DeoR regulates lincomycin production in Streptomyces lincolnensis.
DeoR family
Lincomycin
Streptomyces lincolnensis
Transcriptional regulation
Journal
World journal of microbiology & biotechnology
ISSN: 1573-0972
Titre abrégé: World J Microbiol Biotechnol
Pays: Germany
ID NLM: 9012472
Informations de publication
Date de publication:
06 Oct 2023
06 Oct 2023
Historique:
received:
14
07
2023
accepted:
02
10
2023
medline:
2
11
2023
pubmed:
6
10
2023
entrez:
6
10
2023
Statut:
epublish
Résumé
Regulators belonging to the DeoR family are widely distributed among the bacteria. Few studies have reported that DeoR family proteins regulate secondary metabolism of Streptomyces. This study explored the function of DeoR (SLINC_8027) in Streptomyces lincolnensis. Deletion of deoR in NRRL 2936 led to an increase in cell growth. The lincomycin production of the deoR deleted strain ΔdeoR was 3.4-fold higher than that of the wild strain. This trait can be recovered to a certain extent in the deoR complemented strain ΔdeoR::pdeoR. According to qRT-PCR analysis, DeoR inhibited the transcription of all detectable genes in the lincomycin biosynthesis cluster and repressed the expression of glnR, bldD, and SLCG_Lrp, which encode regulators outside the cluster. DeoR also inhibited the transcription of itself, as revealed by the XylE reporter. Furthermore, we demonstrated that DeoR bound directly to the promoter region of deoR, lmbA, lmbC-D, lmbJ-K, lmrA, lmrC, glnR, and SLCG_Lrp, by recognizing the 5'-CGATCR-3' motif. This study found that versatile regulatory factor DeoR negatively regulates lincomycin biosynthesis and cellular growth in S. lincolnensis, which expanded the regulatory network of lincomycin biosynthesis.
Identifiants
pubmed: 37801155
doi: 10.1007/s11274-023-03788-w
pii: 10.1007/s11274-023-03788-w
doi:
Substances chimiques
Lincomycin
BOD072YW0F
Bacterial Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
332Subventions
Organisme : National Natural Science Foundation of China
ID : 31900059
Organisme : Ministry of Science and Technology of the People's Republic of China
ID : 2021YFC2100600
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Baek M, DiMaio F, Anishchenko I et al (2021) Accurate prediction of protein structures and interactions using a three-track neural network. Science 373(6557):871–876. https://doi.org/10.1126/science.abj8754
doi: 10.1126/science.abj8754
pubmed: 34282049
pmcid: 7612213
Barka EA, Vatsa P, Sanchez L et al (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80(1):1–43. https://doi.org/10.1128/MMBR.00019-15
doi: 10.1128/MMBR.00019-15
pubmed: 26609051
Bierman M, Logan R, O’Brien K et al (1992) Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116(1):43–49. https://doi.org/10.1016/0378-1119(92)90627-2
doi: 10.1016/0378-1119(92)90627-2
pubmed: 1628843
Dalton KA, Thibessard A, Hunter JI et al (2007) A novel compartment, the ‘subapical stem’ of the aerial hyphae, is the location of a sigN-dependent, developmentally distinct transcription in Streptomyces coelicolor. Mol Microbiol 64(3):719–737. https://doi.org/10.1111/j.1365-2958.2007.05684.x
doi: 10.1111/j.1365-2958.2007.05684.x
pubmed: 17462019
Deng L, Zhao Z, Liu L et al (2023) Dissection of 3D chromosome organization in Streptomyces coelicolor A3 (2) leads to biosynthetic gene cluster overexpression. Proc Natl Acad Sci U S A 120(11):e2222045120. https://doi.org/10.1073/pnas.2222045120
