Christina S Lazebnik, Dianna B Kosyan, Inara E Laryushina

Animal Husbandry and Fodder Production. 2023. Vol. 106, no 2. Р. 185-197.

 

doi:10.33284/2658-3135-106-2-185

 

Review article

Antibacterial activity and Quorum quenching mechanisms of the genus Bacillus (review)

 

Christina S Lazebnik1, Dianna B Kosyan2, Inara E Laryushina3

1,2,3Federal Research Centre of Biological Systems and Agrotechnologies of the Russian Academy of Sciences, Orenburg, Russia

1christinakondrashova94@yandex.ru, https://orcid.org/0000-0003-4907-9656

2 kosyan.diana@mail.ru, https://orcid.org/0000-0002-2621-108X

3inhip@mail.ru, https://orcid.org/0000-0001-5571-4535

 

Abstract. Violation of the digestive tract of animals and poultry is one of the urgent problems in agriculture. An effective strategy for the treatment and prevention of diseases of the digestive system is the development and introduction into veterinary practice of new highly effective probiotic preparations. Probiotics have emerged as a potential alternative to antibiotics and are generally considered safe for the health of the host. Cell-to-cell communication, including between pathogenic and probiotic bacteria, is based on complex mechanisms of regulation of gene expression, which depend on the density of the bacterial population. The combination of such mechanisms is called “quorum sensing”. The phenomenon of quorum sensing involves the biosynthesis and release of signaling molecules of various chemical structures (autoinducers), the threshold concentration of which triggers a biological response. The review presents the main mechanisms of suppression of the bacterial quorum sensing and the ways of practical application of this phenomenon in agriculture. One such route is the use of bacterial strains of the genus Bacillus, which produce a diverse array of antimicrobial peptides that differ in chemical structure. Bacteriocins produced by strains of the genus Bacillus can be considered as second in importance after bacteriocins of lactobacilli. A large number of probiotic preparations have been created for medical and veterinary use based on bacilli strains.

Keywords: quorum sensing, quorum quenching, genus Bacillus, bacteriocins

Acknowledgments: the work was supported by the Russian Science Foundation, Project     No. 22-26-00294.

For citation: Lazebnik CS, Kosyan DB, Laryushina IE. Antibacterial activity and Quorum quenching mechanisms of the genus Bacillus (review). Animal Husbandry and Fodder Production. 2023;106(2):185-197. (In Russ.). https://doi.org/10.33284/2658-3135-106-2-185

 

