A Human Lung-Associated Streptomyces sp. TR1341 Produces Various Secondary Metabolites Responsible for Virulence, Cytotoxicity and Modulation of Immune Response
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
32010093
PubMed Central
PMC6978741
DOI
10.3389/fmicb.2019.03028
Knihovny.cz E-zdroje
- Klíčová slova
- Streptomyces, actinomycin, cytolytic polyenes, hemolysis, human pneumonia, pathogenicity, secondary metabolites,
- Publikační typ
- časopisecké články MeSH
Streptomycetes, typical soil dwellers, can be detected as common colonizers of human bodies, especially the skin, the respiratory tract, the guts and the genital tract using molecular techniques. However, their clinical manifestations and isolations are rare. Recently they were discussed as possible "coaches" of the human immune system in connection with certain immune disorders and cancer. This work aimed for the characterization and evaluation of genetic adaptations of a human-associated strain Streptomyces sp. TR1341. The strain was isolated from sputum of a senior male patient with a history of lung and kidney TB, recurrent respiratory infections and COPD. It manifested remarkably broad biological activities (antibacterial, antifungal, beta-hemolytic, etc.). We found that, by producing specific secondary metabolites, it is able to modulate host immune responses and the niche itself, which increase its chances for long-term survival in the human tissue. The work shows possible adaptations or predispositions of formerly soil microorganism to survive in human tissue successfully. The strain produces two structural groups of cytotoxic compounds: 28-carbon cytolytic polyenes of the filipin type and actinomycin X2. Additionally, we summarize and present data about streptomycete-related human infections known so far.
Faculty of Science University of South Bohemia České Budějovice Czechia
Institute of Immunology and Microbiology 1st Faculty of Medicine Charles University Prague Czechia
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Alanjary M., Steinke K., Ziemert N. (2019). AutoMLST: an automated web server for generating multi-locus species trees highlighting natural product potential. Nucleic Acids Res. 47 W276–W282. 10.1093/nar/gkz282 PubMed DOI PMC
Awad A. H. A., Farag S. A. (1999). An indoor bio-contaminants air quality. Int. J. Environ. Health Res. 9 313–319. 10.1080/09603129973100 DOI
Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., et al. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19 455–477. 10.1089/cmb.2012.0021 PubMed DOI PMC
Barka E. A., Vatsa P., Sanchez L., Gaveau-Vaillant N., Jacquard C., Meier-Kolthoff J. P., et al. (2016). Taxonomy, physiology, and natural products of Actinobacteria. Microbiol. Mol. Biol. Rev. 80 1–43. 10.1128/MMBR.00019-15 PubMed DOI PMC
Barke J., Seipke R. F., Gruschow S., Heavens D., Drou N., Bibb M. J., et al. (2010). A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biol. 8:109. 10.1186/1741-7007-8-109 PubMed DOI PMC
Behie S. W., Bonet B., Zacharia V. M., McClung D. J., Traxler M. F. (2016). Molecules to ecosystems: actinomycete natural products in situ. Front. Microbiol. 7:2149. 10.3389/fmicb.2016.02149 PubMed DOI PMC
Bolger A. M., Lohse M., Usadel B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30 2114–2120. 10.1093/bioinformatics/btu170 PubMed DOI PMC
Bolourian A., Mojtahedi Z. (2018a). Immunosuppressants produced by Streptomyces: evolution, hygiene hypothesis, tumour rapalog resistance and probiotics. Environ. Microbiol. Rep. 10 123–126. 10.1111/1758-2229.12617 PubMed DOI
Bolourian A., Mojtahedi Z. (2018b). Streptomyces, shared microbiome member of soil and gut, as ‘old friends’ against colon cancer. FEMS Microbiol. Ecol. 94:fiy120. 10.1093/femsec/fiy120 PubMed DOI
Boya C. A., Fernandez-Marin H., Mejia L. C., Spadafora C., Dorrestein P. C., Gutierrez M. (2017). Imaging mass spectrometry and MS/MS molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing ants. Sci. Rep. 7:5604. 10.1038/s41598-017-05515-6 PubMed DOI PMC
Cano-Jimenez E., Acuna A., Botana M. I., Hermida T., Gonzalez M. G., Leiro V., et al. (2016). Farmer’s lung disease. A review. Arch. Bronconeumol. 52 321–328. 10.1016/j.arbres.2015.12.001 PubMed DOI
Castanho M. A., Coutinho A., Prieto M. J. (1992). Absorption and fluorescence spectra of polyene antibiotics in the presence of cholesterol. J. Biol. Chem. 267 204–209. PubMed
Challacombe J. F., Stubben C. J., Klimko C. P., Welkos S. L., Kern S. J., Bozue J. A., et al. (2014). Interrogation of the Burkholderia pseudomallei genome to address differential virulence among isolates. PLoS One 9:e115951. 10.1371/journal.pone.0115951 PubMed DOI PMC
Chater K. F., Hopwood D. A. (1993). “Streptomyces,” in Bacillus subtilis and Other Gram-Positive Bacteria. Biochemistry, Physiology, and Molecular Genetics, eds Sonenshein A. L., Hoch J. A., Losick R. (Washington, DC: American Society for Microbiology; ), 83–100.
