Abstract
Actinobacteria is a phylum composed of aerobic, Gram-positive, and filamentous bacteria with a broad spectrum of biological activity, including antioxidant, antitumor, and antibiotic. The crude extract of Streptomyces griseocarneus R132 was fractionated on a C18 silica column and the isolated compound was identified by 1H and 13C nuclear magnetic resonance as 3-(phenylprop-2-enoic acid), also known as trans-cinnamic acid. Antimicrobial activity against human pathogens was assayed in vitro (disk-diffusion qualitative test) and in vivo using Galleria mellonella larvae (RT-qPCR). The methanol fractions 132-F30%, 132-F50%, 132-F70%, and 132-F100% inhibited the Escherichia coli (ATCC 25922) and Staphylococcus aureus (MRSA) growth in vitro the most effectively. Compared with the untreated control (60–80% of larvae death), the fractions and isolated trans-cinnamic acid increased the survival rate and modulated the immune system of G. mellonella larvae infected with pathogenic microorganisms. The anti-infection effect of the S. griseocarneus R132 fermentation product led us to sequence its genome, which was assembled and annotated using the Rast and antiSMASH platforms. The assembled genome consisted of 227 scaffolds represented on a linear chromosome of 8.85 Mb and 71.3% of GC. We detected conserved domains typical of enzymes that produce molecules with biological activity, such as polyketides and non-ribosomal and ribosomal peptides, indicating a great potential for obtaining new antibiotics and molecules with biotechnological application.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abildgren MP, Lund F, Thrane U, Elmholt S (1987) Czapek-Dox agar containing iprodione and dicloran as a selective medium for the isolation of Fusarium species. Lett Appl Microbiol 5:83–86. https://doi.org/10.1111/j.1472-765X.1987.tb01620.x
Abozaid OAR, Moawed FSM, Ahmed ESA, Ibrahim ZA (2020) Cinnamic acid nanoparticles modulate redox signal and inflammatory response in gamma irradiated rats suffering from acute pancreatitis. Biochim Biophys Acta - Mol Basis Dis 1866:165904. https://doi.org/10.1016/j.bbadis.2020.165904
Adisakwattana S, Sookkongwaree K, Roengsumran S et al (2004) Structure–activity relationships of trans-cinnamic acid derivatives on α-glucosidase inhibition. Bioorg Med Chem Lett 14:2893–2896. https://doi.org/10.1016/j.bmcl.2004.03.037
Ahmad MS, El-Gendy AO, Ahmed RR et al (2017) Exploring the antimicrobial and antitumor potentials of streptomyces sp. AGM12-1 isolated from Egyptian soil. Front Microbiol 8:1–11. https://doi.org/10.3389/fmicb.2017.00438
Aigle B, Lautru S, Spiteller D et al (2014) Genome mining of Streptomyces ambofaciens. J Ind Microbiol Biotechnol 41:251–263
Al-Dhabi NA, Mohammed Ghilan A-K, Esmail GA et al (2019) Bioactivity assessment of the Saudi Arabian Marine Streptomyces sp. Al-Dhabi-90, metabolic profiling and its in vitro inhibitory property against multidrug resistant and extended-spectrum beta-lactamase clinical bacterial pathogens. J Infect Public Health 12:549–556. https://doi.org/10.1016/j.jiph.2019.01.065
Almalki MA (2020) Isolation and characterization of polyketide drug molecule from Streptomyces species with antimicrobial activity against clinical pathogens. J Infect Public Health 13:125–130. https://doi.org/10.1016/j.jiph.2019.07.002
Almeer RS, Aref AM, Hussein RA et al (2018) Antitumor potential of berberine and cinnamic acid against solid ehrlich carcinoma in mice. Anticancer Agents Med Chem 19:356–364. https://doi.org/10.2174/1871520618666181116162441
