Insights into the Genome of a New Strain Serratia rubidaea XU1 Isolated from Radioactive Soil and its Prodigiosin Production and Antimicrobial Properties.


Journal

Current microbiology
ISSN: 1432-0991
Titre abrégé: Curr Microbiol
Pays: United States
ID NLM: 7808448

Informations de publication

Date de publication:
30 Oct 2024
Historique:
received: 31 03 2024
accepted: 18 10 2024
medline: 31 10 2024
pubmed: 30 10 2024
entrez: 30 10 2024
Statut: epublish

Résumé

The genus Serratia is a typical red bacterium involved in prodigiosin synthesis. Here, we report the genome sequence of Serratia rubidaea XU1, which was isolated from radiation-contaminated soil in Xinjiang, China. The genome of XU1 is composed of 4,972,898 base pairs with a GC content of 59.25%. The genome sequence contains 4707 genes and encodes 4573 proteins, 79 tRNAs, and 17 rRNAs. The prodigiosin biosynthesis gene cluster was identified and analyzed, showing a sequence similarity of 85.55-96.02% with Serratia rubidaea. After optimizing the biosynthesis process, XU1 was able to achieve a maximum titer of 574 units/cell of prodigiosin at a pH of 7.5 and a temperature of 25 °C for 36 h. Glycerol at 20 g/L and beef extract at 5 g/L were used as the carbon and nitrogen sources, respectively. Prodigiosin extracted from XU1 demonstrated inhibition of Escherichia coli, Staphylococcus aureus, Enterococcus faecalis and Pseudomonas aeruginosa. The availability of the sequenced genome of XU1 will be greatly beneficial and contribute to complementary studies on the biosynthetic mechanisms of prodigiosin.

Identifiants

pubmed: 39475970
doi: 10.1007/s00284-024-03958-5
pii: 10.1007/s00284-024-03958-5
doi:

Substances chimiques

Prodigiosin OL369FU7CJ
Anti-Bacterial Agents 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

434

Subventions

Organisme : National Natural Science Foundation of China
ID : 21978136
Organisme : National Natural Science Foundation of China
ID : 32060004
Organisme : Natural Science Foundation of Jiangsu Province
ID : BK20211268
Organisme : Outstanding Youth Fund" of Xinjiang Natural Science Foundation
ID : 2022D01E19

