Multiple Precursor Proteins of Thanatin Isoforms, an Antimicrobial Peptide Associated With the Gut Symbiont of

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2022 Jan 24

PMID 35069496

Authors

Junbeom Lee

Wook Hyun Cha

Dae-Weon Lee

Affiliations

Soon will be listed here.

Abstract

Thanatin is an antimicrobial peptide (AMP) generated by insects for defense against bacterial infections. In the present study, we performed cDNA cloning of thanatin and found the presence of multiple precursor proteins from the bean bug, . The cDNA sequences encoded 38 precursor proteins, generating 13 thanatin isoforms. In the phylogenetic analysis, thanatin isoforms were categorized into two groups based on the presence of the membrane attack complex/perforin (MACPF) domain. In insect-bacterial symbiosis, specific substances are produced by the immune system of the host insect and are known to modulate the symbiont's population. Therefore, to determine the biological function of thanatin isoforms in symbiosis, the expression levels of three AMP genes were compared between aposymbiotic insects and symbiotic . The expression levels of the genes were significantly increased in the M4 crypt, a symbiotic organ, of symbiotic insects upon systemic bacterial injection. Further, synthetic thanatin isoforms exhibited antibacterial activity against gut-colonized symbionts rather than -cultured cells. Interestingly, the suppression of genes significantly increased the population of gut symbionts in the M4 crypt under systemic K12 injection. Overgrown gut symbionts were observed in the hemolymph of host insects and exhibited insecticidal activity. Taken together, these results suggest that thanatin of is a host-derived symbiotic factor and an AMP that controls the population of gut-colonized symbionts.

Citing Articles

Discovery of Novel Thanatin-like Antimicrobial Peptides from Bean Bug .

Panteleev P, Teplovodskaya J, Utkina A, Smolina A, Kruglikov R, Safronova V Pharmaceutics. 2024; 16(11).

PMID: 39598576 PMC: 11597323. DOI: 10.3390/pharmaceutics16111453.

The ncRNA-mediated regulatory networks of and in : involvement in response to gut bacterial disturbances.

Ren Y, Fu S, Dong W, Chen J, Xue H, Bu W Front Microbiol. 2024; 15:1386345.

PMID: 38827147 PMC: 11140134. DOI: 10.3389/fmicb.2024.1386345.

Ingested soil bacteria breach gut epithelia and prime systemic immunity in an insect.

Jang S, Ishigami K, Mergaert P, Kikuchi Y Proc Natl Acad Sci U S A. 2024; 121(11):e2315540121.

PMID: 38437561 PMC: 10945853. DOI: 10.1073/pnas.2315540121.

Outer-Membrane Permeabilization, LPS Transport Inhibition: Activity, Interactions, and Structures of Thanatin Derived Antimicrobial Peptides.

Abdullah S, Yan B, Palanivelu N, Dhanabal V, Bifani J, Bhattacharjya S Int J Mol Sci. 2024; 25(4).

PMID: 38396798 PMC: 10888688. DOI: 10.3390/ijms25042122.

Structures, Interactions and Activity of the N-Terminal Truncated Variants of Antimicrobial Peptide Thanatin.

Abdullah S, Mu Y, Bhattacharjya S Antibiotics (Basel). 2024; 13(1).

PMID: 38247633 PMC: 10812785. DOI: 10.3390/antibiotics13010074.

References

Sinha S, Zheng L, Mu Y, Ng W, Bhattacharjya S . Structure and Interactions of A Host Defense Antimicrobial Peptide Thanatin in Lipopolysaccharide Micelles Reveal Mechanism of Bacterial Cell Agglutination. Sci Rep. 2017; 7(1):17795. PMC: 5736615. DOI: 10.1038/s41598-017-18102-6. View

Lemaitre B, Reichhart J, Hoffmann J . Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci U S A. 1998; 94(26):14614-9. PMC: 25070. DOI: 10.1073/pnas.94.26.14614. View

Fehlbaum P, Bulet P, Chernysh S, Briand J, Roussel J, Letellier L . Structure-activity analysis of thanatin, a 21-residue inducible insect defense peptide with sequence homology to frog skin antimicrobial peptides. Proc Natl Acad Sci U S A. 1996; 93(3):1221-5. PMC: 40060. DOI: 10.1073/pnas.93.3.1221. View

Douglas A . The molecular basis of bacterial-insect symbiosis. J Mol Biol. 2014; 426(23):3830-7. PMC: 4385585. DOI: 10.1016/j.jmb.2014.04.005. View