Chun J., Lee J. H., Jung Y., Kim M., Kim S., Kim B. K., et al. (2007). EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int. J. Syst. Evol. Microbiol. 57 2259–2261. PubMed
Cihak M., Kamenik Z., Smidova K., Bergman N., Benada O., Kofronova O., et al. (2017). Secondary metabolites produced during the germination of Streptomyces coelicolor. Front. Microbiol. 8:2495. 10.3389/fmicb.2017.02495 PubMed DOI PMC
Collado M. C., Rautava S., Aakko J., Isolauri E., Salminen S. (2016). Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci. Rep. 6:23129. 10.1038/srep23129 PubMed DOI PMC
Egan S., Wiener P., Kallifidas D., Wellington E. M. (2001). Phylogeny of Streptomyces species and evidence for horizontal transfer of entire and partial antibiotic gene clusters. Antonie Van Leeuwenhoek 79 127–133. 10.1023/A:1010296220929 PubMed DOI
Engevik M. A., Versalovic J. (2017). Biochemical features of beneficial microbes: foundations for therapeutic microbiology. Microbiol. Spectr. 5:BAD-0012-2016. 10.1128/microbiolspec.BAD-0012-2016 PubMed DOI PMC
Forrellad M. A., Klepp L. I., Gioffre A., Sabio y Garcia J., Morbidoni H. R., de la Paz Santangelo M., et al. (2013). Virulence factors of the Mycobacterium tuberculosis complex. Virulence 4 3–66. 10.4161/viru.22329 PubMed DOI PMC
Furukawa M., Inoue A., Asano K. (1968). Chemical studies on actinomycin S. II. Chemical structures of actinomycin S2 and S3. J. Antibiot. 21 568–570. 10.7164/antibiotics.21.568 PubMed DOI
Gallo R. L., Hooper L. V. (2012). Epithelial antimicrobial defence of the skin and intestine. Nat. Rev. Immunol. 12 503–516. 10.1038/nri3228 PubMed DOI PMC
Gurevich A., Saveliev V., Vyahhi N., Tesler G. (2013). QUAST: quality assessment tool for genome assemblies. Bioinformatics 29 1072–1075. 10.1093/bioinformatics/btt086 PubMed DOI PMC
Gust B., Chandra G., Jakimowicz D., Yuqing T., Bruton C. J., Chater K. F. (2004). Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces. Adv. Appl. Microbiol. 54 107–128. PubMed
Haeder S., Wirth R., Herz H., Spiteller D. (2009). Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis. Proc. Natl. Acad. Sci. U.S.A. 106 4742–4746. 10.1073/pnas.0812082106 PubMed DOI PMC
Hobbs G., Frazer C. M., Gardner D. C. J., Cullum J. A., Oliver S. G. (1989). Dispersed growth of Streptomyces in liquid culture. Appl. Microbiol. Biotechnol. 31 272–277. 10.1007/BF00258408 DOI
Hou B. B., Tao L. Y., Zhu X. Y., Wu W., Guo M. J., Ye J., et al. (2018). Global regulator BldA regulates morphological differentiation and lincomycin production in Streptomyces lincolnensis. Appl. Microbiol. Biotechnol. 102 4101–4115. 10.1007/s00253-018-8900-1 PubMed DOI
Huang Y. J., Nariya S., Harris J. M., Lynch S. V., Choy D. F., Arron J. R., et al. (2015). The airway microbiome in patients with severe asthma: associations with disease features and severity. J. Allergy Clin. Immunol. 136 874–884. 10.1016/j.jaci.2015.05.044 PubMed DOI PMC
Huttunen K., Hyvarinen A., Nevalainen A., Komulainen H., Hirvonen M. R. (2003). Production of proinflammatory mediators by indoor air bacteria and fungal spores in mouse and human cell lines. Environ. Health Perspect. 111 85–92. 10.1289/ehp.5478 PubMed DOI PMC
Kaltenpoth M., Gottler W., Herzner G., Strohm E. (2005). Symbiotic bacteria protect wasp larvae from fungal infestation. Curr. Biol. 15 475–479. 10.1016/j.cub.2004.12.084 PubMed DOI
Kampfer P., Glaeser S. P., Parkes L., Van Keulen G., Dyson P. (2014). “The Family Streptomycetaceae,” in The Prokaryotes: Actinobacteria, eds Rosenberg E., DeLong E. F., Lory S., Stackebrandt E., Thompson F. (Berlin: Springer; ).