doi: 10.1073/pnas.2222045120
pubmed: 36877856
pmcid: 10242723
Gaigalat L, Schluter JP, Hartmann M et al (2007) The DeoR-type transcriptional regulator SugR acts as a repressor for genes encoding the phosphoenolpyruvate: phosphotransferase system (PTS) in Corynebacterium glutamicum. Bmc Mol Biol 8(104). https://doi.org/10.1186/1471-2199-8-104
Garces F, Fernández FJ, Gómez AM et al (2008) Quaternary structural transitions in the DeoR-type repressor UlaR control transcriptional readout from the L-Ascorbate utilization regulon in Escherichia coli. Biochemistry 47(44):11424–11433. https://doi.org/10.1021/bi800748x
doi: 10.1021/bi800748x
pubmed: 18844374
Gaurivaud P, Laigret F, Garnier M et al (2001) Characterization of FruR as a putative activator of the fructose operon of Spiroplasma citri. FEMS Microbiol Lett 198(1):73–78. https://doi.org/10.1111/j.1574-6968.2001.tb10621.x
doi: 10.1111/j.1574-6968.2001.tb10621.x
pubmed: 11325556
Ge B, Liu Y, Liu B et al (2016) Characterization of novel DeoR-family member from the Streptomyces ahygroscopicus strain CK-15 that acts as a repressor of morphological development. Appl Microbiol Biotechnol 100:8819–8828. https://doi.org/10.1007/s00253-016-7661-y
doi: 10.1007/s00253-016-7661-y
pubmed: 27372076
Grant SR, Fisher EJ, Chang JH et al (2006) Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu Rev Microbiol 60:425–449. https://doi.org/10.1146/annurev.micro.60.080805.142251
doi: 10.1146/annurev.micro.60.080805.142251
pubmed: 16753033
Hamedi J, Poorinmohammad N, Papiran R (2017) Growth and life cycle of Actinobacteria. In: Wink J, Mohammadipanah F, Hamedi J (eds) Biology and Biotechnology of Actinobacteria. Springer, Cham
Hou B, Lin Y, Wu H et al (2018a) The novel transcriptional regulator LmbU promotes lincomycin biosynthesis through regulating expression of its target genes in Streptomyces lincolnensis. J Bacteriol 200(2):10–1128. https://doi.org/10.1128/JB.00447-17
doi: 10.1128/JB.00447-17
Hou B, Tao L, Zhu X et al (2018b) Global regulator BldA regulates morphological differentiation and lincomycin production in Streptomyces lincolnensis. Appl Microbiol Biotechnol 102:4101–4115. https://doi.org/10.1007/s00253-018-8900-1
doi: 10.1007/s00253-018-8900-1
pubmed: 29549449
Hou B, Wang R, Zou J et al (2021) A putative redox-sensing regulator Rex regulates lincomycin biosynthesis in Streptomyces lincolnensis. J Basic Microbiol 61(9):772–781. https://doi.org/10.1002/jobm.202100249
doi: 10.1002/jobm.202100249
pubmed: 34313330
Huang H, Zheng G, Jiang W et al (2015) One-step high-efficiency CRISPR/Cas9-mediated genome editing in Streptomyces. Acta Biochim Biophys Sin 47(4):231–243. https://doi.org/10.1093/abbs/gmv007
doi: 10.1093/abbs/gmv007
pubmed: 25739462
Jeon J-M, Choi T-R, Lee B-R et al (2019) Decreased growth and antibiotic production in Streptomyces coelicolor A3(2) by deletion of a highly conserved DeoR family regulator, SCO1463. Biotechnol Bioprocess Eng 24:613–621. https://doi.org/10.1007/s12257-019-0084-8
doi: 10.1007/s12257-019-0084-8
Johnson M, Zaretskaya I, Raytselis Y et al (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36(suppl2):W5–W9. https://doi.org/10.1093/nar/gkn201
doi: 10.1093/nar/gkn201
pubmed: 18440982
pmcid: 2447716
Kang Y, Wang Y, Hou B et al (2019) AdpA
doi: 10.3389/fmicb.2019.02428
