Whole genome sequencing of a siderophore-producing bacterium isolated from Simadu pineapple roots
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Abstract
Abstract. Wijayanti C, Suryadarma P, Mubarik NR. 2024. Whole genome sequencing of a siderophore-producing bacterium isolated from Simadu pineapple roots. Biodiversitas 25: 4860-4869. Siderophores are organic compounds synthesized by bacteria that act as iron-chelating ligands, facilitating the solubilization and transport of iron into the cell. Siderophore-producing bacteria offer significant benefits across various fields of research and application. A recent study investigated a siderophore-producing bacterium, the M7 isolate, from Simadu pineapple roots in the Subang District of West Java, Indonesia. This study aimed to analyze the siderophore biosynthesis gene cluster (BGC) from the complete genome sequence of the M7 isolate through genome mining. Comparative genomic analysis with the strain Providencia manganoxydans LLDRA6 revealed that the M7 isolate has a similar guanine-cytosine (GC) content with a longer sequence length totaling 4,447,159 bp. Genome comparison using average nucleotide identity (ANI) calculations indicated that the M7 isolate had a genome similarity of 98.82% with strain P. manganoxydans LLDRA6. Additionally, the genome of the M7 isolate contains systems for iron acquisition and metabolism, which involve mechanisms for regulating iron. A specific region in the M7 isolate encodes the IucA/IucC family of siderophore biosynthesis proteins responsible for aerobactin biosynthesis through non-ribosomal peptide synthetase-independent siderophore (NIS) pathways. Regarding siderophore BGCs, this isolate showed the highest similarity to Providencia stuartii, with differences in genetic redundancy content. Additionally, pathogen prediction results for the M7 isolate indicate that it is not pathogenic to humans, unlike P. stuartii, which is known to be pathogenic. The new siderophore-producing bacterium, the M7 isolate, harbors a duplication of core biosynthesis genes, representing genetic redundancy that supports siderophore biosynthesis. This genetic feature may enable concurrent protein expression, potentially enhancing siderophore accumulation.
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References
Abdallah M, Balshi A. 2018. First literature review of carbapenem-resistant Providencia. New Microb New Infect 25: 16-23. DOI: 10.1016/j.nmni.2018.05.009.
Ameer AKA, Al-Gburi NM. 2022. Study the pathogenicity of Providencia vermicola in mice. Intl J Health Sci 6: 6895-6906. DOI: 10.53730/ijhs.v6nS4.10020.
Baars O, Zhang X, Morel FMM, Seyedsayamdost MR. 2016. The Siderophore metabolome of Azotobacter vinelandii. Appl Environ Microbiol 82 (1): 27-39. DOI: 10.1128/AEM.03160-15.
Bajbouj K, Shafarin J, Hamad M. 2018. High-dose deferoxamine treatment disrupts intracellular iron homeostasis, reduces growth, and induces apoptosis in metastatic and nonmetastatic breast cancer cell lines. Technol Cancer Res Treat 17: 1533033818764470. DOI: 10.1177/1533033818764470.
Blin K, Shaw S, Augustijn HE, Reitz ZL, Biermann F, Alanjary M, Fetter A, Terlouw BR, Metcalf WW, Helfrich EJN, van Wezel GP, Medema MH, Weber T. 2023. antiSMASH 7.0: New and improved predictions for detection, regulation, chemical structures, and visualization. Nucleic Acids Res 51 (W1): W46-W50. DOI: 10.1093/nar/gkad344.
Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP, Medema MH, Weber T. 2021. antiSMASH 6.0: Improving cluster detection and comparison capabilities. Nucl Acids Res 49 (W1): W29-W35. DOI: 10.1093/nar/gkab335.
Bosshard PP, Abels S, Zbinden R, Böttger EC, Altwegg M. 2003. Ribosomal DNA sequencing for identification of aerobic Gram-positive rods in the clinical laboratory (an 18-Month Evaluation). J Clin Microbiol 41 (9): 4134-4140. DOI: 10.1128/JCM.41.9.4134-4140.2003.
Bradley JM, Svistunenko DA, Wilson MT, Hemmings AM, Moore GR, Le Brun NE. 2020. Bacterial iron detoxification at the molecular level. J Biol Chem 295: 17602-17623. DOI: 10.1074/jbc.REV120.007746.
Bruns H, Crüsemann M, Letzel A-C, Alanjary M, McInerney JO, Jensen PR, Schulz S, Moore BS, Ziemert N. 2018. Function-related replacement of bacterial siderophore pathways. Intl Soc Microb Ecol 12 (2): 320-329. DOI: 10.1038/ismej.2017.137.