Kapadia M., Rolston K. V. I., Han X. Y. (2007). Invasive Streptomyces infections - Six cases and literature review. Am. J. Clin. Pathol. 127 619–624. 10.1309/QJEBXP0BCGR54L15 PubMed DOI
Kim J. D., Han J. W., Hwang I. C., Lee D., Kim B. S. (2012). Identification and biocontrol efficacy of Streptomyces miharaensis producing filipin III against Fusarium wilt. J. Basic Microbiol. 52 150–159. 10.1002/jobm.201100134 PubMed DOI
Kirby R., Sangal V., Tucker N. P., Zakrzewska-Czerwinska J., Wierzbicka K., Herron P. R., et al. (2012). Draft genome sequence of the human pathogen Streptomyces somaliensis, a significant cause of actinomycetoma. J. Bacteriol. 194 3544–3545. 10.1128/JB.00534-12 PubMed DOI PMC
Knopik-Skrocka A., Bielawski J. (2002). The mechanism of the hemolytic activity of polyene antibiotics. Cell. Mol. Biol. Lett. 7 31–48. PubMed
Kozlov A. M., Darriba D., Flouri T., Morel B., Stamatakis A. (2019). RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35 4453–4455. 10.1093/bioinformatics/btz305 PubMed DOI PMC
Labeda D. P., Goodfellow M., Brown R., Ward A. C., Lanoot B., Vanncanneyt M., et al. (2012). Phylogenetic study of the species within the family Streptomycetaceae. Antonie Van Leeuwenhoek 101 73–104. PubMed
Langmead B., Salzberg S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 357–359. 10.1038/nmeth.1923 PubMed DOI PMC
Lee J. S., Yilmaz O. (2018). Unfolding role of a danger molecule adenosine signaling in modulation of microbial infection and host cell response. Int. J. Mol. Sci. 19:E199. 10.3390/ijms19010199 PubMed DOI PMC
Liu C. X., Han C. Y., Jiang S. W., Zhao X. L., Tian Y. Y., Yan K., et al. (2018). Streptomyces lasii sp nov., a novel actinomycete with antifungal activity isolated from the head of an ant (Lasius flavus). Curr. Microbiol. 75 353–358. 10.1007/s00284-017-1388-6 PubMed DOI
Liu J., Xie S., Wu Y., Xu M., Ao C., Wang W., et al. (2016). Apoptosis of human prostate cancer cells induced by marine actinomycin X2 through the mTOR pathway compounded by MiRNA144. Anticancer Drugs 27 156–163. 10.1097/CAD.0000000000000309 PubMed DOI
Magoc T., Salzberg S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27 2957–2963. 10.1093/bioinformatics/btr507 PubMed DOI PMC
Martin M. C., Manteca A., Castillo M. L., Vazquez F., Mendez F. J. (2004). Streptomyces albus isolated from a human actinomycetoma and characterized by molecular techniques. J. Clin. Microbiol. 42 5957–5960. 10.1128/JCM.42.12.5957-5960.2004 PubMed DOI PMC
May H. C., Yu J. J., Zhang H., Wang Y., Cap A. P., Chambers J. P., et al. (2019). Thioredoxin-A is a virulence factor and mediator of the type IV pilus system in Acinetobacter baumannii. PLoS One 14:e0218505. 10.1371/journal.pone.0218505 PubMed DOI PMC
McDonald B. R., Currie C. R. (2017). Lateral gene transfer dynamics in the ancient bacterial genus Streptomyces. mBio 8:e00644-17. 10.1128/mBio.00644-17 PubMed DOI PMC
McLean T. C., Hoskisson P. A., Seipke R. F. (2016). Coordinate regulation of antimycin and candicidin biosynthesis. mSphere 1:e00305-16. PubMed PMC
McNeil M. M., Brown J. M., Jarvis W. R., Ajello L. (1990). Comparison of species distribution and antimicrobial susceptibility of aerobic actinomycetes from clinical specimens. Rev. Inf. Dis. 12 778–783. PubMed