pubmed: 31708899
pmcid: 6819324
Kang Y, Wu W, Zhang F et al (2023) AdpA
doi: 10.1002/jobm.202200692
pubmed: 36734183
Kieser T, Bibb MJ, Buttner MJ et al (2000) Practical Streptomyces genetics. John Innes Foundation. https://doi.org/10.1111/j.1365-2427.2007.01876.x
doi: 10.1111/j.1365-2427.2007.01876.x
Koberska M, Vesela L, Vimberg V et al (2021) Beyond self-resistance: ABCF ATPase LmrC is a signal-transducing component of an antibiotic-driven signaling cascade accelerating the onset of lincomycin biosynthesis. mBio 12(5):10-1128. https://doi.org/10.1128/mbio.01731-21
Koberská M, Kopecký J, Olsovská J et al (2008) Sequence analysis and heterologous expression of the lincomycin biosynthetic cluster of the type strain Streptomyces lincolnensis ATCC 25466. Folia Microbiol 53:395–401. https://doi.org/10.1007/s12223-008-0060-8
doi: 10.1007/s12223-008-0060-8
Küster E (1959) Outline of a comparative study of criteria used in characterization of the actinomycetes. Int Bull Bacteriological Nomenclature Taxonomy 9(2):97–104. https://doi.org/10.1099/0096266x-9-2-97
doi: 10.1099/0096266x-9-2-97
Li Y, Tan H (2017) Biosynthesis and molecular regulation of secondary metabolites in microorganisms. Sci China Life Sci 60:935–938. https://doi.org/10.1007/s11427-017-9115-x
doi: 10.1007/s11427-017-9115-x
pubmed: 28785948
MacNeil DJ, Occi JL, Gewain KM et al (1992) Complex organization of the Streptomyces avermitilis genes encoding the avermectin polyketide synthase. Gene 115(1–2):119–125. https://doi.org/10.1016/0378-1119(92)90549-5
doi: 10.1016/0378-1119(92)90549-5
pubmed: 1612425
Marchler-Bauer A, Bo Y, Han L et al (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45(D1):D200–D203. https://doi.org/10.1093/nar/gkw1129
doi: 10.1093/nar/gkw1129
pubmed: 27899674
Meng S, Wu H, Wang L et al (2017) Enhancement of antibiotic productions by engineered nitrate utilization in actinomycetes. Appl Microbiol Biotechnol 101:5341–5352. https://doi.org/10.1007/s00253-017-8292-7
doi: 10.1007/s00253-017-8292-7
pubmed: 28455615
Mortensen L, Dandanell G, Hammer K (1989) Purification and characterization of the deoR repressor of Escherichia coli. EMBO J 8(1):325–331. https://doi.org/10.1002/j.1460-2075.1989.tb03380.x
doi: 10.1002/j.1460-2075.1989.tb03380.x
pubmed: 2653814
pmcid: 400807
Procópio REL, Silva IR, Martins MK et al (2012) Antibiotics produced by Streptomyces. Braz J Infect Dis 16:466–471. https://doi.org/10.1016/j.bjid.2012.08.014
doi: 10.1016/j.bjid.2012.08.014
pubmed: 22975171
Řezáčová P, Kožíšek M, Moy SF et al (2008) Crystal structures of the effector-binding domain of repressor central glycolytic gene regulator from Bacillus subtilis reveal ligand-induced structural changes upon binding of several glycolytic intermediates. Mol Microbiol 69(4):895–910. https://doi.org/10.1111/j.1365-2958.2008.06318.x
doi: 10.1111/j.1365-2958.2008.06318.x
pubmed: 18554327
pmcid: 2764557
Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42(W1):W320–W324. https://doi.org/10.1093/nar/gku316
doi: 10.1093/nar/gku316
pubmed: 24753421
pmcid: 4086106
Romero-Rodriguez A, Robledo-Casados I, Sánchez S (2015) An overview on transcriptional regulators in Streptomyces. Biochim Biophys Acta 1849(8):1017–1039. https://doi.org/10.1016/j.bbagrm.2015.06.007
doi: 10.1016/j.bbagrm.2015.06.007
pubmed: 26093238