Cavas L, Kirkiz I. 2022. Characterization of siderophores from Escherichia coli strains through genome mining tools: An antiSMASH study. Appl Microbiol Biotechnol Expr 12 (1): 74-87. DOI: 10.1186/s13568-022-01421-x.
Chandrangsu P, Rensing C, Helmann JD. 2017. Metal homeostasis and resistance in bacteria. Nat Rev Microbiol 15 (6): 338-350. DOI: 10.1038/nrmicro.2017.15.
Cosentino S, Voldby Larsen M, Møller Aarestrup F, Lund O. 2013. PathogenFinder-distinguishing friend from foe using bacterial whole genome sequence data. PLoS One 8 (10): e77302. DOI: 10.1371/journal.pone.0077302.
Crits-Christoph A, Bhattacharya N, Olm M, Song Y, Banfield J. 2020. Transporter genes in biosynthetic gene clusters predict metabolite characteristics and siderophore activity. Genome Res 31 (2): 239-250. DOI: 10.1101%2Fgr.268169.120.
Cui Y, Cui Z, Xu J, Hao D, Shi J, Wang D, Xiao H, Duan X, Chen R, Li W. 2020. NG-Circos: Next-generation Circos for data visualization and interpretation. NAR Genom Bioinform 2 (3): lqaa069. DOI: 10.1093/nargab/lqaa069.
De Coster W, D'Hert S, Schultz DT, Cruts M, Van Broeckhoven C. 2018. NanoPack: Visualizing and processing long-read sequencing data. Bioinformatics 34: 2666-2669. DOI: 10.1093/bioinformatics/bty149.
de Lorenzo V, Neilands JB. 1986. Characterization of iucA and iucC genes of the aerobactin system of plasmid ColV-K30 in Escherichia coli. J Bacteriol 167: 350-355. DOI: 10.1128/jb.167.1.350-355.1986.
Dong X, Jia H, Yu Y, Xiang Y, Zhang Y. 2024. Genomic revisitation and reclassification of the genus Providencia. mSphere 9 (3): e00731-23. DOI: 10.1128/msphere.00731-23.
Drechsel H, Jung G, Winkelmann G. 1993. Alpha-keto acids are novel siderophores in the genera Proteus, Providencia, and Morganella and are produced by amino acid deaminases. J Bacteriol 175 (9): 2727-2733. DOI: 10.1128/jb.175.9.2727-2733.1993.
Du Y, Li X, Liu Y, Mu S, Shen D, Fan S, Lou Z, Zhang S, Xia H, Yuan Y, Wang S. 2022. The species identification and genomic analysis of Haemobacillus shengwangii: A novel pathogenic bacterium isolated from a critically ill patient with bloodstream infection. Front Microbiol 13: 919169. DOI: 10.3389/fmicb.2022.919169.
Fuadi H, Suryadarma P, Syamsu K, Surono S, Setiyani NA, Ridhoha SM, Zahra AS, Stepani N, Ramadhan MR. 2022. Isolation and selection of siderophore-producing bacteria from roots of Simadu pineapple (Ananas comosus) in Subang District, West Java. Menara Perkebunan 90 (2): 160-167. DOI: 10.22302/iribb.jur.mpv90i2.502.
Gu S, Shao Y, Rehm K, Bigler L, Zhang D, He R, Xu R, Shao J, Jousset A, Friman VP, Bian X, Wei Z, Kümmerli L, Li Z. 2024. Feature sequence-based genome mining uncovers the hidden diversity of bacterial siderophore pathways. eLife 13: RP96719. DOI: 10.7554/eLife.96719.3.
Guidone GHM, Cardozo JG, Silva LC, Sanches MS, Galhardi LCF, Kobayashi RKT, Vespero EC, Rocha SPD. 2023. Epidemiology and characterization of Providencia stuartii isolated from hospitalized patients in southern Brazil: A possible emerging pathogen. MicroSoc 55 (10): 000652-v4. DOI: 10.1099/acmi.0.000652.v2.
Gurevich A, Saveliev V, Vyahhi N, Tesler G. 2013. QUAST: Quality assessment tool for genome assemblies. Bioinformatics 29 (8): 1072-1075. DOI: 10.1093/bioinformatics/btt086.
Ho Y-H, Ho S-Y, Hsu C-C, Shie J-J, Wang T-SA. 2017. Utilizing an iron(III)-chelation masking strategy to prepare mono- and bis-functionalized aerobactin analogues for targeting pathogenic bacteria. Chem Commun 53 (66): 9265-9268. DOI: 10.1039/C7CC05197B.
