Skip to main content
Log in

Molecular, Structural, and Functional Diversity of Universal Stress Proteins (USPs) in Bacteria, Plants, and Their Biotechnological Applications

  • Published:
The Protein Journal Aims and scope Submit manuscript

Abstract

Universal stress proteins (USPs) are widely distributed and play crucial roles in cellular responses to biotic and abiotic stresses. These roles include regulating cell growth and development, cell motility, hypoxia responses, and ion sequestration. With the increasing frequency and intensity of extreme weather events due to climate change, pathogens have developed different strategies to withstand environmental stresses, in which USPs play a significant role in their survival and virulence. In this study, we analyzed the importance of USPs in various organisms, such as archaea, plants, and fungi, as a parameter that influences their survival. We discussed the different types Of USPs and their role, aiming to carry out fundamental research in this field to identify significant constraints for better understanding of USP functions at molecular level. Additionally, we discussed concepts and research techniques that could help overcome these hurdles and facilitate new molecular approaches to better understand and target USPs as important stress adaptation and survival regulators. Although the precise characteristics of USPs are still unclear, numerous innovative uses have already been developed, tested, and implemented. Complementary approaches to basic research and applications, as well as new technology and analytical techniques, may offer insights into the cryptic but crucial activities of USPs in various living systems.

Graphical Abstract

Shows the different environmental stresses faced by plants and microbes and how they respond by generating stress proteins, which are enhanced when stressors trigger organisms and help the organism in stress tolerance and resistance and the pathogenesis of microbes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Vollmer AC, Bark SJ (2018) Twenty-five years of investigating the universal stress protein: function, structure, and applications. Advances in applied microbiology. Elsevier, pp 1–36

  2. Kvint K, Nachin L, Diez A, Nyström T (2003) The bacterial universal stress protein: function and regulation. Curr Opin Microbiol 6(2):140–145

    Article  CAS  PubMed  Google Scholar 

  3. Drumm JE, Mi K, Bilder P, Sun M, Lim J, Bielefeldt-Ohmann H et al (2009) Mycobacterium tuberculosis universal stress protein Rv2623 regulates bacillary growth by ATP-Binding: requirement for establishing chronic persistent infection. PLoS Pathog 5(5):e1000460

    Article  PubMed  PubMed Central  Google Scholar 

  4. Aravind L, Anantharaman V, Koonin EV (2002) Monophyly of class I aminoacyl tRNA synthetase, USPA, ETFP, photolyase, and PP‐ATPase nucleotide‐binding domains: implications for protein evolution in the RNA world. Proteins Struct Funct Bioinf 48(1):1–14

  5. Sousa MC, McKay DB (2001) Structure of the universal stress protein of Haemophilus influenzae. Structure 9(12):1135–1141

    Article  CAS  PubMed  Google Scholar 

  6. Luo D, Wu ZL, Bai Q, Zhang Y, Huang M, Huang YJ et al (2023) Universal stress proteins: from gene to function. Int J Mol Sci 24(5):4725. https://doi.org/10.3390/Ijms24054725

  7. Lee ES, Phan KAT, Jun SE, Park JH, Paeng SK, Chae HB et al (2022) Universal Stress Protein (USP) enhances plant growth and development by promoting cell expansion. J Plant Biol 65(3):231–239. https://doi.org/10.1007/s12374-022-09348-3

    Article  CAS  Google Scholar 

  8. Wang XF, Su J, Yang N, Zhang H, Cao XY, Kang JF (2017) Functional characterization of selected universal stress protein from (SmUSP) in. Genes-Basel 8(9). Artn 224. https://doi.org/10.3390/Genes8090224

  9. Chi YH, Koo SS, Oh HT, Lee ES, Park JH, Phan KAT et al (2019) The physiological functions of universal stress proteins and their molecular mechanism to protect plants from environmental stresses. Front Plant Sci 10:750. https://doi.org/10.3389/Fpls.2019.0075