Angolini CFF, Gonçalves AB, Sigrist R et al (2016) Genome mining of endophytic Streptomyces wadayamensis reveals high antibiotic production capability. J Braz Chem Soc 00:1–11. https://doi.org/10.5935/0103-5053.20160180
Aziz RK, Bartels D, Best AA et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75
Bankevich A, Nurk S, Antipov D et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Bentley SD, Chater KF, Cerdeño-Tárraga A-M et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147. https://doi.org/10.1038/417141a
Bernard K, Funke G (2012) Bergey’s manual® of systematic bacteriology. Springer, New York, New York, NY
Blattner FR, Plunkett G, Bloch CA, et al (1997) The complete genome sequence of Escherichia coli K-12. science, 277(5331), pp.1453-1462. https://doi.org/10.1126/science.277.5331.1453
Bolger AM, Lohse M, Usadel B (2014) Genome Analysis Trimmomatic : a Flexible Trimmer for Illumina Sequence Data 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bolouri Moghaddam MR, Tonk M, Schreiber C et al (2016) The potential of the Galleria mellonella innate immune system is maximized by the co-presentation of diverse antimicrobial peptides. Biol Chem 397:939–945. https://doi.org/10.1515/hsz-2016-0157
Buchmann A, Eitel M, Koch P et al (2016) High-quality draft genome sequence of the actinobacterium Nocardia terpenica IFM 0406, producer of the immunosuppressant brasilicardins, using illumina and PacBio technologies. Genome Announc 4:4–5. https://doi.org/10.1128/genomeA.01391-16
Chandrakar S, Gupta AK (2019) Actinomycin-producing endophytic streptomyces parvulus associated with root of aloe vera and optimization of conditions for antibiotic production. Probiotics Antimicrob Proteins 11:1055–1069. https://doi.org/10.1007/s12602-018-9451-6
Chen Y-L, Huang S-T, Sun F-M et al (2011) Transformation of cinnamic acid from trans- to cis-form raises a notable bactericidal and synergistic activity against multiple-drug resistant Mycobacterium tuberculosis. Eur J Pharm Sci 43:188–194. https://doi.org/10.1016/j.ejps.2011.04.012
Chen J, Sun R, Pan C, et al (2020) Antibiotics and Food Safety in Aquaculture. J Agric Food Chem acs.jafc.0c03996. https://doi.org/10.1021/acs.jafc.0c03996
Cheung-Lee WL, Parry ME, Jaramillo Cartagena A et al (2019) Discovery and structure of the antimicrobial lasso peptide citrocin. J Biol Chem 294:6822–6830. https://doi.org/10.1074/jbc.RA118.006494
Cheung-Lee WL, Parry ME, Zong C et al (2020) Discovery of ubonodin, an antimicrobial lasso peptide active against members of the Burkholderia cepacia complex. ChemBioChem 21:1335–1340. https://doi.org/10.1002/cbic.201900707
Detlefsen DJ, Hill SE, Volk KJ et al (1995) Siamycins I and II, new anti-HIV-1 peptides: II. sequence analysis and structure determination of siamycin I. J Antibiot (tokyo) 48:1515–1517. https://doi.org/10.7164/antibiotics.48.1515
Ding J-L, Hou J, Feng M-G, Ying S-H (2020) Transcriptomic analyses reveal comprehensive responses of insect hemocytes to mycopathogen Beauveria bassiana, and fungal virulence-related cell wall protein assists pathogen to evade host cellular defense. Virulence 11:1352–1365. https://doi.org/10.1080/21505594.2020.1827886
El-Seedi HR, El-Said AMA, Khalifa SAM et al (2012) Biosynthesis, natural sources, dietary intake, pharmacokinetic properties, and biological activities of hydroxycinnamic acids. J Agric Food Chem 60:10877–10895. https://doi.org/10.1021/jf301807g
Garcia-Gutierrez E, O’Connor PM, Saalbach G et al (2020) First evidence of production of the lantibiotic nisin P. Sci Rep 10:3738. https://doi.org/10.1038/s41598-020-60623-0
