusion, the secretion of protons and organic acids was related to the high PS ability of B. aryabhattai NM1-A2 under ammonium stress. The accumulation of 2-OG and the inhibition of GS/GOGAT pathway might play a key role in ammonium detoxification. Our work provides new insights into the PS mechanism, which will provide theoretical guidance for the application of PSMs to promote environment-friendly agricultural development.