Lee D, Lee J, Jang H, Ferrandon D, Lee B . An antimicrobial protein of the Riptortus pedestris salivary gland was cleaved by a virulence factor of Serratia marcescens. Dev Comp Immunol. 2016; 67:427-433. DOI: 10.1016/j.dci.2016.08.009. View

Miura K, Ueno S, Kamiya K, Kobayashi J, Matsuoka H, Ando K . Cloning of mRNA sequences for two antibacterial peptides in a hemipteran insect, Riptortus clavatus. Zoolog Sci. 1996; 13(1):111-7. DOI: 10.2108/zsj.13.111. View

Li W, Tailhades J, OBrien-Simpson N, Separovic F, Otvos Jr L, Hossain M . Proline-rich antimicrobial peptides: potential therapeutics against antibiotic-resistant bacteria. Amino Acids. 2014; 46(10):2287-94. DOI: 10.1007/s00726-014-1820-1. View

Kim J, Jang H, Kim M, Cho J, Lee J, Di Lorenzo F . The lipopolysaccharide core oligosaccharide of plays a critical role in maintaining a proper gut symbiosis with the bean bug . J Biol Chem. 2017; 292(47):19226-19237. PMC: 5702664. DOI: 10.1074/jbc.M117.813832. View

Kikuchi Y, Hosokawa T, Fukatsu T . An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J. 2010; 5(3):446-60. PMC: 3105724. DOI: 10.1038/ismej.2010.150. View

10.

Florez L, Biedermann P, Engl T, Kaltenpoth M . Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat Prod Rep. 2015; 32(7):904-36. DOI: 10.1039/c5np00010f. View

11.

Dash R, Bhattacharjya S . Thanatin: An Emerging Host Defense Antimicrobial Peptide with Multiple Modes of Action. Int J Mol Sci. 2021; 22(4). PMC: 7913509. DOI: 10.3390/ijms22041522. View

12.

Vetterli S, Zerbe K, Muller M, Urfer M, Mondal M, Wang S . Thanatin targets the intermembrane protein complex required for lipopolysaccharide transport in . Sci Adv. 2018; 4(11):eaau2634. PMC: 6235536. DOI: 10.1126/sciadv.aau2634. View

13.

Kim J, Lee J, Jang H, Han Y, Fukatsu T, Lee B . Understanding regulation of the host-mediated gut symbiont population and the symbiont-mediated host immunity in the Riptortus-Burkholderia symbiosis system. Dev Comp Immunol. 2016; 64:75-81. DOI: 10.1016/j.dci.2016.01.005. View

14.

Forbes-Beadle L, Crossman T, Johnson T, Burke R, Warr C, Whisstock J . Development of the Cellular Immune System of Drosophila Requires the Membrane Attack Complex/Perforin-Like Protein Torso-Like. Genetics. 2016; 204(2):675-681. PMC: 5068854. DOI: 10.1534/genetics.115.185462. View

15.

Kikuchi Y, Meng X, Fukatsu T . Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae). Appl Environ Microbiol. 2005; 71(7):4035-43. PMC: 1169019. DOI: 10.1128/AEM.71.7.4035-4043.2005. View

16.

Kikuchi Y, Hosokawa T, Fukatsu T . Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol. 2007; 73(13):4308-16. PMC: 1932760. DOI: 10.1128/AEM.00067-07. View

17.

Bulet P, Hetru C, Dimarcq J, Hoffmann D . Antimicrobial peptides in insects; structure and function. Dev Comp Immunol. 1999; 23(4-5):329-44. DOI: 10.1016/s0145-305x(99)00015-4. View

18.

Lavine M, Strand M . Insect hemocytes and their role in immunity. Insect Biochem Mol Biol. 2002; 32(10):1295-309. DOI: 10.1016/s0965-1748(02)00092-9. View

19.

Wu G, Wu H, Li L, Fan X, Ding J, Li X . Membrane aggregation and perturbation induced by antimicrobial peptide of S-thanatin. Biochem Biophys Res Commun. 2010; 395(1):31-5. DOI: 10.1016/j.bbrc.2010.03.107. View

20.

Lee J, Park K, Ah Lee S, Jang S, Eo H, Jang H . Gut symbiotic bacteria stimulate insect growth and egg production by modulating hexamerin and vitellogenin gene expression. Dev Comp Immunol. 2016; 69:12-22. DOI: 10.1016/j.dci.2016.11.019. View