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Functional characterization of the ABC transporters and transposable elements of an uncultured Paracoccus sp. recovered from a hydrocarbon-polluted soil metagenome

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Abstract

Environmental microorganisms usually exhibit a high level of genomic plasticity and metabolic versatility that allow them to be well-adapted to diverse environmental challenges. This study used shotgun metagenomics to decipher the functional and metabolic attributes of an uncultured Paracoccus recovered from a polluted soil metagenome and determine whether the detected attributes are influenced by the nature of the polluted soil. Functional and metabolic attributes of the uncultured Paracoccus were elucidated via functional annotation of the open reading frames (ORFs) of its contig. Functional tools deployed for the analysis include KEGG, KEGG KofamKOALA, Clusters of Orthologous Groups of proteins (COG), Comprehensive Antibiotic Resistance Database (CARD), and the Antibiotic Resistance Gene-ANNOTation (ARG-ANNOT V6) for antibiotic resistance genes, TnCentral for transposable element, Transporter Classification Database (TCDB) for transporter genes, and FunRich for gene enrichment analysis. Analyses revealed the preponderance of ABC transporter genes responsible for the transport of oligosaccharides (malK, msmX, msmK, lacK, smoK, aglK, togA, thuK, treV, msiK), monosaccharides (glcV, malK, rbsC, rbsA, araG, ytfR, mglA), amino acids (thiQ, ynjD, thiZ, glnQ, gluA, gltL, peb1C, artP, aotP, bgtA, artQ, artR), and several others. Also detected are transporter genes for inorganic/organic nutrients like phosphate/phosphonate, nitrate/nitrite/cyanate, sulfate/sulfonate, bicarbonate, and heavy metals such as nickel/cobalt, molybdate/tungstate, and iron, among others. Antibiotic resistance genes that mediate efflux, inactivation, and target protection were detected, while transposable elements carrying resistance phenotypes for antibiotics and heavy metals were also annotated. The findings from this study have established the resilience, adaptability, and survivability of the uncultured Paracoccus in the hydrocarbon-polluted soil.

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References

  • Abskharon RNN, Hassan SHA, Kabir MH, Qadir SA, Gad El Rab SM, Wang MH (2010) The role of antioxidants enzymes of E. coli ASU3, a tolerant strain to heavy metals toxicity, in combating oxidative stress of copper. World J Microbiol Biotechnol 26(2):241–247

  • Alfano M, Cavazza C (2020) Structure, function, and biosynthesis of nickel-dependent enzymes. Protein Sci 29(5):1071–1089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrew RWJ, Jackson JM (1996) Pollution and waste management. The natural environment and human impact. Longman Publishers, Singapore, pp 281–297

    Google Scholar 

  • Anjem A, Imlay JA (2012) Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. J Biol Chem 287(22411989):15544–15556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Antonelli A, D’Andrea MM, Brenciani A, Galeotti CL, Morroni G, Pollini S, Varaldo PE, Rossolini GM (2018) Characterization of poxtA, a novel phenicol-oxazolidinone-tetracycline resistance gene from an MRSA of clinical origin. J Antimicrob Chemother 73(7):1763–1769

    Article  CAS  PubMed  Google Scholar 

  • Antony R, Sujith PP, Fernandes SO, Verma P, Khedekar VD, Loka Bharathi PA (2011) Cobalt immobilization by manganese oxidizing bacteria from the Indian Ridge System. Curr Microbiol 62(3):840–849

    Article  CAS  PubMed  Google Scholar 

  • Aramaki T, Blanc-Mathieu R, Endo H, Ohkubo K, Kanehisa M, Goto S, Ogata H (2020) KofamKOALA: KEGG ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics 36(7):2251–2252

    Article  CAS  PubMed  Google Scholar 

  • Bader GD, Hogue CW (2003) An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhandal IS, Hauptman RM, Widholm JM (1985) Trehalose as cryoprotectant for the freeze preservation of carrot and tobacco cells. Plant Physiol 78:430–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bissonnette L, Roy PH (1992) Characterization of In0 of Pseudomonas aeruginosa plasmid pVS1, an ancestor of integrons of multi-resistance plasmids and transposons of gram-negative bacteria. J Bacteriol 174(4):1248–1257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bockwoldt JA, Zimmermann M, Tiso T, Blank LM (2020) Complete genome sequence and annotation of the Paracoccus pantotrophus type strain DSM 2944. Microbiol Resour Announc 9:1–2