  10. Nachin L, Nannmark U, Nyström T (2005) Differential roles of the universal stress proteins of Escherichia coli in oxidative stress resistance, adhesion, and motility. J Bacteriol 187(18):6265–6272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. O’Connor A, McClean S (2017) The role of universal stress proteins in bacterial infections. Curr Med Chem 24(36):3970–3979

    Article  CAS  PubMed  Google Scholar 

  12. Gonzali S, Loreti E, Cardarelli F, Novi G, Parlanti S, Pucciariello C et al (2015) Universal stress protein HRU1 mediates ROS homeostasis under anoxia. Nat Plants 1(11):1–9

    Article  Google Scholar 

  13. Gutiérrez-Beltrán E, Personat JM, de la Torre F, Del Pozo O (2017) A universal stress protein involved in oxidative stress is a phosphorylation target for protein kinase CIPK6. Plant Physiol 173(1):836–852

    Article  PubMed  Google Scholar 

  14. Matarredona L, Camacho M, Zafrilla B, Bonete MJ, Esclapez J (2020) The role of stress proteins in Haloarchaea and their adaptive response to environmental shifts. Biomolecules 10(10):1390. https://doi.org/10.3390/Biom10101390

  15. Tkaczuk KL, Shumilin IA, Chruszcz M, Evdokimova E, Savchenko A, Minor W (2013) Structural and functional insight into the universal stress protein family. Evol Appl 6(3):434-49. 10.1111/eva.12057

  16. Chi YH, Koo SS, Oh HT, Lee ES, Park JH, Phan KAT et al (2019) The physiological functions of universal stress proteins and their molecular mechanism to protect plants from environmental stresses. Front Plant Sci 10:750. 10.3389/Fpls.2019.0075

  17. Nabi B, Kumawat M, Ahlawat S, Ahlawat N, Yadav PK, Mir MA (2024) Molecular prediction and correlation of the structure and function of universal stress protein A (UspA) from Salmonella Typhimurium. Biochem Genet. https://doi.org/10.1007/s10528-024-10699-4e73be817-35b3-44f0-8304-ed194b66dbc2

    Article  PubMed  Google Scholar 

  18. Kerk D, Bulgrien J, Smith DW, Gribskov M (2003) Arabidopsis proteins containing similarity to the universal stress protein domain of bacteria. Plant Physiol 131(3):1209–1219. https://doi.org/10.1104/pp.102.016006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bandyopadhyay D, Mukherjee M (2022) Systematic comparison of the protein-protein interaction network of bacterial universal stress protein A (UspA): an insight into its discrete functions. Biologia 77(9):2631–2642

    Article  CAS  Google Scholar 

  20. Masamba P, Kappo AP (2021) Parasite survival and disease persistence in cystic fibrosis, schistosomiasis and pathogenic bacterial diseases: a role for universal stress proteins? Int J Mol Sci 22(19):10878. https://doi.org/10.3390/Ijms221910878

  21. Farewell A, Kvint K, Nyström T (1998) uspB, a new ςS-regulated gene in Escherichia coli which is required for stationary-phase resistance to ethanol. J Bacteriol 180(23):6140–6147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Nachin L, Brive L, Persson K-C, Svensson P, Nyström T (2008) Heterodimer formation within universal stress protein classes revealed by an in silico and experimental approach. J Mol Biol 380(2):340–350

    Article  CAS  PubMed  Google Scholar 

  23. Diez A, Gustavsson N, Nyström T (2000) The universal stress protein A of Escherichia coli is required for resistance to DNA damaging agents and is regulated by a RecA/FtsK-dependent regulatory pathway. Mol Microbiol 36(6):1494–1503

    Article  CAS  PubMed  Google Scholar 

  24. Puškárová A, Ferianc P, Kormanec J, Homerova D, Farewell A, Nyström T (2002) Regulation of yodA encoding a novel cadmium-induced protein in Escherichia coliThe GenBank accession number for the E. coli yodA gene and the SWISS-PROT accession number for E. coli YodA protein in this paper are AAC75039 and P76344, respectively. Microbiology 148(12):3801–11

  25. Nyström T, Neidhardt FC (1994) Expression and role of the universal stress protein, UspA, of Escherichia coli during growth arrest. Mol Microbiol 11(3):537–544