Gavrish E, Sit CS, Cao S et al (2014) Lassomycin, a ribosomally synthesized cyclic peptide, kills mycobacterium tuberculosis by targeting the ATP-dependent protease ClpC1P1P2. Chem Biol 21:509–518. https://doi.org/10.1016/j.chembiol.2014.01.014
Geng M, Ravichandran A, Escano J, Smith L (2018) Efficacious analogs of the lantibiotic mutacin 1140 against a systemic methicillin-resistant staphylococcus aureus infection. Antimicrob Agents Chemother 62:1–14. https://doi.org/10.1128/AAC.01626-18
Graham ML, Prescott MJ (2015) The multifactorial role of the 3Rs in shifting the harm-benefit analysis in animal models of disease. Eur J Pharmacol 759:19–29
Gravina HD, Tafuri NF, Silva Júnior A et al (2011) In vitro assessment of the antiviral potential of trans-cinnamic acid, quercetin and morin against equid herpesvirus 1. Res Vet Sci 91:e158–e162. https://doi.org/10.1016/j.rvsc.2010.11.010
Gu Y, Yang C, Wang X et al (2014) Genome sequence of the ε-poly-L-lysine-producing strain Streptomyces albulus NK660, isolated from soil in Gutian, Fujian Province, China. Genome Announc 2:3–4. https://doi.org/10.1128/genomeA.00532-14
Gupta V, Singhal L (2018) Antibiotics and Antimicrobial Resistance. In: Infectious Diseases and Your Health. Springer Singapore, Singapore, pp 215–224
Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075. https://doi.org/10.1093/bioinformatics/btt086
Hegemann JD (2020) Factors governing the thermal stability of lasso peptides. ChemBioChem 21:7–18. https://doi.org/10.1002/cbic.201900364
Hegemann JD, Fage CD, Zhu S et al (2016) The ring residue proline 8 is crucial for the thermal stability of the lasso peptide caulosegnin II. Mol Biosyst 12:1106–1109. https://doi.org/10.1039/C6MB00081A
Hopwood DA (2006) Soil to genomics: the streptomyces chromosome. Annu Rev Genet 40:1–23. https://doi.org/10.1146/annurev.genet.40.110405.090639
Ignasiak K, Maxwell A (2017) Galleria mellonella (greater wax moth) larvae as a model for antibiotic susceptibility testing and acute toxicity trials. BMC Res Notes 10:1–8. https://doi.org/10.1186/s13104-017-2757-8
Inokoshi J, Koyama N, Miyake M et al (2016) Structure-activity analysis of gram-positive bacterium-producing lasso peptides with anti-mycobacterial activity. Sci Rep 6:30375. https://doi.org/10.1038/srep30375
Islam MR, Nagao J, Zendo T, Sonomoto K (2012) Antimicrobial mechanism of lantibiotics. Biochem Soc Trans 40:1528–1533. https://doi.org/10.1042/BST20120190
Jabés D, Brunati C, Candiani G et al (2011) Efficacy of the new lantibiotic NAI-107 in experimental infections induced by multidrug-resistant gram-positive pathogens. Antimicrob Agents Chemother 55:1671–1676. https://doi.org/10.1128/AAC.01288-10
Kapoor G, Saigal S (2017) Action and resistance mechanisms of antibiotics: a guide for clinicians. J Anaesthesiol Clin Pharmacol 33:300. https://doi.org/10.4103/joacp.JOACP_349_15
Kivits T, Broers HP, Beeltje H et al (2018) Presence and fate of veterinary antibiotics in age-dated groundwater in areas with intensive livestock farming. Environ Pollut 241:988–998. https://doi.org/10.1016/j.envpol.2018.05.085
Knerr PJ, van der Donk WA (2012) Discovery, biosynthesis, and engineering of lantipeptides. Annu Rev Biochem 81:479–505. https://doi.org/10.1146/annurev-biochem-060110-113521
Komaki H, Sakurai K, Hosoyama A et al (2018) Diversity of nonribosomal peptide synthetase and polyketide synthase gene clusters among taxonomically close Streptomyces strains. Sci Rep 8:6888. https://doi.org/10.1038/s41598-018-24921-y
Kreft L, Botzki A, Coppens F et al (2017) PhyD3: A phylogenetic tree viewer with extended phyloXML support for functional genomics data visualization. Bioinformatics 33:2946–2947. https://doi.org/10.1093/bioinformatics/btx324