Miethke M., Marahiel M. A. (2007). Siderophore-based iron acquisition and pathogen control. Microbiol. Mol. Biol. Rev. 71 413–451. PubMed PMC
Molloy E. M., Cotter P. D., Hill C., Mitchell D. A., Ross R. P. (2011). Streptolysin S-like virulence factors: the continuing sagA. Nat. Rev. Microbiol. 9 670–681. 10.1038/nrmicro2624 PubMed DOI PMC
Muth G., Nusbaumer B., Wohlleben W., Puhler A. (1989). A vector system with temperature-sensitive replication for gene disruption and mutational cloning in streptomycetes. Mol. Gen. Genet. 219 341–348. 10.1007/Bf00259605 DOI
Nechitaylo T. Y., Westermann M., Kaltenpoth M. (2014). Cultivation reveals physiological diversity among defensive ‘Streptomyces philanthi’ symbionts of beewolf digger wasps (Hymenoptera, Crabronidae). BMC Microbiol. 14:202. 10.1186/s12866-014-0202-x PubMed DOI PMC
Ochi K. (1987). Metabolic initiation of differentiation and secondary metabolism by Streptomyces griseus: significance of the stringent response (ppGpp) and GTP content in relation to A factor. J. Bacteriol. 169 3608–3616. 10.1128/jb.169.8.3608-3616.1987 PubMed DOI PMC
Oh D. C., Poulsen M., Currie C. R., Clardy J. (2011). Sceliphrolactam, a polyene macrocyclic lactam from a wasp-associated Streptomyces sp. Org. Lett. 13 752–755. 10.1021/ol102991d PubMed DOI PMC
Oh D. C., Scott J. J., Currie C. R., Clardy J. (2009). Mycangimycin, a polyene peroxide from a mutualist Streptomyces sp. Org. Lett. 11 633–636. 10.1021/ol802709x PubMed DOI PMC
Okonechnikov K., Conesa A., Garcia-Alcalde F. (2016). Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 32 292–294. 10.1093/bioinformatics/btv566 PubMed DOI PMC
Olano C., Mendez C., Salas J. A. (2009). Antitumor compounds from actinomycetes: from gene clusters to new derivatives by combinatorial biosynthesis. Nat. Prod. Rep. 26 628–660. 10.1039/b822528a PubMed DOI
Park S. Y., Kang H. O., Jang H. S., Lee J. K., Koo B. T., Yum D. Y. (2005). Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl. Environ. Microbiol. 71 2632–2641. 10.1128/AEM.71.5.2632-2641.2005 PubMed DOI PMC
Parrot D., Blumel M., Utermann C., Chianese G., Krause S., Kovalev A., et al. (2019). Mapping the surface microbiome and metabolome of brown seaweed Fucus vesiculosus by amplicon sequencing, integrated metabolomics and imaging techniques. Sci. Rep. 9:1061. 10.1038/s41598-018-37914-8 PubMed DOI PMC
Payero T. D., Vicente C. M., Rumbero A., Barreales E. G., Santos-Aberturas J., de Pedro A., et al. (2015). Functional analysis of filipin tailoring genes from Streptomyces filipinensis reveals alternative routes in filipin III biosynthesis and yields bioactive derivatives. Microb. Cell Fact. 14:114. 10.1186/s12934-015-0307-4 PubMed DOI PMC
Pellegrini G. J., Graziano J. C., Ragunathan L., Bhat M. A., Hemashettar B. M., Brown J. M. (2012). Scalp abscess due to Streptomyces cacaoi subsp. cacaoi, first report in a human infection. J. Clin. Microbiol. 50 1484–1486. 10.1128/JCM.06372-11 PubMed DOI PMC
Petrickova K., Pospisil S., Kuzma M., Tylova T., Jagr M., Tomek P., et al. (2014). Biosynthesis of colabomycin E, a new manumycin-family metabolite, involves an unusual chain-length factor. Chembiochem 15 1334–1345. 10.1002/cbic.201400068 PubMed DOI
Poulsen M., Oh D. C., Clardy J., Currie C. R. (2011). Chemical analyses of wasp-associated Streptomyces bacteria reveal a prolific potential for natural products discovery. PLoS One 6:e16763. 10.1371/journal.pone.0016763 PubMed DOI PMC