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Chiaverini A, Di Domenico M, Del Matto I, Rossi F, Centorotola G, Cornacchia A, Cornacchione N, Petrone D, Iannitto G, Marino L, Camma C, Pomilio F (2021) Draft genome sequence of Serratia rubidaea, a potential opportunistic pathogen isolated from food in Italy. Microbiol Resour Ann 10(30):2. https://doi.org/10.1128/mra.00707-21
doi: 10.1128/mra.00707-21
Karkey A, Joshi N, Chalise S, Joshi S, Shrestha S, Nguyen TNT, Dongol S, Basnyat B, Baker S, Boinett CJ (2018) Outbreaks of Serratia marcescens and Serratia rubidaea bacteremia in a central Kathmandu hospital following the 2015 earthquakes. Trans Roy Soc Trop Med Hyg 112(10):467–472. https://doi.org/10.1093/trstmh/try077
doi: 10.1093/trstmh/try077 pubmed: 30107587
Cook MA, Lopez JJ (2023) Serratia odorifera biogroup I: an emerging pathogen. J Osteopath Med 98(9):505–507. https://doi.org/10.1515/jom-1998-0092
doi: 10.1515/jom-1998-0092
Coggins SA, Edwards EM, Flannery DD, Gerber JS, Horbar JD, Puopolo KM (2023) Serratia infection epidemiology among very preterm infants in the neonatal intensive care Unit. Pediatr Infect Dis J 42(2):152–158. https://doi.org/10.1097/inf.0000000000003736
doi: 10.1097/inf.0000000000003736 pubmed: 36638403
Hu XC, Cheng T, Liu JH (2018) A novel Serratia sp ZS6 isolate derived from petroleum sludge secretes biosurfactant and lipase in medium with olive oil as sole carbon source. AMB Express 8:12. https://doi.org/10.1186/s13568-018-0698-9
doi: 10.1186/s13568-018-0698-9
Clements T, Ndlovu T, Khan W (2019) Broad-spectrum antimicrobial activity of secondary metabolites produced by Serratia marcescens strains. Microbiol Res 229:10. https://doi.org/10.1016/j.micres.2019.126329
doi: 10.1016/j.micres.2019.126329
Granada SD, Ramirez-Restrepo S, Lopez-Lujan L, Pelaez-Jaramillo CA, Bedoya-Perez JC (2018) Screening of a biological control bacterium to fight avocado diseases: from agroecosystem to bioreactor. Biocatal Agric Biotechnol 14:109–115. https://doi.org/10.1016/j.bcab.2018.02.005
doi: 10.1016/j.bcab.2018.02.005
Fulazzaky MA, Abdullah S, Muda K, Martin AY, Fulazzaky M (2022) New kinetic models for predicting the removal of oil and grease from food-processing industry wastewater. Chem Eng Res Des 188:1067–1076. https://doi.org/10.1016/j.cherd.2022.10.047
doi: 10.1016/j.cherd.2022.10.047
Eckelmann D, Spiteller M, Kusari S (2018) Spatial-temporal profiling of prodiginines and serratamolides produced by endophytic Serratia marcescens harbored in Maytenus serrata. Sci Rep 8:15. https://doi.org/10.1038/s41598-018-23538-5
doi: 10.1038/s41598-018-23538-5
Clements T, Ndlovu T, Khan S, Khan W (2019) Biosurfactants produced by Serratia species: classification, biosynthesis, production and application. Appl Microbiol Biotechnol 103(2):589–602. https://doi.org/10.1007/s00253-018-9520-5
doi: 10.1007/s00253-018-9520-5 pubmed: 30456577
Williams DJ, Grimont PAD, Cazares A, Grimont F, Ageron E, Pettigrew KA, Cazares D, Njamkepo E, Weill FX, Heinz E, Holden MTG, Thomson NR, Coulthurst SJ (2022) The genus Serratia revisited by genomics. Nat Commun 13(1):18. https://doi.org/10.1038/s41467-022-32929-2
doi: 10.1038/s41467-022-32929-2
Xing S, Ma T, Zhang X, Huang Y, Mi Z, Sun Q, An X, Fan H, Wu S, Wei L (2017) First complete genome sequence of a virulent bacteriophage infecting the opportunistic pathogen Serratia rubidaea. Arch Virol 162:2021–2028. https://doi.org/10.1007/s00705-017-3300-x
doi: 10.1007/s00705-017-3300-x pubmed: 28265773
Gentille D, Perez M, Centelles MJ (2014) Bacteremia by a Serratia rubidaea with an atypical quinolones resistance phenotype, probably related to a intravascular catheter, in a healthy teenager. Rev Chil Infectol 31(3):351–352. https://doi.org/10.4067/s0716-10182014000300017
doi: 10.4067/s0716-10182014000300017
Thomson NR, Crow MA, McGowan SJ, Cox A, Salmond GPC (2000) Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol 36(3):539–556. https://doi.org/10.1046/j.1365-2958.2000.01872.x
doi: 10.1046/j.1365-2958.2000.01872.x pubmed: 10844645
Kim D, Kim JF, Yim JH, Kwon SK, Lee CH, Lee HK (2008) Red to red—the marine bacterium Hahella chejuensis and its product prodigiosin for mitigation of harmful algal blooms. J Microbiol Biotechnol 18(10):1621–1629. https://doi.org/10.4014/jmb.2008.18.10.1621
doi: 10.4014/jmb.2008.18.10.1621 pubmed: 18955809