References

 
  1. Abisado RG, Benomar S, Klaus JR, Dandekar AA, Chandler JR. Bacterial quorum sensing and microbial community interactions. MBio. 2018;9(3):e02331-17. doi: 10.1128/mBio.02331-17
  2. Anandan K, Vittal RR. Quorum quenching activity of AiiA lactonase KMMI17 from endophytic Bacillus thuringiensis KMCL07 on AHL-mediated pathogenic phenotype in Pseudomonas aeruginosa. Microb pathog. 2019;132:230-242. doi: 10.1016/j.micpath.2019.05.015
  3. Baindara P, Korpole S, Grover V. Bacteriocins: perspective for the development of novel anticancer drugs. Appl Microbiol and Biotechnol. 2018;102(24):10393- doi: 10.1007/s00253-018-9420-8
  4. Bergonzi C, Schwab M, Naik T, Daudé D, Chabrière E, Elias M. Structural and biochemical characterization of AaL, a quorum quenching lactonase with unusual kinetic properties. Scientific Reports. 2018;8(1):11262. doi: 10.1038/s41598-018-28988-5
  5. Caulier S, Nannan C, Gillis A, Licciardi F, Bragard C, Mahillon J. Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Front Microbiol. 2019;10:302. doi: 10.3389/fmicb.2019.00302
  6. Chen B, Peng M, Tong W, Zhang Q, Song Z. The quorum quenching bacterium Bacillus licheniformis T-1 protects zebrafish against Aeromonas hydrophila infection. Probiotics Antimicrob. Proteins. 2020;12:160- doi: 10.1007/s12602-018-9495-7
  7. Choi HJ, Shin D, Shin M, Yun B, Kang M, Yang HJ, Oh S. Comparative genomic and functional evaluations of Bacillus subtilis newly isolated from Korean traditional fermented foods. Foods. 2020;9(12):1805. doi: 10.3390/foods9121805
  8. Coquant G, Aguanno D, Pham S, Grellier N, Thenet S, Carrière V, Seksik P. Gossip in the gut: Quorum sensing, a new player in the host-microbiota interactions. World J Gastroenterol. 2021;27(42):7247-7270. doi: 3748/wjg.v27.i42.7247
  9. Dehghanifar S, Keyhanfar M, Emtiazi G. Production and partial purification of thermostable bacteriocins from Bacillus pumilus ZED17 and DFAR8 strains with antifungal activity. Mol Biol Res Commun. 2019;8(1):41-49. doi: 22099/mbrc.2019.31563.1367
  10. Djokic L, Stankovic N, Galic I, Moric I, Radakovic N, Šegan S, .Senerovic L. Novel quorum quenching YtnP lactonase from Bacillus paralicheniformis reduces Pseudomonas aeruginosa Virulence and increases antibiotic efficacy in vivo. Front Microbiol. 2022;13:906312. doi: 3389/fmicb.2022.906312
  11. Dong W, Zhu J, Guo X, Kong D, Zhang Q, Zhou Y, Ruan Z. Characterization of AiiK, an AHL lactonase, from Kurthia huakui LAM0618T and its application in quorum quenching on Pseudomonas aeruginosa PAO1. Scientific Reports. 2018;8(1):6013. doi: 10.1038/s41598-018-24507-8
  12. Dor S, Prusky D, Afriat-Jurnou L. Bacterial quorum-quenching lactonase hydrolyzes fungal mycotoxin and reduces pathogenicity of penicillium expansum—suggesting a mechanism of bacterial antagonism. J Fungi. 2021;7(10):826. doi: 10.3390/jof7100826
  13. Epparti P, Eligar SM, Sattur AP, Kumar BG, Halami PM. Characterization of dual bacteriocins producing Bacillus subtilis SC3. 7 isolated from fermented food. LWT. 2022;154:112854. doi: 10.1016/j.lwt.2021.112854
  14. Faisal AJ, Said LA, Ali MR. Quorum quenching effect of recombinant Paraoxonase-1 enzyme against quorum sensing genes produced from Pseudomonas aeruginosa. Gene Reports. 2021;25:101412. doi: 10.1016/j.genrep.2021.101412
  15. Fathima S, Shanmugasundaram R, Adams D, Selvaraj RK. Gastrointestinal microbiota and their manipulation for improved growth and performance in chickens. Foods. 2022;11(10):1401. doi:  10.3390/foods11101401