    Article  Google Scholar 

  • Bonhivers M, Ghazi A, Boulanger P, Letellier L (1996) FhuA, a transporter of the Escherichia coli outer membrane, is converted into a channel upon binding of bacteriophage T5. EMBO J 15(8):1850–1856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonnin RA, Nordmann P, Carattoli A, Poirel L (2013) Comparative genomics of IncL/M-type plasmids: evolution by acquisition of resistance genes and insertion sequences. Antimicrob Agents Chemother 57(1):674–676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bougouffa S, Radovanovic A, Essack M, Bajic VB (2014) DEOP: a database on osmoprotectants and associated pathways. Database 2014

  • Cai J, Wang Y, Schwarz S et al (2015) Enterococcal isolates carrying the novel oxazolidinone resistance gene optrA from hospitals in Zhejiang, Guangdong, and Henan, China, 2010–2014. Clin Microbiol Infect 21(12):1095-e1

    Article  Google Scholar 

  • Carmel G, Coulton JW (1991) Internal deletions in the FhuA receptor of Escherichia coli K-12 define domains of ligand interactions. J Bacteriol 173(14):4394–4403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caza M, Kronstad JW (2013) Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans. Front Cell Infect Microbiol 3:80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chesneau O, Ligeret H, Hosan-Aghaie N, Morvan A, Dassa E (2005) Molecular analysis of resistance to streptogramin A compounds conferred by the Vga proteins of staphylococci. Antimicrob Agents Chemother 49(3):973–980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chouchani C, El Salabi A, Marrakchi R, Ferchichi L, Walsh TR (2012) First report of mefA and msrA/msrB multidrug efflux pumps associated with blaTEM-1 β-lactamase in Enterococcus faecalis. Int J Infect Dis 16(2):e104–e109

    Article  CAS  PubMed  Google Scholar 

  • Cui J, Davidson AL (2011) ABC solute importers in bacteria. Essays Biochem 50:85–99

    Article  CAS  PubMed  Google Scholar 

  • Cuthbertson L, Kos V, Whitfield C (2010) ABC transporters involved in export of cell surface glycoconjugates. Microbiol Mol Biol Rev 74:341–362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cuzon G, Naas T, Nordmann P (2011) Functional characterization of Tn4401, a Tn3-based transposon involved in blaKPC gene mobilization. Antimicrob Agents Chemother 55(11):5370–5373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai Z, Wu Z, Zhu W, Wu G (2022) Amino acids in microbial metabolism and function. Adv Exp Med Biol 1354:127–143

    Article  PubMed  Google Scholar 

  • Davidson AL, Dassa E, Orelle C, Chen J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Decewicz P, Dziewit L, Golec P, Kozlowska P, Bartosik D, Radlinska M (2019) Characterization of the virome of Paracoccus spp. (Alphaproteobacteria) by combined in silico and in vivo approaches. Sci Rep 9:7899

  • Deole R, Hoff WD (2020) A potassium chloride to glycine betaine osmoprotectant switch in the extreme halophile Halorhodospira halophila. Sci Rep 10:3383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elleuche S, Fodor K, von der Heyde A, Klippel B, Wilmanns M, Antranikian G (2014) Group III alcohol dehydrogenase from Pectobacterium atrosepticum: insights into enzymatic activity and organization of the metal ion-containing region. Appl Microbiol Biotechnol 98(9):4041–4051

    Article  CAS  PubMed  Google Scholar 

  • Ero R, Kumar V, Su W, Gao YG (2019) Ribosome protection by ABC-F proteins - molecular mechanism and potential drug design. Protein Sci 28(4):684–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez JE, Perreten V, Schwendener S (2021) The novel macrolide resistance genes mef(F) and msr(G) are located on a plasmid in Macrococcus canis and a transposon in Macrococcus caseolyticus. J Antimicrob Chemother 76(1):48–54

    Article  CAS  PubMed  Google Scholar 

  • Galinski EA, Herzog RM (1990) The role of trehalose as a substitute for nitrogen-containing compatible solutes (Ectothiorhodospira halochloris). Arch Microbiol 153:607–613

    Article  CAS  Google Scholar 

  • Greene NP, Kaplan E, Crow A, Koronakis V (2018) Antibiotic resistance mediated by the MacB ABC transporter family: a structural and functional perspective. Front Microbiol 9:950

    Article  PubMed  PubMed Central  Google Scholar 

  • Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, Rolain JM (2014) ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 58:212–220

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoffmann T, Bremer E (2017) Guardians in a stressful world: the Opu family of compatible solute transporters from Bacillus subtilis. Biol Chem 398:193–214

    Article  CAS  PubMed  Google Scholar 

  • Hottiger T, Boller T, Wiemken A (1989) Correlation of trehalose content and heat resistance in yeast mutants altered in the RAS/adenylate cyclase pathway: is trehalose a thermoprotectant. FEBS Lett 255:431–434