Staric N, Danevcic T, Stopar D (2010) Vibrio sp. DSM 14379 pigment production-a competitive advantage in the environment? Microb Ecol 60(3):592–598. https://doi.org/10.1007/s00248-010-9671-0
doi: 10.1007/s00248-010-9671-0 pubmed: 20405118
Kawasaki T, Sakurai F, Hayakawa Y (2008) A prodigiosin from the roseophilin producer Streptomyces griseoviridis. J Nat Prod 71(7):1265–1267. https://doi.org/10.1021/np7007494
doi: 10.1021/np7007494 pubmed: 18553921
Sakai-Kawada FE, Ip CG, Hagiwara KA, Awaya JD (2019) Biosynthesis and bioactivity of prodiginine analogs in marine bacteria, Pseudoalteromonas: a mini review. Front Microbiol 10:9. https://doi.org/10.3389/fmicb.2019.01715
doi: 10.3389/fmicb.2019.01715
Gupta V, Sharma S, Pal K, Goyal P, Agarwal D, Chander J (2021) Serratia, no longer an uncommon opportunistic pathogen—case series & review of literature. Infect Disord Drug Targets 21(7):e300821191666. https://doi.org/10.2174/1871526521666210222125215
doi: 10.2174/1871526521666210222125215 pubmed: 33618650
Yip CH, Yarkoni O, Ajioka J, Wan KL, Nathan S (2019) Recent advancements in high-level synthesis of the promising clinical drug, prodigiosin. Appl Microbiol Biotechnol 103(4):1667–1680. https://doi.org/10.1007/s00253-018-09611-z
doi: 10.1007/s00253-018-09611-z pubmed: 30637495
Nguyen SLT, Nguyen TC, Do TT, Vu TL, Nguyen TT, Do TT, Nguyen THT, Le TH, Trinh DK, Nguyen TAT (2022) Study on the anticancer activity of prodigiosin from variants of Serratia Marcescens QBN VTCC 910026. Biomed Res Int 2022:11. https://doi.org/10.1155/2022/4053074
doi: 10.1155/2022/4053074
Yip CH, Mahalingam S, Wan KL, Nathan S (2021) Prodigiosin inhibits bacterial growth and virulence factors as a potential physiological response to interspecies competition. PLoS ONE 16(6):24. https://doi.org/10.1371/journal.pone.0253445
doi: 10.1371/journal.pone.0253445
Gajadhar S, Mellem JJ (2019) Isolation and characterization of a microbial pigment obtained from Serratia Marcescens as a natural food colourant. Ann Univ Dunarea Jos Galati, F VI-Food Technol 43(1):137–154. https://doi.org/10.35219/foodtechnology.2019.1.11
doi: 10.35219/foodtechnology.2019.1.11
Jia XB, Liu FC, Zhao K, Lin JJ, Fang Y, Cai SP, Lin CQ, Zhang H, Chen LJ, Chen JC (2021) Identification of essential genes associated with prodigiosin production in Serratia marcescens FZSF02. Front Microbiol 12:11. https://doi.org/10.3389/fmicb.2021.705853
doi: 10.3389/fmicb.2021.705853
Williamson NR, Fineran PC, Leeper FJ, Salmond GPC (2006) The biosynthesis and regulation of bacterial prodiginines. Nat Rev Microbiol 4(12):887–899. https://doi.org/10.1038/nrmicro1531
doi: 10.1038/nrmicro1531 pubmed: 17109029
Williamson NR, Simonsen HT, Ahmed RAA, Goldet G, Slater H, Woodley L, Leeper FJ, Salmond GPC (2005) Biosynthesis of the red antibiotic, prodigiosin, in Serratia: identification of a novel 2-methyl-3-n-amyl-pyrrole (MAP) assembly pathway, definition of the terminal condensing enzyme, and implications for undecylprodigiosin biosynthesis in Streptomyces. Mol Microbiol 56(4):971–989. https://doi.org/10.1111/j.1365-2958.2005.04602.x
doi: 10.1111/j.1365-2958.2005.04602.x pubmed: 15853884
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170
doi: 10.1093/bioinformatics/btu170 pubmed: 24695404
Luo RB, Liu BH, Xie YL, Li ZY, Huang WH, Yuan JY, He GZ, Chen YX, Pan Q, Liu YJ, Tang JB, Wu GX, Zhang H, Shi YJ, Liu Y, Yu C, Wang B, Lu Y, Han CL, Cheung DW, Yiu SM, Peng SL, Zhu XQ, Liu GM, Liao XK, Li YR, Yang HM, Wang J, Lam TW, Wang J (2015) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience. https://doi.org/10.1186/s13742-015-0069-2
doi: 10.1186/s13742-015-0069-2 pubmed: 26161257
Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23(6):673–679. https://doi.org/10.1093/bioinformatics/btm009
doi: 10.1093/bioinformatics/btm009 pubmed: 17237039
Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30. https://doi.org/10.1093/nar/28.1.27
doi: 10.1093/nar/28.1.27 pubmed: 10592173 pmcid: 102409
Muller J, Szklarczyk D, Julien P, Letunic I, Roth A, Kuhn M, Powell S, von Mering C, Doerks T, Jensen LJ, Bork P (2010) eggNOG v2.0: extending the evolutionary genealogy of genes with enhanced non-supervised orthologous groups, species and functional annotations. Nucleic Acids Res 38:D190–D195. https://doi.org/10.1093/nar/gkp951
doi: 10.1093/nar/gkp951 pubmed: 19900971
Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Muller R, Wohlleben W, Breitling R, Takano E, Medema MH (2015) antiSMASH 3.0-a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43(1):W237–W243. https://doi.org/10.1093/nar/gkv437
doi: 10.1093/nar/gkv437 pubmed: 25948579
Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M (2022) TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 50(D1):D801–D807. https://doi.org/10.1093/nar/gkab902
doi: 10.1093/nar/gkab902 pubmed: 34634793
Sproer C, Mendrock U, Swiderski J, Lang E, Stackebrandt E (1999) The phylogenetic position of Serratia, Buttiauxella and some other genera of the family Enterobacteriaceae. Int J Syst Bacteriol 49(Pt 4):1433–1438. https://doi.org/10.1099/00207713-49-4-1433
doi: 10.1099/00207713-49-4-1433 pubmed: 10555323
Kim M, Oh HS, Park SC, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351. https://doi.org/10.1099/ijs.0.059774-0
doi: 10.1099/ijs.0.059774-0 pubmed: 24505072
Metwally RA, El Sikaily A, El-Sersy NA, Ghozlan HA, Sabry SA (2021) Antimicrobial activity of textile fabrics dyed with prodigiosin pigment extracted from marine Serratia rubidaea RAM_Alex bacteria. Egypt J Aquatic Res 47(3):301–305. https://doi.org/10.1016/j.ejar.2021.05.004
doi: 10.1016/j.ejar.2021.05.004
Siva R, Subha K, Bhakta D, Ghosh AR, Babu S (2012) Characterization and enhanced production of prodigiosin from the spoiled coconut. Appl Biochem Biotechnol 166(1):187–196. https://doi.org/10.1007/s12010-011-9415-8
doi: 10.1007/s12010-011-9415-8 pubmed: 22072139
Elkenawy NM, Yassin AS, Elhifnawy HN, Amin MA (2017) Optimization of prodigiosin production by Serratia marcescens using crude glycerol and enhancing production using gamma radiation. Biotechnol Rep 14:47–53. https://doi.org/10.1016/j.btre.2017.04.001
doi: 10.1016/j.btre.2017.04.001
Romanowski EG, Lehner CM, Martin NC, Patel KR, Callaghan JD, Stella NA, Shanks RMQ (2019) Thermoregulation of prodigiosin biosynthesis by Serratia marcescens is controlled at the transcriptional level and requires HexS. Pol J Microbiol 68(1):43–50. https://doi.org/10.21307/pjm-2019-005
doi: 10.21307/pjm-2019-005 pubmed: 31050252
Wang SL, Wang CY, Yen YH, Liang TW, Chen SY, Chen CH (2012) Enhanced production of insecticidal prodigiosin from Serratia marcescens TKU011 in media containing squid pen. Process Biochem 47(11):1684–1690. https://doi.org/10.1016/j.procbio.2011.07.010
doi: 10.1016/j.procbio.2011.07.010
Fender JE, Bender CM, Stella NA, Lahr RM, Kalivoda EJ, Shanks RMQ (2012) Serratia marcescens quinoprotein glucose dehydrogenase activity mediates medium acidification and inhibition of prodigiosin production by glucose. Appl Environ Microbiol 78(17):6225–6235. https://doi.org/10.1128/aem.01778-12
doi: 10.1128/aem.01778-12 pubmed: 22752173
Paul T, Bandyopadhyay TK, Mondal A, Tiwari ON, Muthuraj M, Bhunia B (2022) A comprehensive review on recent trends in production, purification, and applications of prodigiosin. Biomass Convers Bior 12(4):1409–1431. https://doi.org/10.1007/s13399-020-00928-2
doi: 10.1007/s13399-020-00928-2
Darshan N, Manonmani HK (2016) Prodigiosin inhibits motility and activates bacterial cell death revealing molecular biomarkers of programmed cell death. AMB Express 6:12. https://doi.org/10.1186/s13568-016-0222-z
doi: 10.1186/s13568-016-0222-z
Balasubramaniam B, Alexpandi R, Darjily DR (2019) Exploration of the optimized parameters for bioactive prodigiosin mass production and its biomedical applications in vitro as well as in silico. Biocatal Agric Biotechnol 22:12. https://doi.org/10.1016/j.bcab.2019.101385
doi: 10.1016/j.bcab.2019.101385
Han R, Xiang R, Li J, Wang F, Wang C (2021) High-level production of microbial prodigiosin: a review. J Basic Microbiol 61(6):506–523. https://doi.org/10.1002/jobm.202100101
doi: 10.1002/jobm.202100101 pubmed: 33955034
Zhang B, Zhang L, Dai RX, Yu MY, Zhao GP, Ding XM (2013) An efficient procedure for marker-free mutagenesis of S. coelicolor by site-specific recombination for secondary metabolite overproduction. PLoS ONE 8(2):8. https://doi.org/10.1371/journal.pone.0055906
doi: 10.1371/journal.pone.0055906
Kwon SK, Park YK, Kim JF (2010) Genome-wide screening and identification of factors affecting the biosynthesis of prodigiosin by Hahella chejuensis, using Escherichia coli as a surrogate host. Appl Environ Microbiol 76(5):1661–1668. https://doi.org/10.1128/aem.01468-09
doi: 10.1128/aem.01468-09 pubmed: 20038694