  16. Fleitas Martínez O, Cardoso MH, Ribeiro SM, Franco OL. Recent advances in anti-virulence therapeutic strategies with a focus on dismantling bacterial membrane microdomains, toxin neutralization, quorum-sensing interference and biofilm inhibition. Front Cell Infect Microbiol. 2019;9:74. doi: 10.3389/fcimb.2019.00074
  17. Gebreyohannes G, Nyerere A, Bii C, Sbhatu DB. Challenges of intervention, treatment, and antibiotic resistance of biofilm-forming microorganisms. Heliyon. 2019;5(8):e02192. doi: 10.1016/j.heliyon.2019.e02192
  18. Halami PM. Sublichenin, a new subtilin-like lantibiotics of probiotic bacterium Bacillus licheniformis MCC 2512T with antibacterial activity. Microb Pathog. 2019;128:139-146. doi: 10.1016/j.micpath.2018.12.044
  19. Jamal MT, Abdulrahman IA, Al Harbi M, Chithambaran S. Probiotics as alternative control measures in shrimp aquaculture: a review. J Appl Biol Biotechnol 2019;7(3):69- doi: 10.7324/JABB.2019.70313
  20. James G, Das BC, Jose S, VJ RK. Bacillus as an aquaculture friendly microbe. Aquacul Int. 2021;29:323-353. doi: 1007/s10499-020-00630-0
  21. Kim MK, Zhao A, Wang A, Brown ZZ, Muir TW, Stone HA, Bassler BL. Surface-attached molecules control Staphylococcus aureus quorum sensing and biofilm development. Nat Microbial. 2017;2(8):17080. doi: 10.1038/nmicrobiol.2017.80
  22. Kachhadia R, Kapadia C, Singh S, Gandhi K, Jajda H, Alfarraj S, Datta R. Quorum sensing inhibitory and quenching activity of Bacillus cereus RC1 extracts on Soft Rot-Causing Bacteria Lelliottia amnigena. ACS omega. 2022;7(29):25291-25308. doi: 10.1021/acsomega.2c02202
  23. Kuebutornye FKA, Abarikea ED, Lu Y. A review on the application of Bacillus as probiotics in Aquaculture. Fish Shellfish Immun. 2019;87:820- doi: 10.1016/j.fsi.2019.02.010
  24. Kumar L, Patel SKS, Kharga K, Kumar R, Kumar P, Pandohee J, Chhibber S. Molecular mechanisms and applications of N-Acyl homoserine lactone-mediated quorum sensing in bacteria. Molecules. 2022;27(21):7584. doi: 10.3390/molecules27217584
  25. Li Q, Mao S, Wang H, Ye X. The molecular architecture of Pseudomonas aeruginosa quorum-sensing inhibitors. Mar Drugs, 2022;20(8):488. doi: 10.3390/md20080488
  26. Liu J, Fu K, Wu C, Qin K, Li F, Zhou L. “In-Group” communication in marine vibrio: a review of N-acyl homoserine lactones-driven quorum sensing. Front Cell Infect Microbial. 2018;8:139. doi: 10.3389/fcimb.2018.00139
  27. Malesevic M, Stanisavljevic N, Novovic K, Polovic N, Vasiljevic Z, Kojic M, Jovcic B. Burkholderia cepacia YtnP and Y2-aiiA lactonases inhibit virulence of Pseudomonas aeruginosa via quorum quenching activity. Microb Pathogenesis. 2020;149:104561. doi: 10.1016/j.micpath.2020.104561
  28. Meade E, Slattery MA, Garvey M. Bacteriocins, potent antimicrobial peptides and the fight against multi drug resistant species: resistance is futile? Antibiotics. 2020;9(1):32. doi: 10.3390/antibiotics9010032
  29. Mercado V, Olmos J. Bacteriocin production by Bacillus species: Isolation, characterization, and application. Probiotics Antimicrob Proteins. 2022;14(6):1151-1169. doi: 10.1007/s12602-022-09966-w
  30. Mukherjee S, Bassler BL. Bacterial quorum sensing in complex and dynamically changing environments. Nat Rev Microbiol. 2019;17(6):371-382. doi: 10.1038/s41579-019-0186-5
  31. Murugayah SA, Gerth ML. Engineering quorum quenching enzymes: progress and perspectives. Biochel Soc Trans. 2019;47(3):793-800. doi: 10.1042/BST20180165
  32. Nain Z, Adhikari UK, Abdulla F, Hossain N, Barman NC, Mansur FJ, Karim MM. Computational prediction of active sites and ligands in different AHL quorum quenching lactonases and acylases. J Biosci. 2020;45(1):26. doi: 10.1007/s12038-020-0005-1