    Article  PubMed  Google Scholar 

  26. Freestone P, Nyström T, Trinei M, Norris V (1997) The universal stress protein, UspA, of Escherichia coli is phosphorylated in response to stasis. J Mol Biol 274(3):318–324

    Article  CAS  PubMed  Google Scholar 

  27. Farewell A, Diez AA, DiRusso CC, Nyström T (1996) Role of the Escherichia coli FadR regulator in stasis survival and growth phase-dependent expression of the uspA, fad, and fab genes. J Bacteriol 178(22):6443–6450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Gustavsson N, Diez A, Nyström T (2002) The universal stress protein paralogues of Escherichia coli are co-ordinately regulated and co-operate in the defence against DNA damage. Mol Microbiol 43(1):107–117

    Article  CAS  PubMed  Google Scholar 

  29. Persson Ö, Valadi Å, Nyström T, Farewell A (2007) Metabolic control of the Escherichia coli universal stress protein response through fructose-6-phosphate. Mol Microbiol 65(4):968–978

    Article  CAS  PubMed  Google Scholar 

  30. Elhosseiny NM, Amin MA, Yassin AS, Attia AS (2015) Acinetobacter baumannii universal stress protein A plays a pivotal role in stress response and is essential for pneumonia and sepsis pathogenesis. Int J Med Microbiol 305(1):114–123

    Article  CAS  PubMed  Google Scholar 

  31. Liu W-T, Karavolos MH, Bulmer DM, Allaoui A, Hormaeche RDCE, Lee JJ et al (2007) Role of the universal stress protein UspA of Salmonella in growth arrest, stress and virulence. Microb Pathog 42(1):2–10

    Article  CAS  PubMed  Google Scholar 

  32. Esvan H, Minet J, Laclie C, Cormier M (2000) Proteins variations in Listeria monocytogenes exposed to high salinities. Int J Food Microbiol 55(1–3):151–155

    Article  CAS  PubMed  Google Scholar 

  33. Seifart Gomes C, Izar B, Pazan F, Mohamed W, Mraheil MA, Mukherjee K et al (2011) Universal stress proteins are important for oxidative and acid stress resistance and growth of Listeria monocytogenes EGD-e in vitro and in vivo. PLoS ONE 6(9):e24965

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  34. Kuramitsu HK, Chen W, Ikegami A (2005) Biofilm formation by the periodontopathic bacteria Treponema denticola and Porphyromonas gingivalis. J Periodontol 76:2047–2051

    Article  PubMed  Google Scholar 

  35. Chen W, Honma K, Sharma A, Kuramitsu HK (2006) A universal stress protein of Porphyromonas gingivalis is involved in stress responses and biofilm formation. FEMS Microbiol Lett 264(1):15–21

    Article  CAS  PubMed  Google Scholar 

  36. Yoon SS, Hennigan RF, Hilliard GM, Ochsner UA, Parvatiyar K, Kamani MC et al (2002) Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev Cell 3(4):593–603

    Article  CAS  PubMed  Google Scholar 

  37. Glass LN, Swapna G, Chavadi SS, Tufariello JM, Mi K, Drumm JE et al (2017) Mycobacterium tuberculosis universal stress protein Rv2623 interacts with the putative ATP binding cassette (ABC) transporter Rv1747 to regulate mycobacterial growth. PLoS Pathog 13(7):e1006515

    Article  PubMed  PubMed Central  Google Scholar 

  38. Banerjee A, Chakraborty MM, Sharma S, Chaturvedi R, Bose A, Biswas P et al (2023) A universal stress protein is essential for the survival of Mycobacterium tuberculosis. bioRxiv 2023.01. 23.525157. https://doi.org/10.1101/2023.01.23.525157

  39. Chi YH, Koo SS, Oh HT, Lee ES, Park JH, Phan KAT, Wi SD, Bae SB, Paeng SK, Chae HB, Kang CH, Kim MG, Kim W-Y, Yun D-J, Lee SY (2019) The physiological functions of universal stress proteins and their molecular mechanism to protect plants from environmental stresses. Front Plant Sci 10:750. https://doi.org/10.3389/fpls.2019.00750