Hussain K, Hameed S, Shahid M, Ali A, Iqbal J, Hahn D. 2015. First report of Providencia vermicola strains characterized for enhanced rapeseed growth attributing parameters. Intl J Agric Biol 17 (6): 1110-1116. DOI: 10.17957/IJAB/15.0033.
Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, Aarestrup FM. 2014. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol 52 (5): 1501-1510. DOI: 10.1128/JCM.03617-13.
Klein JA, Predeus AV, Greissl AR, Clark-Herrera MM, Cruz E, Cundiff JA, Haeberle AL, Howell M, Lele A, Robinson DJ, Westerman TL, Wrande M, Wright SJ, Green NM, Vallance BA, McClelland M, Mejia A, Goodman AG, Elfenbein JR, Knodler LA. 2024. Pathogenic diversification of the gut commensal Providencia alcalifaciens via acquisition of a second type III secretion system. Infect Immun 92 (10): e00314-24. DOI: 10.1128/iai.00314-24.
Kolmogorov M, Bickhart DM, Behsaz B, Gurevich A, Rayko M, Shin SB, Kuhn K, Yuan J, Polevikov E, Smith TPL, Pevzner PA. 2020. metaFlye: scalable long-read metagenome assembly using repeat graphs. Nat Methods 17 (11): 1103-1110. DOI: 10.1038/s41592-020-00971-x.
Lee I, Ouk Kim Y, Park S-C, Chun J. 2016. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Intl J Syst Evol Microbiol 66: 1100-1103. DOI: 10.1099/ijsem.0.000760.
Li C, Zhu L, Pan D, Li S, Xiao H, Zhang Z, Shen X, Wang Y, Long M. 2019. Siderophore-mediated iron acquisition enhances resistance to oxidative and aromatic compound stress in Cupriavidus necator JMP134. Appl Environ Microbiol 85 (1): e01938-18. DOI: 10.1128/AEM.0193818.
Li D, Li R, Ding Z, Ruan X, Luo J, Chen J, Zheng J, Tang J. 2020. Discovery of a novel native bacterium of Providencia sp. with high biosorption and oxidation ability of manganese for bioleaching of heavy metal contaminated soils. Chemosphere 241: 125039. DOI: 10.1016/j.chemosphere.2019.125039.
Li K, Chen W-H, Bruner SD. 2016. Microbial siderophore-based iron assimilation and therapeutic applications. Biometals 29: 377-388. DOI: 10.1007/s10534-016-9935-3.
Li Y, Ma Q. 2017. Iron acquisition strategies of Vibrio anguillarum. Front Cell Infect Microbiol 7: 342-354. DOI: 10.3389/fcimb.2017.00342.
Lupande-Mwenebitu D, Khedher MB, Khabthani S, Rym L, Phoba MF, Nabti LZ, Lunguya-Metila O, Pantel A, Lavigne JP, Rolain JM, Diene SM. 2021. First genome description of Providencia vermicola isolate bearing NDM-1 from blood culture. Microorganisms 9 (8): 1751. DOI: 10.3390/microorganisms9081751.
Lv H, Hung CS, Henderson JP. 2014. Metabolomic analysis of siderophore cheater mutants reveals metabolic costs of expression in uropathogenic Escherichia coli. J Proteome Res 13 (3): 1397-1404. DOI: 10.1021/pr4009749.
Majewska M, S?omka A, Hanaka A. 2024. Siderophore-producing bacteria from Spitsbergen soils-novel agents assisted in bioremediation of the metal-polluted soils. Environ Sci Pollut Res 31: 32371-32381. DOI: 10.1007/s11356-024-33356-0.
Manni M, Berkeley MR, Seppey M, Simão FA, Zdobnov EM, Joana K. 2021. BUSCO Update: Novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol 38 (10): 4647-4654. DOI: 10.1093/molbev/msab199.
Medema MH, Blin K, Cimermancic P, De Jager V, Zakrzewski P, Fischbach MA, Weber T, Takano E, Breitling R. 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. DOI: 10.1093/nar/gkr466.
Miethke M, Marahiel MA. 2007. Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71 (3): 413-451. DOI: 10.1128/MMBR.00012-07.
Nowak MA, Boerlijst MC, Cooke J, Smith JM. 1997. Evolution of genetic redundancy. Nature 388 (6638): 167-171. DOI: 10.1038/40618.
Paredes C, Chi SI, Flint A, Weedmark K, McDonald C, Bearne J, Ramirez-Arcos S, Pagotto F. 2021. Complete genome sequence of Staphylococcus aureus PS/BAC/169/17/W, isolated from a contaminated platelet concentrate in england. Microbiol Resour Announc 10 (45): e00841-21. DOI: 10.1128/MRA.00841-21.