  33. Olmos J, Acosta M, Mendoza G, Pitones V. Bacillus subtilis, an ideal probiotic bacterium to shrimp and fish aquaculture that increase feed digestibility, prevent microbial diseases, and avoid water pollution. Arch Microbiol. 2020;202:427-435. doi: 10.1007/s00203-019-01757-2
  34. Paluch E, Rewak-Soroczyńska J, Jędrusik I, Mazurkiewicz E, Jermakow K. Prevention of biofilm formation by quorum quenching. Appl Microbiol Biotechnol. 2020;104(5):1871-1881. doi: 10.1007/s00253-020-10349-w
  35. Parween F, Yadav P, Singh K, Gupta RD. Production of highly soluble native human paraoxonase 2 with potential anti-biofilm property. Prep Biochem Biotechnol; 2022:1-10. doi: 10.1080/10826068.2022.2101000
  36. Pereyra MG, Martínez MP, Cavaglieri LR. Presence of aiiA homologue genes encoding for N-Acyl homoserine lactone-degrading enzyme in aflatoxin B1-decontaminating Bacillus strains with potential use as feed additives. Food Chem Toxicol. 2019;124:316-323. doi: 10.1016/j.fct.2018.12.016
  37. Qin Y, Wang Y, He Y, Zhang Y, She Q, Chai Y, Shang Q. Characterization of subtilin L-Q11, a novel class I bacteriocin synthesized by Bacillus subtilis L-Q11 isolated from orchard soil. Front Microbiol. 2019;10: 484. doi: 10.3389/fmicb.2019.00484
  38. Rodríguez M, Torres M, Blanco L, Béjar V, Sampedro I, Llamas I. Plant growth-promoting activity and quorum quenching-mediated biocontrol of bacterial phytopathogens by Pseudomonas segetis strain P6. Sci Rep. 2020;10(1):4121. doi: 10.1038/s41598-020-61084-1
  39. Shao Y, Wang X, Qiu X, Niu L, Ma Z. Isolation and purification of a new Bacillus subtilis strain from deer dung with anti-microbial and anti-cancer activities. Curr Med Sci. 2021;41(4):832- doi: 10.1007/s11596-021-2383-5
  40. Sharma D, Singh SS, Baindara P, Sharma S, Khatri N, Grover V, Korpole S. Surfactin like broad spectrum antimicrobial lipopeptide co-produced with sublancin from Bacillus subtilis strain A52: dual reservoir of bioactives. Front Microbial. 2020;11:1167. doi: 10.3389/fmicb.2020.01167
  41. Simons A, Alhanout K, Duval RE. Bacteriocins, antimicrobial peptides from bacterial origin: Overview of their biology and their impact against multidrug-resistant bacteria. Microorganisms. 2020;8(5):639. doi: 10.3390/microorganisms8050639
  42. Sionov RV, Steinberg D. Targeting the holy triangle of quorum sensing, biofilm formation, and antibiotic resistance in pathogenic bacteria. Microorganisms. 2022;10(6):1239. doi: 10.3390/microorganisms10061239
  43. Torres M, Dessaux Y, Llamas I. Saline environments as a source of potential quorum sensing disruptors to control bacterial infections: a review. Mar Drugs. 2019;17(3):191. doi: 10.3390/md17030191
  44. Vadakkan K, Choudhury AA, Gunasekaran R, Hemapriya J, Vijayanand S. Quorum sensing intervened bacterial signaling: pursuit of its cognizance and repression. J Genet Eng Biotechnol. 2018;16(2):239-252. doi: 10.1016/j.jgeb.2018.07.001
  45. Velasco-Bucheli R, Hormigo D, Fernández-Lucas J, Torres-Ayuso P, Alfaro-Urena Y, Saborido AI, de la Mata I. Penicillin acylase from Streptomyces lavendulae and aculeacin a acylase from Actinoplanes utahensis: two versatile enzymes as useful tools for quorum quenching processes. Catalysts. 2020;10(7):730. doi: 3390/catal10070730
  46. Vesuna A, Nerurkar AS. Enzymatic quorum quenching for virulence attenuation of phytopathogenic bacteria. In: Kalia V, editor.  Biotechnological applications of quorum sensing inhibitors. Singapore: Springer. 2018;21:447-473.