Auteurs

Mengjuan Sun (M)

School of Food Science and Pharmaceutical Engineering, Nanjing Normal University, Nanjing, 210046, Jiangsu, China.

Xueting Lu (X)

School of Food Science and Pharmaceutical Engineering, Nanjing Normal University, Nanjing, 210046, Jiangsu, China.

Bowen Fu (B)

School of Food Science and Pharmaceutical Engineering, Nanjing Normal University, Nanjing, 210046, Jiangsu, China.

Guocui Zhu (G)

School of Food Science and Pharmaceutical Engineering, Nanjing Normal University, Nanjing, 210046, Jiangsu, China.

Lele Ma (L)

School of Food Science and Pharmaceutical Engineering, Nanjing Normal University, Nanjing, 210046, Jiangsu, China.

Chengjia Xie (C)

School of Chemical Engineering, Yangzhou Polytechnic Institute, Yangzhou, 225127, Jiangsu, China.

Zhidong Zhang (Z)

Institute of Microbiology, Xinjiang Academy of Agricultural Sciences, Urumqi, 830091, Xinjiang Uyghur Autonomous Region, People's Republic of China.

Xian Xu (X)

School of Food Science and Pharmaceutical Engineering, Nanjing Normal University, Nanjing, 210046, Jiangsu, China. xuxian@njnu.edu.cn.

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