Kuroda M, Ohta T, Uchiyama I et al (2001) Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357:1225–1240. https://doi.org/10.1016/S0140-6736(00)04403-2
Lagesen K, Hallin P, Rødland EA et al (2007) Rnammer : Consistent and Rapid Annotation of Ribosomal RNA Genes 35:3100–3108. https://doi.org/10.1093/nar/gkm160
Laslett D, Canback B (2004) ARAGORN , a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic acid Res. https://doi.org/10.1093/nar/gkh152
Letsididi KS, Lou Z, Letsididi R et al (2018) Antimicrobial and antibiofilm effects of trans -cinnamic acid nanoemulsion and its potential application on lettuce. LWT 94:25–32. https://doi.org/10.1016/j.lwt.2018.04.018
Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714. https://doi.org/10.1093/bioinformatics/btn025
Liotti RG, da Silva Figueiredo MI, Soares MA (2019) Streptomyces griseocarneus R132 controls phytopathogens and promotes growth of pepper (Capsicum annuum). Biol Control 138:104065. https://doi.org/10.1016/j.biocontrol.2019.104065
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Magalhães dos Santos D, Sanches MP, Poffo CM, et al (2020) Syringic and cinnamic acids antiradical/antioxidant activities as R. ferruginea extract components and membrane physico-chemical influence. J Mol Struct 1220:128749. https://doi.org/10.1016/j.molstruc.2020.128749
Maravilla E, Le DP, Tran JJ et al (2020) Apolipophorin III interaction with phosphatidylglycerol and lipopolysaccharide: a potential mechanism for antimicrobial activity. Chem Phys Lipids 229:104909. https://doi.org/10.1016/j.chemphyslip.2020.104909
Mathur H, Field D, Rea MC, et al (2018) Fighting biofilms with lantibiotics and other groups of bacteriocins. npj Biofilms Microbiomes. 4(1):9. https://doi.org/10.1038/s41522-018-0053-6
Medema MH, Blin K, Cimermancic P et al (2011) antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 39:W339–W346. https://doi.org/10.1093/nar/gkr466
Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10:2182. https://doi.org/10.1038/s41467-019-10210-3
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics. https://doi.org/10.1186/1471-2105-14-60
Mendes SJF, Sousa FIAB, Pereira DMS et al (2016) Cinnamaldehyde modulates LPS-induced systemic inflammatory response syndrome through TRPA1-dependent and independent mechanisms. Int Immunopharmacol 34:60–70. https://doi.org/10.1016/j.intimp.2016.02.012
Ondov BD, Treangen TJ, Melsted P et al (2016) Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 17:1–14. https://doi.org/10.1186/s13059-016-0997-x
Perini HF, Moralez ATP, Almeida RSC et al (2019) Phenotypic switching in Candida tropicalis alters host-pathogen interactions in a Galleria mellonella infection model. Sci Rep 9:12555. https://doi.org/10.1038/s41598-019-49080-6
Pokhrel R, Bhattarai N, Baral P et al (2019) Molecular mechanisms of pore formation and membrane disruption by the antimicrobial lantibiotic peptide Mutacin 1140. Phys Chem Chem Phys 21:12530–12539. https://doi.org/10.1039/C9CP01558B
Porta-de-la-Riva M, Fontrodona L, Villanueva A, Cerón J (2012) Basic Caenorhabditis elegans Methods: Synchronization and Observation. JoVE e4019. https://doi.org/10.3791/4019
Qiu J, Zhuo Y, Zhu D et al (2011) Overexpression of the ABC transporter AvtAB increases avermectin production in Streptomyces avermitilis. Appl Microbiol Biotechnol 92:337–345. https://doi.org/10.1007/s00253-011-3439-4