  47. Wang D, Cui F, Ren L, Li J, Li T. Quorum‐quenching enzymes: Promising bioresources and their opportunities and challenges as alternative bacteriostatic agents in food industry. Compr Rev Food Sci Food Saf. 2023;22(2):1104-1127. doi. 10.1111/1541-4337.13104
  48. Whiteley M, Diggle SP, Greenberg EP. Progress in and promise of bacterial quorum sensing research. Nature. 2017;551(7680):313-320. doi: 10.1038/nature24624
  49. Wei Z, Shan C, Zhang L, Wang Y, Xia X, Liu X, Zhou J. A novel subtilin-like lantibiotics subtilin JS-4 produced by Bacillus subtilis JS-4, and its antibacterial mechanism against Listeria monocytogenes. LWT. 2021;142:110993. doi: 10.1016/j.lwt.2021.110993
  50. Xiang YZ, Li XY, Zheng HL, Chen JY, Lin LB, Zhang QL. Purification and antibacterial properties of a novel bacteriocin against Escherichia coli from Bacillus subtilis isolated from blueberry ferments. LWT. 2021;146:111456.  doi: 10.1016/j.lwt.2021.111456
  51. Xin B, Liu H, Zheng J, Xie C, Gao Y, Dai D, Sun M. In silico analysis highlights the diversity and novelty of circular bacteriocins in sequenced microbial genomes. Msystems. 2020;5(3):e00047-20. doi: 10.1128/mSystems.00047-20
  52. Xin B, Xu H, Liu H, Liu S, Wang J, Xue J, Zhang F, Deng S, Zeng H, Zeng X, Xu D, Zhao Y, Li F, Wang G. Identification and characterization of a novel circular bacteriocin, bacicyclicin XIN-1, from Bacillus sp. Xin1. Food Control. 2021;121:107696. doi: 10.1016/j.foodcont.2020.107696
  53. Xu H, Huang W, Hou Q, Kwok L Y, Laga W, Wang Y, Zhang H. Oral administration of compound probiotics improved canine feed intake, weight gain, immunity and intestinal microbiota. Front Immunol. 2019;10:666. doi: 10.3389/fimmu.2019.00666
  54. Yan W, Sun C, Yuan J, Yang N. Gut metagenomic analysis reveals prominent roles of Lactobacillus and cecal microbiota in chicken feed efficiency. Sci Rep. 2017;7:45308. doi: 10.1038/srep45308
  55. Zhang JW, Xuan CG, Lu CH, Guo S, Yu JF, Asif M, Zhang LQ. AidB, a novel thermostable N-acylhomoserine lactonase from the bacterium Bosea sp. Appl Environ Microbial. 2019;85(24):e02065-19. doi: 10.1128/AEM.02065-19
  56. Zhang M, Wu C. The relationship between intestinal goblet cells and the immune response. Biosci Rep. 2020;40(10):BSR20201471. doi: 10.1042/BSR20201471
  57. Zou J, Jiang H, Cheng H, Fang J, Huang G. Strategies for screening, purification, and characterization of bacteriocins. Int J Biol Macromol. 2018;117:781-789. doi: 10.1016/j.ijbiomac.2018.05.233
  58. Zulkhairi Amin FA, Sabri S, Ismail M, Chan KW, Ismail N, Mohd Esa N, Zawawi N. Probiotic properties of Bacillus strains isolated from stingless bee (Heterotrigona itama) honey collected across Malaysia. Int J Environ Res Public Health. 2020;17(1):278. doi: 10.3390/ijerph17010278
 

Information about the authors:

Christina S Lazebnik, Post-graduate student, Researcher, Laboratory of Breeding and Genetic Research in Animal Husbandry, Federal Research Centre of Biological Systems and Agrotechnologies of the Russian Academy of Sciences, 29, 9 Yanvarya St., Orenburg, 460000.

Dianna B Kosyan, Cand. Sci. (Biology), Senior Researcher, Laboratory of Breeding and Genetic Research in Animal Husbandry, Federal Research Centre for Biological Systems and Agrotechnologies of the Russian Academy of Sciences, 29, 9 Yanvarya St., Orenburg, 460000.

Inara E Laryushina, Cand. Sci. (Medicine), Senior Researcher, Laboratory of Breeding and Genetic Research in Animal Husbandry, Federal Research Centre for Biological Systems and Agrotechnologies of the Russian Academy of Sciences, 29, 9 Yanvarya St., Orenburg, 460000.

 

The article was submitted 31.01.2023; approved after reviewing 20.03.2023; accepted for publication 13.06.2023.

Download