Rahman A., Srivastava S. S., Sneh A., Ahmed N., Krishnasastry M. V. (2010). Molecular characterization of tlyA gene product, Rv1694 of Mycobacterium tuberculosis: a non-conventional hemolysin and a ribosomal RNA methyl transferase. BMC Biochem. 11:35. 10.1186/1471-2091-11-35 PubMed DOI PMC
Rahman M. A., Sobia P., Dwivedi V. P., Bhawsar A., Singh D. K., Sharma P., et al. (2015). Mycobacterium tuberculosis TlyA protein negatively regulates T helper (Th) 1 and Th17 differentiation and promotes tuberculosis pathogenesis. J. Biol. Chem. 290 14407–14417. 10.1074/jbc.M115.653600 PubMed DOI PMC
Rajesh T., Jeon J. M., Kim Y. H., Kim H. J., Yi da H., Park S. H., et al. (2013). Functional analysis of the gene SCO1782 encoding Streptomyces hemolysin (S-hemolysin) in Streptomyces coelicolor M145. Toxicon 71 159–165. 10.1016/j.toxicon.2013.05.023 PubMed DOI
Rea D., Coppola G., Palma G., Barbieri A., Luciano A., Del Prete P., et al. (2018). Microbiota effects on cancer: from risks to therapies. Oncotarget 9 17915–17927. 10.18632/oncotarget.24681 PubMed DOI PMC
Relhan V., Mahajan K., Agarwal P., Garg V. K. (2017). Mycetoma: an update. Indian J. Dermatol. 62 332–340. 10.4103/ijd.IJD_476_16 PubMed DOI PMC
Roussel S., Reboux G., Dalphin J. C., Pernet D., Laplante J. J., Millon L., et al. (2005). Farmer’s lung disease and microbiological composition of hay: a case-control study. Mycopathologia 160 273–279. PubMed
Ryan R. P., An S. Q., Allan J. H., McCarthy Y., Dow J. M. (2015). The DSF family of cell-cell signals: an expanding class of bacterial virulence regulators. PLoS Pathog. 11:e1004986. 10.1371/journal.ppat.1004986 PubMed DOI PMC
Santos C. L., Correia-Neves M., Moradas-Ferreira P., Mendes M. V. (2012). A walk into the LuxR regulators of Actinobacteria: phylogenomic distribution and functional diversity. PLoS One 7:e46758. 10.1371/journal.pone.0046758 PubMed DOI PMC
Sarmiento-Ramirez J. M., van der Voort M., Raaijmakers J. M., Dieguez-Uribeondo J. (2014). Unravelling the microbiome of eggs of the endangered sea turtle Eretmochelys imbricata identifies bacteria with activity against the emerging pathogen Fusarium falciforme. PLoS One 9:e95206. 10.1371/journal.pone.0095206 PubMed DOI PMC
Schoenian I., Spiteller M., Ghaste M., Wirth R., Herz H., Spiteller D. (2011). Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proc. Natl. Acad. Sci. U.S.A. 108 1955–1960. 10.1073/pnas.1008441108 PubMed DOI PMC
Seipke R. F., Barke J., Brearley C., Hill L., Yu D. W., Goss R. J., et al. (2011). A single Streptomyces symbiont makes multiple antifungals to support the fungus farming ant Acromyrmex octospinosus. PLoS One 6:e22028. 10.1371/journal.pone.0022028 PubMed DOI PMC
Sharma M., Manhas R. K. (2019). Purification and characterization of actinomycins from Streptomyces strain M7 active against methicillin resistant Staphylococcus aureus and vancomycin resistant Enterococcus. BMC Microbiol. 19:44. 10.1186/s12866-019-1405-y PubMed DOI PMC
Shintani M., Matsui K., Inoue J., Hosoyama A., Ohji S., Yamazoe A., et al. (2014). Single-cell analyses revealed transfer ranges of IncP-1, IncP-7, and IncP-9 plasmids in a soil bacterial community. Appl. Environ. Microbiol. 80 138–145. 10.1128/AEM.02571-13 PubMed DOI PMC