Rastogi N (1998) Synergistic activities of antituberculous drugs with cerulenin and trans-cinnamic acid against Mycobacterium tuberculosis. FEMS Immunol Med Microbiol 21:149–157. https://doi.org/10.1016/S0928-8244(98)00044-3
Rastogi N, Goh KS, Wright EL, Barrow WW (1994) Potential drug targets for Mycobacterium avium defined by radiometric drug-inhibitor combination techniques. Antimicrob Agents Chemother 38:2287–2295. https://doi.org/10.1128/AAC.38.10.2287
Rather IA, Kim B-C, Bajpai VK, Park Y-H (2017) Self-medication and antibiotic resistance: Crisis, current challenges, and prevention. Saudi J Biol Sci 24:808–812. https://doi.org/10.1016/j.sjbs.2017.01.004
Robertson AW, MacLeod JM, MacIntyre LW et al (2018) Post polyketide synthase carbon-carbon bond formation in type-II PKS-derived natural products from streptomyces venezuelae. J Org Chem 83:1876–1890. https://doi.org/10.1021/acs.joc.7b02823
Seitz M, Valentin-Weigand P, Willenborg J (2016) Use of Antibiotics and Antimicrobial Resistance in Veterinary Medicine as Exemplified by the Swine Pathogen Streptococcus suis. In: Assessment & Evaluation in Higher Education. pp 103–121
Shaik HA, Mishra A, Sehadová H, Kodrík D (2020) Responses of sericotropin to toxic and pathogenic challenges: possible role in defense of the wax moth Galleria mellonella. Comp Biochem Physiol Part C Toxicol Pharmacol 227:108633. https://doi.org/10.1016/j.cbpc.2019.108633
Silva RHN, Andrade ACM, Nóbrega DF et al (2019) Antimicrobial activity of 4-chlorocinnamic acid derivatives. Biomed Res Int 2019:1–13. https://doi.org/10.1155/2019/3941242
Simão FA, Waterhouse RM, Ioannidis P et al (2015) BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212. https://doi.org/10.1093/bioinformatics/btv351
Simpson JT, Wong K, Jackman SD et al (2009) ABySS: A parallel assembler for short read sequence data. Genome Res 19:1117–1123. https://doi.org/10.1101/gr.089532.108
Singh R, Dubey AK (2020) Isolation and characterization of a new endophytic actinobacterium streptomyces californicus strain ADR1 as a promising source of anti-bacterial. Anti-Biofilm and Antioxidant Metabolites Microorganisms 8:929. https://doi.org/10.3390/microorganisms8060929
Singh LS, Sharma H, Talukdar NC (2014) Production of potent antimicrobial agent by actinomycete, Streptomyces sannanensis strain SU118 isolated from phoomdi in Loktak Lake of Manipur. India BMC Microbiol 14:278. https://doi.org/10.1186/s12866-014-0278-3
Soudy R, Etayash H, Bahadorani K et al (2017) Breast cancer targeting peptide binds keratin 1: a new molecular marker for targeted drug delivery to breast cancer. Mol Pharm 14:593–604. https://doi.org/10.1021/acs.molpharmaceut.6b00652
Stączek S, Zdybicka-Barabas A, Mak P et al (2018) Studies on localization and protein ligands of Galleria mellonella apolipophorin III during immune response against different pathogens. J Insect Physiol 105:18–27. https://doi.org/10.1016/j.jinsphys.2017.12.009
Stączek S, Zdybicka-Barabas A, Wiater A et al (2020) Activation of cellular immune response in insect model host Galleria mellonella by fungal α-1,3-glucan. Pathog Dis. https://doi.org/10.1093/femspd/ftaa062
Stanton BC, Nielsen AAK, Tamsir A et al (2014) Genomic mining of prokaryotic repressors for orthogonal logic gates. Nat Chem Biol 10:99–105. https://doi.org/10.1038/nchembio.1411
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197
Tian X, Zhang Z, Yang T et al (2016) Comparative genomics analysis of Streptomyces species reveals their adaptation to the marine environment and their diversity at the genomic level. Front Microbiol 7:1–16. https://doi.org/10.3389/fmicb.2016.00998