    Article  PubMed  PubMed Central  Google Scholar 

  40. Cui X, Zhang P, Hu Y, Chen C, Liu Q, Guan P et al (2021) Genome-wide analysis of the Universal stress protein A gene family in Vitis and expression in response to abiotic stress. Plant Physiol Biochem PPB 165:57–70. https://doi.org/10.1016/j.plaphy.2021.04.033

    Article  CAS  PubMed  Google Scholar 

  41. Sauter M, Rzewuski G, Marwedel T, Lorbiecke R (2002) The novel ethylene-regulated gene OsUsp1 from rice encodes a member of a plant protein family related to prokaryotic universal stress proteins. J Exp Bot 53(379):2325–2331

    Article  CAS  PubMed  Google Scholar 

  42. Sapitnitskaya M, Maul P, McCollum GT, Guy CL, Weiss B, Samach A et al (2006) Postharvest heat and conditioning treatments activate different molecular responses and reduce chilling injuries in grapefruit. J Exp Bot 57(12):2943–2953

    Article  CAS  PubMed  Google Scholar 

  43. Jung YJ, Melencion SMB, Lee ES, Park JH, Alinapon CV, Oh HT et al (2015) Universal stress protein exhibits a redox-dependent chaperone function in Arabidopsis and enhances plant tolerance to heat shock and oxidative stress. Front Plant Sci 6:1141

    Article  PubMed  PubMed Central  Google Scholar 

  44. Melencion SMB, Chi YH, Pham TT, Paeng SK, Wi SD, Lee C et al (2017) RNA chaperone function of a universal stress protein in Arabidopsis confers enhanced cold stress tolerance in plants. Int J Mol Sci 18(12):2546

    Article  PubMed  PubMed Central  Google Scholar 

  45. Maqbool A, Zahur M, Irfan M, Younas M, Barozai K, Rashid B et al (2008) Identification and expression of six drought responsive transcripts through differential display in desi cottion (Gossypium aroreum). Mol Biol 42(4):559–565

    Article  CAS  Google Scholar 

  46. Hassan S, Ahmad A, Batool F, Rashid B, Husnain T (2021) Genetic modification of Gossypium arboreum universal stress protein (GUSP1) improves drought tolerance in transgenic cotton (Gossypium hirsutum). Physiol Mol Biol Plants 27(8):1779–1794. https://doi.org/10.1007/s12298-021-01048-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Zahur M, Maqbool A, Irfan M, Barozai MYK, Rashid B, Riazuddin S et al (2009) Isolation and functional analysis of cotton universal stress protein promoter in response to phytohormones and abiotic stresses. Mol Biol 43(4):578–585

    Article  CAS  Google Scholar 

  48. Li W, Zhao Fa, Fang W, Xie D, Hou J, Yang X et al (2015) Identification of early salt stress responsive proteins in seedling roots of upland cotton (Gossypium hirsutum L.) employing iTRAQ-based proteomic technique. Front Plant Sci 6:732

  49. Wang H, Wang Y, Zu Y, Sun L (2008) Construction and analysis of subtractive cDNA library of Phellodendron amurense under drought stress. Chin J Biotechnol 24(2):198–202

    Article  Google Scholar 

  50. Loukehaich R, Wang T, Ouyang B, Ziaf K, Li H, Zhang J et al (2012) SpUSP, an annexin-interacting universal stress protein, enhances drought tolerance in tomato. J Exp Bot 63(15):5593–5606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Chou M-X, Wei X-Y, Chen D-S, Zhou J-C (2007) A novel nodule-enhanced gene encoding a putative universal stress protein from Astragalus sinicus. J Plant Physiol 164(6):764–772

    Article  CAS  PubMed  Google Scholar 

  52. Udawat P, Jha RK, Sinha D, Mishra A, Jha B (2016) Overexpression of a cytosolic abiotic stress responsive universal stress protein (SbUSP) mitigates salt and osmotic stress in transgenic tobacco plants. Front Plant Sci 7:518