Silva P. E. S., Reis M. P., Avila M. P., Dias M. F., Costa P. S., Suhadolnik M. L. S., et al. (2018). Insights into the skin microbiome dynamics of leprosy patients during multi-drug therapy and in healthy individuals from Brazil. Sci. Rep. 8:8783. 10.1038/s41598-018-27074-0 PubMed DOI PMC
Sing D., Sing C. F. (2010). Impact of direct soil exposures from airborne dust and geophagy on human health. Int. J. Environ. Res. Publ. Health 7 1205–1223. 10.3390/ijerph7031205 PubMed DOI PMC
Somboro A. M., Osei Sekyere J., Amoako D. G., Essack S. Y., Bester L. A. (2018). Diversity and proliferation of metallo-beta-lactamases: a clarion call for clinically effective metallo-beta-lactamase inhibitors. Appl. Environ. Microbiol. 84:e00698-18. 10.1128/AEM.00698-18 PubMed DOI PMC
Striz I., Krasna E., Petrickova K., Brabcova E., Kolesar L., Slavcev A., et al. (2008). Manumycin and asukamycin inhibition of IL-1beta and IL-18 release from human macrophages by caspase-1 blocking. Allergy 63 142–143.
Stubbendieck R. M., Vargas-Bautista C., Straight P. D. (2016). Bacterial communities: interactions to scale. Front. Microbiol. 7:1234. 10.3389/fmicb.2016.01234 PubMed DOI PMC
Tingstad J. E., Garrett E. R. (1960). Studies on the stability of filipin.1. Thermal degradation in the presence of air. J. Am. Pharm. Assoc. 49 352–355. 10.1002/jps.3030490607 PubMed DOI
van de Sande W. W. J. (2013). Global burden of human mycetoma: a systematic review and meta-analysis. PLoS Negl. Trop. Dis. 7:e2550. 10.1371/journal.pntd.0002550 PubMed DOI PMC
Vandenesch F., Lina G., Henry T. (2012). Staphylococcus aureus hemolysins, bi-component leukocidins, and cytolytic peptides: a redundant arsenal of membrane-damaging virulence factors? Front. Cell. Infect. Microbiol. 2:12. 10.3389/fcimb.2012.00012 PubMed DOI PMC
Verma P., Jha A. (2019). Mycetoma: reviewing a neglected disease. Clin. Exp. Dermatol. 44 123–129. 10.1111/ced.13642 PubMed DOI
Vicente C. M., Santos-Aberturas J., Payero T. D., Barreales E. G., de Pedro A., Aparicio J. F. (2014). PAS-LuxR transcriptional control of filipin biosynthesis in S. avermitilis. Appl. Microbiol. Biotechnol. 98 9311–9324. 10.1007/s00253-014-5998-7 PubMed DOI
Wang J., Xu J., Luo S., Ma Z., Bechthold A., Yu X. P. (2018). AdpAsd, a positive regulator for morphological development and toyocamycin biosynthesis in Streptomyces diastatochromogenes 1628. Curr. Microbiol. 75 1345–1351. PubMed
Wang R., Zhang M., Liu H., Xu J., Yu J., He F., et al. (2016). PsAAT3, an oomycete-specific aspartate aminotransferase, is required for full pathogenicity of the oomycete pathogen Phytophthora sojae. Fungal Biol. 120 620–630. 10.1016/j.funbio.2016.01.005 PubMed DOI
Wu X., Chen J., Xu M., Zhu D., Wang X., Chen Y., et al. (2017). 16S rDNA analysis of periodontal plaque in chronic obstructive pulmonary disease and periodontitis patients. J. Oral Microbiol. 9:1324725. 10.1080/20002297.2017.1324725 PubMed DOI PMC
Yacoub A. T., Velez A. P., Khwaja S. I., Sandin R. L., Greene J. (2014). Streptomyces pneumonia in an immunocompromised patient: a case report and a review of literature. Inf. Dis. Clin. Pract. 22 e113–e115. 10.1097/IPC.0000000000000172 DOI
Polyenic Antibiotics and Other Antifungal Compounds Produced by Hemolytic Streptomyces Species