    Article  CAS  PubMed  Google Scholar 

  • Huda N, Lee EW, Chen J, Morita Y, Kuroda T, Mizushima T, Tsuchiya T (2003) Molecular cloning and characterization of an ABC multidrug efflux pump, VcaM, in non-O1 Vibrio cholerae. Antimicrob Agents Chemother 47(8):2413–2417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung YH, Shin ES, Kim O, Yoo JS, Lee KM, Yoo JI, Chung GT, Lee YS (2010) Characterization of two newly identified genes, vgaD and vatH, [corrected] conferring resistance to streptogramin A in Enterococcus faecium. Antimicrob Agents Chemother 54(11):4744–4749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalaiyezhini D, Ramachandran KB (2015) Biosynthesis of poly-3-hydroxybutyrate (PHB) from glycerol by Paracoccus denitrificans in a batch bioreactor: effect of process variables. Prep Biochem Biotechnol 45:69–83

    Article  CAS  PubMed  Google Scholar 

  • Kerr ID, Reynolds ED, Cove JH (2005) ABC proteins and antibiotic drug resistance: is it all about transport. Biochem Soc Trans 33:1000–1002

    Article  CAS  PubMed  Google Scholar 

  • Kletzin A, Adams MWW (1996) Tungsten in biological systems. FEMS Microbiol Rev 18:5–63

    Article  CAS  PubMed  Google Scholar 

  • Kohl M, Wiese S, Warscheid B (2011) Cytoscape: software for visualization and analysis of biological networks. Methods Mol Biol 696:291–303

    Article  CAS  PubMed  Google Scholar 

  • Kun-Tai L, Dong-Hong L, Ying-Ping Z, Yong-Hong W, Ju C, Si-Liang Z (2008) Influence of Zn2+, Co2+ and dimethylbenzimidazole on vitamin B12 biosynthesis by Pseudomonas denitrificans. World J Microbiol Biotechnol 24:2525–2530

    Article  Google Scholar 

  • Lavilla Lerma L, Benomar N, Valenzuela AS, Casado Muñoz Mdel C, Gálvez A, Abriouel H (2014) Role of EfrAB efflux pump in biocide tolerance and antibiotic resistance of Enterococcus faecalis and Enterococcus faecium isolated from traditional fermented foods and the effect of EDTA as EfrAB inhibitor. Food Microbiol 44:249–257

    Article  CAS  PubMed  Google Scholar 

  • Lenart J, Vimberg V, Vesela L, Janata J, Balikova Novotna G (2015) Detailed mutational analysis of Vga(A) interdomain linker: implication for antibiotic resistance specificity and mechanism. Antimicrob Agents Chemother 59:1360–1364

    Article  PubMed  PubMed Central  Google Scholar 

  • Lisher JP, Giedroc DP (2013) Manganese acquisition and homeostasis at the host-pathogen interface. Front Cell Infect Microbiol 3(24367765):91

    CAS  PubMed  PubMed Central  Google Scholar 

  • Locher KP (2016) Mechanistic diversity in ATP-binding cassette (ABC) transporters. Nat Struct Mol Biol 23:487–493

    Article  CAS  PubMed  Google Scholar 

  • Martin JE, Giedroc DP (2016) Functional determinants of metal ion transport and selectivity in paralogous cation diffusion facilitator transporters CzcD and MntE in Streptococcus pneumoniae. J Bacteriol 198(26787764):1066–1076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuo T, Chen J, Minato Y, Ogawa W, Mizushima T, Kuroda T, Tsuchiya T (2008) SmdAB, a heterodimeric ABC-type multidrug efflux Pump, in Serratia Marcescens. J Bacteriol 190(2):648–654

    Article  CAS  PubMed  Google Scholar 

  • McArthur AG, Waglechner N, Nizam F et al (2013) The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 57(7):3348–3357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer JF, Nies BA, Wiedemann BERND (1983) Amikacin resistance mediated by multi-resistance transposon Tn2424. J Bacteriol 155(2):755–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minamihata K, Goto M, Kamiya N (2012) Activation of Pyrococcus furiosus alkaline phosphatase by divalent metal ions. Biotechnol Lett 34(11):2055–2060

    Article  CAS  PubMed  Google Scholar 

  • Mota MJ, Lopes RP, Simões MMQ, Delgadillo I, Saraiva JA (2019) Effect of high pressure on Paracoccus denitrificans growth and Polyhydroxyalkanoates production from glycerol. Appl Biochem Biotechnol 188:810–823

    Article  CAS  PubMed  Google Scholar 

  • Moura A, Soares M, Pereira C, Leitão N, Henriques I, Correia A (2009) INTEGRALL: a database and search engine for integrons, integrases and gene cassettes. Bioinformatics 25(8):1096–1098

    Article  CAS  PubMed  Google Scholar 

  • Ning M, Hao W, Cao C et al (2020) Toxicity of deltamethrin to Eriocheir sinensis and the isolation of a deltamethrin-degrading bacterium, Paracoccus sp. P-2. Chemosphere 257:127162