  53. Dhanyalakshmi K, Nataraja K (2021) Universal stress protein-like gene from mulberry enhances abiotic stress tolerance in Escherichia coli and transgenic tobacco cells. Plant Biol 23(6):1190–1194

    Article  CAS  PubMed  Google Scholar 

  54. Udawat P, Jha RK, Sinha D, Mishra A, Jha B (2016) Overexpression of a cytosolic abiotic stress responsive universal stress protein (SbUSP) mitigates salt and osmotic stress in transgenic tobacco plants. Front Plant Sci 7:518

    Article  PubMed  PubMed Central  Google Scholar 

  55. Technau U, Rudd S, Maxwell P, Gordon PM, Saina M, Grasso LC et al (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet TIG 21(12):633–639. https://doi.org/10.1016/j.tig.2005.09.007

    Article  CAS  PubMed  Google Scholar 

  56. Isokpehi RD, Mahmud O, Mbah AN, Simmons SS, Avelar L, Rajnarayanan RV et al (2011) Developmental regulation of genes encoding universal stress proteins in Schistosoma mansoni. Gene Regul Syst Bio 5:61–74. https://doi.org/10.4137/GRSB.S7491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Zvi A, Ariel N, Fulkerson J, Sadoff JC, Shafferman A (2008) Whole genome identification of Mycobacterium tuberculosisvaccine candidates by comprehensive data mining and bioinformatic analyses. BMC Med Genomics 1(1):1–25

    Article  Google Scholar 

  58. O’Toole R, Williams HD (2003) Universal stress proteins and Mycobacterium tuberculosis. Res Microbiol 154(6):387–392

    Article  CAS  PubMed  Google Scholar 

  59. Xu YB, Quan CS, Jin XZ, Jin XL, Zhao J, Li XH et al (2014) Crystallization and preliminary X-ray diffraction analysis of UspE from. Acta Crystallogr F 70:1640–1642. https://doi.org/10.1107/S2053230x14023437

    Article  CAS  Google Scholar 

  60. Melencion SMB, Chi YH, Pham TT, Paeng SK, Wi SD, Lee C et al (2017) RNA Chaperone Function of a universal stress protein in confers enhanced cold stress tolerance in plants. Int J Mol Sci 18(12). Artn 2546. https://doi.org/10.3390/Ijms18122546

  61. Gorshkova D, Getman I, Voronkov A, Chizhova S, Kuznetsov VV, Pojidaeva E (2018) The gene encoding the universal stress protein AtUSP is regulated by phytohormones and involved in seed germination of Arabidopsis thaliana. Doklady Biochemistry and Biophysics, Springer; pp 105–7

  62. Tkaczuk KL, Shumilin IA, Chruszcz M, Evdokimova E, Savchenko A, Minor W (2013) Structural and functional insight into the universal stress protein family. Evol Appl 6(3):434–449. https://doi.org/10.1111/eva.12057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Deparis Q, Claes A, Foulquié-Moreno MR, Thevelein JM (2017) Engineering tolerance to industrially relevant stress factors in yeast cell factories. Fems Yeast Res 17(4). ARTN fox036. https://doi.org/10.1093/femsyr/fox036

  64. Bandyopadhyay D, Singh G, Mukherjee M, Akhter Y (2021) Computational approach towards the design of novel inhibitor against universal stress protein A to combat multidrug resistant uropathogenic Escherichia coli. J Mol Struct 1238:130379

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Dean JIBB and head of department Biochemistry & Biochemical Engineering, SHUATS for providing the necessary funds and facilities for the current study.

Author information

Authors and Affiliations

Authors

Contributions

BN and MK designed the review and carried out the writing work. All authors were involved in scientific discussion and analysis of the data. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Manoj Kumawat or Sushma Ahlawat.

Ethics declarations

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nabi, B., Kumawat, M., Ahlawat, N. et al. Molecular, Structural, and Functional Diversity of Universal Stress Proteins (USPs) in Bacteria, Plants, and Their Biotechnological Applications. Protein J (2024). https://doi.org/10.1007/s10930-024-10192-2

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10930-024-10192-2

Keywords

Navigation