Biosurfactants Induce Antimicrobial Peptide Production Through the Activation of Spatzles in

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2020 Aug 28

PMID 32847078

Citations 4

Authors

Tariku Tesfaye Edosa

Yong Hun Jo

Maryam Keshavarz

In Seon Kim

Yeon Soo Han

Affiliations

Soon will be listed here.

Abstract

Biosurfactant immunomodulatory activities in mammals, nematodes, and plants have been investigated. However, the immune activation property of biosurfactants in insects has not been reported. Therefore, here, we studied the defense response triggered by lipopeptides (fengycin and iturin A), glycolipids (rhamnolipid), and cyclic polypeptides (bacitracin) in the coleopteran insect, mealworm . The in vitro antimicrobial activities against Gram-positive () and Gram-negative () bacteria and fungi () were assessed by mixing these pathogens with the hemolymph of biosurfactant-immune-activated larvae. growth was remarkably inhibited by this hemolymph. The antimicrobial peptide (AMP) induction results also revealed that all biosurfactants tested induced several AMPs, exclusively in hemocytes. The survivability analysis of larvae challenged by (10 CFU/µL) at 24 h post biosurfactant-immune activation showed that fengycin, iturin A, and rhamnopid significantly increased survivability against . Biosurfactant-induced activation was also monitored, and the results showed that and were upregulated in the hemocytes of iturin A-injected larvae, while and were upregulated in the fat bodies of the fengycin-, iturin A-, and rhamnolipid-injected larvae. Overall, these results suggest that lipopeptide and glycolipid biosurfactants induce the expression of AMPs in via the activation of spätzle genes, thereby increasing the survivability of against .

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References

Chen Y, Liu S, Mou H, Ma Y, Li M, Hu X . Characterization of Lipopeptide Biosurfactants Produced by MB01 from Marine Sediments. Front Microbiol. 2017; 8:871. PMC: 5432566. DOI: 10.3389/fmicb.2017.00871. View

Carlsson A, Engstrom P, Palva E, Bennich H . Attacin, an antibacterial protein from Hyalophora cecropia, inhibits synthesis of outer membrane proteins in Escherichia coli by interfering with omp gene transcription. Infect Immun. 1991; 59(9):3040-5. PMC: 258132. DOI: 10.1128/iai.59.9.3040-3045.1991. View

Keshavarz M, Jo Y, Park K, Ko H, Tesfaye Edosa T, Lee Y . TmDorX2 positively regulates antimicrobial peptides in Tenebrio molitor gut, fat body, and hemocytes in response to bacterial and fungal infection. Sci Rep. 2019; 9(1):16878. PMC: 6856108. DOI: 10.1038/s41598-019-53497-4. View

Ahimou , Jacques , Deleu . Surfactin and iturin A effects on Bacillus subtilis surface hydrophobicity. Enzyme Microb Technol. 2000; 27(10):749-754. DOI: 10.1016/s0141-0229(00)00295-7. View

Gan P, Gao Z, Zhao X, Qi G . Surfactin inducing mitochondria-dependent ROS to activate MAPKs, NF-κB and inflammasomes in macrophages for adjuvant activity. Sci Rep. 2016; 6:39303. PMC: 5155226. DOI: 10.1038/srep39303. View

Jang I, Chosa N, Kim S, Nam H, Lemaitre B, Ochiai M . A Spätzle-processing enzyme required for toll signaling activation in Drosophila innate immunity. Dev Cell. 2006; 10(1):45-55. DOI: 10.1016/j.devcel.2005.11.013. View

Casteels P, Ampe C, Jacobs F, Tempst P . Functional and chemical characterization of Hymenoptaecin, an antibacterial polypeptide that is infection-inducible in the honeybee (Apis mellifera). J Biol Chem. 1993; 268(10):7044-54. View

Kim C, Kim S, Kan H, Kwon H, Roh K, Jiang R . A three-step proteolytic cascade mediates the activation of the peptidoglycan-induced toll pathway in an insect. J Biol Chem. 2008; 283(12):7599-607. DOI: 10.1074/jbc.M710216200. View

Giri S, Sen S, Jun J, Sukumaran V, Park S . Role of VS16-Derived Biosurfactant in Mediating Immune Responses in Carp Rohu and its Application to the Food Industry. Front Microbiol. 2017; 8:514. PMC: 5368236. DOI: 10.3389/fmicb.2017.00514. View

10.

Zaman M, Toth I . Immunostimulation by synthetic lipopeptide-based vaccine candidates: structure-activity relationships. Front Immunol. 2013; 4:318. PMC: 3793171. DOI: 10.3389/fimmu.2013.00318. View

11.

Rozgonyi F, Szabo D, Kocsis B, Ostorhazi E, Abbadessa G, Cassone M . The antibacterial effect of a proline-rich antibacterial peptide A3-APO. Curr Med Chem. 2009; 16(30):3996-4002. DOI: 10.2174/092986709789352295. View

12.

Mondol M, Shin H, Islam M . Diversity of secondary metabolites from marine Bacillus species: chemistry and biological activity. Mar Drugs. 2013; 11(8):2846-72. PMC: 3766869. DOI: 10.3390/md11082846. View

13.

Haddad N, Wang J, Mu B . Isolation and characterization of a biosurfactant producing strain, Brevibacilis brevis HOB1. J Ind Microbiol Biotechnol. 2008; 35(12):1597-604. DOI: 10.1007/s10295-008-0403-0. View

14.

Roh K, Kim C, Lee H, Kwon H, Park J, Ryu J . Proteolytic cascade for the activation of the insect toll pathway induced by the fungal cell wall component. J Biol Chem. 2009; 284(29):19474-81. PMC: 2740573. DOI: 10.1074/jbc.M109.007419. View

15.

Yu Y, Park J, Kwon H, Hwang H, Jang I, Masuda A . Diversity of innate immune recognition mechanism for bacterial polymeric meso-diaminopimelic acid-type peptidoglycan in insects. J Biol Chem. 2010; 285(43):32937-32945. PMC: 2963372. DOI: 10.1074/jbc.M110.144014. View

16.

Takeda K, Kaisho T, Akira S . Toll-like receptors. Annu Rev Immunol. 2003; 21:335-76. DOI: 10.1146/annurev.immunol.21.120601.141126. View

17.

Iatsenko I, Yim J, Schroeder F, Sommer R . B. subtilis GS67 protects C. elegans from Gram-positive pathogens via fengycin-mediated microbial antagonism. Curr Biol. 2014; 24(22):2720-7. DOI: 10.1016/j.cub.2014.09.055. View

18.

Tesfaye Edosa T, Jo Y, Keshavarz M, Bae Y, Kim D, Lee Y . Spz6 Is Essential for Regulating the Immune Response to Escherichia Coli and Staphylococcus Aureus Infection in Tenebrio Molitor. Insects. 2020; 11(2). PMC: 7074004. DOI: 10.3390/insects11020105. View

19.

Patocka J, Nepovimova E, Klimova B, Wu Q, Kuca K . Antimicrobial Peptides: Amphibian Host Defense Peptides. Curr Med Chem. 2018; 26(32):5924-5946. DOI: 10.2174/0929867325666180713125314. View

20.

Zhu S . Discovery of six families of fungal defensin-like peptides provides insights into origin and evolution of the CSalphabeta defensins. Mol Immunol. 2007; 45(3):828-38. DOI: 10.1016/j.molimm.2007.06.354. View