Škerlová J, Fábry M, Hubálek M et al (2014) Structure of the effector-binding domain of deoxyribonucleoside regulator DeoR from Bacillus subtilis. Febs J 281(18):4280–4292. https://doi.org/10.1111/febs.12856
doi: 10.1111/febs.12856
pubmed: 24863636
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38(7):3022–3027. https://doi.org/10.1093/molbev/msab120
doi: 10.1093/molbev/msab120
pubmed: 33892491
pmcid: 8233496
Thompson JD, Gibson TJ, Higgins DG (2003) Multiple sequence alignment using ClustalW and ClustalX. Curr Protocols Bioinf 1:231–2322
Tu B, Mao Y, Wang R et al (2023) An alternative sigma factor σ
doi: 10.1002/jobm.202200485
pubmed: 36453540
Turner SE, Pang YY, O’Malley MR et al (2020) A DeoR-type transcription regulator is required for sugar-induced expression of type III secretion-encoding genes in Pseudomonas syringae pv. Tomato DC3000. Mol Plant Microbe Interact 33(3):509–518. https://doi.org/10.1094/MPMI-10-19-0290-R
doi: 10.1094/MPMI-10-19-0290-R
pubmed: 31829102
Ulanova D, Kitani S, Fukusaki E et al (2013) SdrA, a new DeoR family regulator involved in Streptomyces avermitilis morphological development and antibiotic production. Appl Environ Microbiol 79(24):7916–7921. https://doi.org/10.1128/AEM.02843-13
doi: 10.1128/AEM.02843-13
pubmed: 24123736
pmcid: 3837817
Valentin-Hansen P, Hammer-Jespersen K, Boetius F et al (1984) Structure and function of the intercistronic regulatory deoc-deoa element of Escherichia coli K-12. EMBO J 3(1):179–183. https://doi.org/10.1002/j.1460-2075.1984.tb01781.x
doi: 10.1002/j.1460-2075.1984.tb01781.x
pubmed: 6323164
pmcid: 557317
Wang F, Ren NN, Luo S et al (2014) DptR2, a DeoR-type auto-regulator, is required for daptomycin production in Streptomyces roseosporus. Gene 544(2):208–215. https://doi.org/10.1016/j.gene.2014.04.044
doi: 10.1016/j.gene.2014.04.044
pubmed: 24768321
Wang R, Kong F, Wu H et al (2020) Complete genome sequence of high-yield strain S. lincolnensis B48 and identification of crucial mutations contributing to lincomycin overproduction. Synth Syst Biotechnol 5(2):37–48. https://doi.org/10.1016/j.synbio.2020.03.001
doi: 10.1016/j.synbio.2020.03.001
pubmed: 32322696
pmcid: 7160387
Wang R, Cao Y, Kong F et al (2022) Developmental regulator RamR
doi: 10.1111/jam.15568
pubmed: 35384192
Wang R, Zhou T, Kong F et al (2023) AflQ1-Q2 represses lincomycin biosynthesis via multiple cascades in Streptomyces lincolnensis. Appl Microbiol Biotechnol 107(9):2933–2945. https://doi.org/10.1007/s00253-023-12429-z
doi: 10.1007/s00253-023-12429-z
pubmed: 36930277
Xu Y, Ke M, Li J et al (2019) TetR-type regulator SLCG_2919 is a negative regulator of lincomycin biosynthesis in Streptomyces lincolnensis. Appl Environ Microbiol 85(1):e02091–e02018. https://doi.org/10.1128/aem.02091-18
doi: 10.1128/aem.02091-18
pubmed: 30341075
Xu Y, Tang Y, Wang N et al (2020) Transcriptional regulation of a leucine-responsive regulatory protein for directly controlling lincomycin biosynthesis in Streptomyces lincolnensis. Appl Microbiol Biotechnol 104:2575–2587. https://doi.org/10.1007/s00253-020-10381-w
doi: 10.1007/s00253-020-10381-w
pubmed: 31993701
Zou Z, Du D, Zhang Y et al (2014) A γ-butyrolactone-sensing activator/repressor, JadR3, controls a regulatory mini-network for jadomycin biosynthesis. Mol Microbiol 94(3):490–505. https://doi.org/10.1111/mmi.12752
doi: 10.1111/mmi.12752
pubmed: 25116816