Giving a Signal: How Protein Phosphorylation Helps Bacillus Navigate Through Different Life Stages

Overview

Journal FEMS Microbiol Rev

Publisher Oxford University Press

Specialty Microbiology

Date 2023 Aug 3

PMID 37533212

Authors

Aakriti Gangwal

Nishant Kumar

Nitika Sangwan

Neha Dhasmana

Uma Dhawan

Andaleeb Sajid

Gunjan Arora

Yogendra Singh

Affiliations

Soon will be listed here.

Abstract

Protein phosphorylation is a universal mechanism regulating a wide range of cellular responses across all domains of life. The antagonistic activities of kinases and phosphatases can orchestrate the life cycle of an organism. The availability of bacterial genome sequences, particularly Bacillus species, followed by proteomics and functional studies have aided in the identification of putative protein kinases and protein phosphatases, and their downstream substrates. Several studies have established the role of phosphorylation in different physiological states of Bacillus species as they pass through various life stages such as sporulation, germination, and biofilm formation. The most common phosphorylation sites in Bacillus proteins are histidine, aspartate, tyrosine, serine, threonine, and arginine residues. Protein phosphorylation can alter protein activity, structural conformation, and protein-protein interactions, ultimately affecting the downstream pathways. In this review, we summarize the knowledge available in the field of Bacillus signaling, with a focus on the role of protein phosphorylation in its physiological processes.

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References

Tanaka K, Kobayashi K, Ogasawara N . The Bacillus subtilis YufLM two-component system regulates the expression of the malate transporters MaeN (YufR) and YflS, and is essential for utilization of malate in minimal medium. Microbiology (Reading). 2003; 149(Pt 9):2317-2329. DOI: 10.1099/mic.0.26257-0. View

Foulquier E, Pompeo F, Bernadac A, Espinosa L, Galinier A . The YvcK protein is required for morphogenesis via localization of PBP1 under gluconeogenic growth conditions in Bacillus subtilis. Mol Microbiol. 2011; 80(2):309-18. DOI: 10.1111/j.1365-2958.2011.07587.x. View

Sharma A, Dhasmana N, Dubey N, Kumar N, Gangwal A, Gupta M . Bacterial Virulence Factors: Secreted for Survival. Indian J Microbiol. 2017; 57(1):1-10. PMC: 5243249. DOI: 10.1007/s12088-016-0625-1. View

Birkey S, Liu W, Zhang X, Duggan M, Hulett F . Pho signal transduction network reveals direct transcriptional regulation of one two-component system by another two-component regulator: Bacillus subtilis PhoP directly regulates production of ResD. Mol Microbiol. 1999; 30(5):943-53. DOI: 10.1046/j.1365-2958.1998.01122.x. View

Freitas C, Plannic J, Isticato R, Pelosi A, Zilhao R, Serrano M . A protein phosphorylation module patterns the Bacillus subtilis spore outer coat. Mol Microbiol. 2020; 114(6):934-951. PMC: 7821199. DOI: 10.1111/mmi.14562. View

Fuhrmann J, Subramanian V, Kojetin D, Thompson P . Activity-Based Profiling Reveals a Regulatory Link between Oxidative Stress and Protein Arginine Phosphorylation. Cell Chem Biol. 2016; 23(8):967-977. PMC: 5157131. DOI: 10.1016/j.chembiol.2016.07.008. View

Zhou C, Zhang H, Fang H, Sun Y, Zhou H, Yang G . Transcriptome based functional identification and application of regulator AbrB on alkaline protease synthesis in Bacillus licheniformis 2709. Int J Biol Macromol. 2020; 166:1491-1498. DOI: 10.1016/j.ijbiomac.2020.11.028. View

Gonzalez-Sanchez M, Lanucara F, Helm M, Eyers C . Attempting to rewrite History: challenges with the analysis of histidine-phosphorylated peptides. Biochem Soc Trans. 2013; 41(4):1089-95. DOI: 10.1042/BST20130072. View

Stauff D, Skaar E . Bacillus anthracis HssRS signalling to HrtAB regulates haem resistance during infection. Mol Microbiol. 2009; 72(3):763-78. PMC: 2891670. DOI: 10.1111/j.1365-2958.2009.06684.x. View

10.

Hoch J . A Life in Bacillus subtilis Signal Transduction. Annu Rev Microbiol. 2017; 71:1-19. DOI: 10.1146/annurev-micro-030117-020355. View

11.

Prashar A, Bhatia S, Gigliozzi D, Martin T, Duncan C, Guyard C . Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages. J Cell Biol. 2013; 203(6):1081-97. PMC: 3871431. DOI: 10.1083/jcb.201304095. View

12.

Shi Y, Zhang Y, Lin S, Wang C, Zhou J, Peng D . dbPSP 2.0, an updated database of protein phosphorylation sites in prokaryotes. Sci Data. 2020; 7(1):164. PMC: 7260176. DOI: 10.1038/s41597-020-0506-7. View

13.

Yague P, Gonzalez-Quinonez N, Fernandez-Garcia G, Alonso-Fernandez S, Manteca A . Correction: Yagüe, P., et al. Goals and Challenges in Bacterial Phosphoproteomics. 2019, , 5678. Int J Mol Sci. 2020; 21(24). PMC: 7764465. DOI: 10.3390/ijms21249381. View

14.

Stannek L, Gunka K, Care R, Gerth U, Commichau F . Factors that mediate and prevent degradation of the inactive and unstable GudB protein in Bacillus subtilis. Front Microbiol. 2015; 5:758. PMC: 4285742. DOI: 10.3389/fmicb.2014.00758. View

15.

Torres R, Serrano E, Alonso J . Bacillus subtilis RecA interacts with and loads RadA/Sms to unwind recombination intermediates during natural chromosomal transformation. Nucleic Acids Res. 2019; 47(17):9198-9215. PMC: 6755099. DOI: 10.1093/nar/gkz647. View

16.

Mukai K, Kawata M, Tanaka T . Isolation and phosphorylation of the Bacillus subtilis degS and degU gene products. J Biol Chem. 1990; 265(32):20000-6. View

17.

Hobley L, Harkins C, MacPhee C, Stanley-Wall N . Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes. FEMS Microbiol Rev. 2015; 39(5):649-69. PMC: 4551309. DOI: 10.1093/femsre/fuv015. View

18.

Stephenson K, Hoch J . Evolution of signalling in the sporulation phosphorelay. Mol Microbiol. 2002; 46(2):297-304. DOI: 10.1046/j.1365-2958.2002.03186.x. View

19.

Isticato R, Lanzilli M, Petrillo C, Donadio G, Baccigalupi L, Ricca E . Bacillus subtilis builds structurally and functionally different spores in response to the temperature of growth. Environ Microbiol. 2019; 22(1):170-182. DOI: 10.1111/1462-2920.14835. View

20.

Manuse S, Fleurie A, Zucchini L, Lesterlin C, Grangeasse C . Role of eukaryotic-like serine/threonine kinases in bacterial cell division and morphogenesis. FEMS Microbiol Rev. 2015; 40(1):41-56. DOI: 10.1093/femsre/fuv041. View