Peng J. 2019. Gene redundancy and gene compensation: An updated view. J Genet Genom 46 (7): 329-333. DOI: 10.1016/j.jgg.2019.07.001.
Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P. 2016. Microbial siderophores and their potential applications: A review. Environ Sci Pollut Res 23: 3984-3999. DOI: 10.1007/s11356-015-4294-0.
Sasirekha B, Srividya S. 2016. Siderophore production by Pseudomonas aeruginosa FP6, a biocontrol strain for Rhizoctonia solani and Colletotrichum gloeosporioides causing diseases in chili. Agric Nat Resour 50 (4): 250-256. DOI: 10.1016/j.anres.2016.02.003.
Sayyed RZ, Chincholkar SB. 2010. Growth and siderophores production in Alcaligenes faecalis is regulated by metal ions. Indian J Microbiol 50: 179-182. DOI: 10.1007/s12088-010-0021-1.
Segond D, Abi Khalil E, Buisson C, Daou N, Kallassy M, Lereclus D, Arosio P, Bou-Abdallah F, Nielsen Le Roux C. 2014. Iron acquisition in Bacillus cereus: The roles of IlsA and bacillibactin in exogenous ferritin iron mobilization. PLoS Pathog 10 (2): e1003935. DOI: 10.1371/journal.ppat.1003935.
Seppey M, Manni M, Zdobnov EM. 2019. BUSCO: Assessing genome assembly and annotation completeness. Gene Prediction 1962: 227-25. DOI: 10.1007/978-1-4939-9173-0_14.
Seyoum Y, Baye K, Humblot C. 2021. Iron homeostasis in host and gut bacteria - a complex interrelationship. Gut Microbes 13 (1): 1874855. DOI: 10.1080/19490976.2021.1874855.
Simao FA, Waterhouse RM, Ionnidis P, Kriventseva EV, Zdobnov EM, 2015. BUSCO: Assessing genome assembly and annotation completeness with single copy orthologs. Bioinformatics 31 (19): 3210-3212. DOI: 10.1093/bioinformatics/btv351.
Srivastava P, Sahgal M, Sharma K, Enshasy HAE, Gafur A, Alfarraj S, Ansari MJ, Sayyed RZ. 2022. Optimization and identification of siderophores produced by Pseudomonas monteilii strain MN759447 and its antagonism toward fungi associated with mortality in Dalbergia sissoo plantation forests. Front Plant Sci 13: 984522. DOI: 10.3389/fpls.2022.984522.
Swayambhu G, Bruno M, Gulick AM, Pfeifer BA. 2021. Siderophore natural products as pharmaceutical agents. Curr Opin Biotechnol 69: 242-251. DOI: 10.1016/j.copbio.2021.01.021.
Tamang P, Upadhaya A, Paudel P, Meepagala K, Cantrell CL. 2024. Mining biosynthetic gene clusters of Pseudomonas vancouverensis utilizing whole genome sequencing. Microorganisms 12 (3): 548-565. DOI: 10.3390/microorganisms12030548.
Telfer TJ, Liddell JR, Duncan C, White AR, Codd R. 2017. Adamantyl- and other polycyclic cage-based conjugates of desferrioxamine B (DFOB) for treating iron-mediated toxicity in cell models of parkinson's disease. Bioorg Med Chem Lett 27 (8): 1698-1704. DOI: 10.1016/j.bmcl.2017.03.001.
Vaser R, Sovi? I, Nagarajan N, Šiki? M. 2017. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res 27 (5): 737-746. DOI: 10.1101/gr.214270.116.
Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Müller 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 (W1): W237-W243. DOI: 10.1093/nar/gkv437.
Wilson BR, Bogdan AR, Miyazawa M, Hashimoto K, Tsuji Y. 2016. Siderophores in iron metabolism: From mechanism to therapy potential. Trends Mol Med 22: 1077-1090. DOI: 10.1016/j.molmed.2016.10.005.
Yu S, Teng C, Bai X, Liang J, Song T, Dong L, Jin Y, Qu J. 2017. Optimization of siderophore production by Bacillus sp. PZ-1 and its potential enhancement of phytoextration of pb from soil. J Microbiol Biotechnol 27 (8): 1500-1512. DOI: 10.4014/jmb.1705.05021.
Zavascki AP, Goldani LZ, Li J, Nation RL. 2007. Polymyxin B for the treatment of multidrug-resistant pathogens: A critical review. J Antimicrob Chemother 60 (6): 1206-1215. DOI: 10.1093/jac/dkm357.