Trevijano-Contador N, Zaragoza O (2019) Immune response of Galleria mellonella against human fungal pathogens. J Fungi 5:1–13. https://doi.org/10.3390/jof5010003
Trevijano-Contador N, Herrero-Fernández I, García-Barbazán I et al (2015) Cryptococcus neoformans induces antimicrobial responses and behaves as a facultative intracellular pathogen in the non mammalian model Galleria mellonella. Virulence 6:66–74. https://doi.org/10.4161/21505594.2014.986412
Turner LB, Mueller-Harvey I, McAllan AB (1993) Light-induced isomerization and dimerization of cinnamic acid derivatives in cell walls. Phytochemistry 33:791–796. https://doi.org/10.1016/0031-9422(93)85276-W
Upadhyay A, Venkitanarayanan K (2016) In vivo efficacy of trans-cinnamaldehyde, carvacrol, and thymol in attenuating Listeria monocytogenes infection in a Galleria mellonella model. J Nat Med 70:667–672. https://doi.org/10.1007/s11418-016-0990-4
Valiante V, Monteiro MC, Martín J et al (2015) Hitting the caspofungin salvage pathway of human-pathogenic fungi with the novel lasso peptide humidimycin (MDN-0010). Antimicrob Agents Chemother 59:5145–5153. https://doi.org/10.1128/AAC.00683-15
Van der Horst DJ, Rodenburg KW (2010) Lipoprotein assembly and function in an evolutionary perspective. Biomol Concepts 1:165–183. https://doi.org/10.1515/bmc.2010.012
Vertyporokh L, Taszłow P, Samorek-Pieróg M, Wojda I (2015) Short-term heat shock affects the course of immune response in Galleria mellonella naturally infected with the entomopathogenic fungus Beauveria bassiana. J Invertebr Pathol 130:42–51. https://doi.org/10.1016/j.jip.2015.07.001
Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20. https://doi.org/10.1093/mp/ssp106
Wei J, He L, Niu G (2018) Regulation of antibiotic biosynthesis in actinomycetes: perspectives and challenges. Synth Syst Biotechnol 3:229–235
Wojda I (2017) Immunity of the greater wax moth Galleria mellonella. Insect Sci 24:342–357. https://doi.org/10.1111/1744-7917.12325
Wojda I, Jakubowicz T (2007) Humoral immune response upon mild heat-shock conditions in Galleria mellonella larvae. J Insect Physiol 53:1134–1144. https://doi.org/10.1016/j.jinsphys.2007.06.003
Wojda I, Kowalski P, Jakubowicz T (2009) Humoral immune response of Galleria mellonella larvae after infection by Beauveria bassiana under optimal and heat-shock conditions. J Insect Physiol 55:525–531. https://doi.org/10.1016/j.jinsphys.2009.01.014
Xin B, Zheng J, Liu H et al (2016) Thusin, a novel two-component lantibiotic with potent antimicrobial activity against several gram-positive pathogens. Front Microbiol 7:1–12. https://doi.org/10.3389/fmicb.2016.01115
Zhong Z, He B, Li J, Li Y-X (2020) Challenges and advances in genome mining of ribosomally synthesized and post-translationally modified peptides (RiPPs). Synth Syst Biotechnol 5:155–172. https://doi.org/10.1016/j.synbio.2020.06.002
Zimmermann M, Hegemann JD, Xie X, Marahiel MA (2013) The astexin-1 lasso peptides: biosynthesis, stability, and structural studies. Chem Biol 20:558–569. https://doi.org/10.1016/j.chembiol.2013.03.013
Acknowledgements
The authors thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, grant 3348/2013) and the Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT, grant # 0583867/2016) for the financial support.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
de Siqueira, K.A., Liotti, R.G., de Sousa, J.R. et al. Streptomyces griseocarneus R132 expresses antimicrobial genes and produces metabolites that modulate Galleria mellonella immune system. 3 Biotech 11, 396 (2021). https://doi.org/10.1007/s13205-021-02942-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-021-02942-1