  • Novotna G, Janata J (2006) A new evolutionary variant of the streptogramin A resistance protein, Vga(A)LC, from Staphylococcus haemolyticus with shifted substrate specificity towards lincosamides. Antimicrob Agents Chemother 50(12):4070–4076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Obayori OS, Ilori MO, Adebusoye SA, Amund OO, Oyetibo GO (2008) Microbial population changes in tropical agricultural soil experimentally contaminated with crude petroleum. Afr J Biotechnol 7:4512–4520

    CAS  Google Scholar 

  • Obayori OS, Salam LB, Anifowoshe WT, Odunewu ZM, Amosu OE, Ofulue BE (2015) Enhanced degradation of petroleum hydrocarbons in corn-steep-liquor-treated soil microcosm. Soil Sediment Contam 24(7):731–743

    Article  CAS  Google Scholar 

  • Partridge SR, Hall RM (2003) In34, a complex In5 family class 1 integron containing orf513 and dfrA10. Antimicrob Agents Chemother 47(1):342–349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pathan M, Keerthikumar S, Ang C-S et al (2015) FunRich: an open access standalone functional enrichment and interaction network analysis tool. Proteomics 15(15):2597–2601

    Article  CAS  PubMed  Google Scholar 

  • Pau RN, Lawson DM (2002) Transport, homeostasis, regulation, and binding of molybdate and tungstate to proteins. Metal Ions Biol Syst 39:31–74

    CAS  Google Scholar 

  • Pierce JR, Earhart CF (1986) Escherichia coli K-12 envelope proteins specifically required for ferrienterobactin uptake. J Bacteriol 166(3):930–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poole K (2005) Efflux-mediated antimicrobial resistance. J Antimicrob Chemother 56(1):20–51

    Article  CAS  PubMed  Google Scholar 

  • Puri A, Bajaj A, Singh Y, Lal R (2022) Harnessing taxonomically diverse and metabolically versatile genus Paracoccus for bioplastic synthesis and xenobiotic biodegradation. J Appl Microbiol 132:4208–4224

    Article  CAS  PubMed  Google Scholar 

  • Puri A, Bajaj A, Verma H, Kumar R, Singh Y (2020) Complete genome sequence of Paracoccus sp. strain AK26: insights into multipartite genome architecture and methylotropy. Genomics 112:2572–2582

    Article  CAS  PubMed  Google Scholar 

  • Raetz CRH, Reynolds CM, Trent MS, Bishop RE (2007) Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76:295–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rath H, Reder A, Hoffmann T, Hammer E, Seubert A, Bremer E, Völker U, Mäder U (2020) Management of osmoprotectant uptake hierarchy in Bacillus subtilis via a SigB-dependent antisense RNA. Front Microbiol 11:622

    Article  PubMed  PubMed Central  Google Scholar 

  • Rho M, Tang H, Ye Y (2010) FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acid Res 38:20–191

    Article  Google Scholar 

  • Rodionov DA, Hebbeln P, Gelfand MS, Eitinger T (2006) Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters. J Bacteriol 188(1):317–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ross K, Varani AM, Snesrud E et al (2021) TnCentral: a prokaryotic transposable element database and web portal for transposon analysis. MBio 12:e02060–21

  • Rudolph AS, Crowe JH, Crowe LM (1986) Effects of three stabilizing agents – proline, betaine. and trehalose – on membrane phospholipids. Arch Biochem Biophys 245:134–143

    Article  CAS  PubMed  Google Scholar 

  • Ruiz N, Gronenberg LS, Kahne D, Silhavy TJ (2008) Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 105:5537–5542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sahoo B, Ningthoujam R, Chaudhuri S (2018) Isolation and characterization of a lindane degrading bacteria Paracoccus sp. NITDBR1 and evaluation of its plant growth promoting traits. Int Microbiol 22:155–167

    Article  PubMed  Google Scholar 

  • Saier Jr MH, Reddy VS, Tamang DG, Västermark A (2014) The transporter classification database. Nucleic Acids Res 42(Database issue):D251-D258

  • Salam LB (2018) Detection of carbohydrate-active enzymes and genes in a spent engine oil-perturbed agricultural soil. Bull Natl Res Cent 42:10

    Article  Google Scholar 

  • Salam LB (2020) Unravelling the antibiotic and heavy metal resistome of a chronically polluted soil. 3 Biotech 10(6):1–23

  • Salam LB, Ishaq A (2019) Biostimulation potentials of corn steep liquor in enhanced hydrocarbon degradation in chronically polluted soil. 3 Biotech 9:46

  • Salam LB, Obayori OS, Ilori MO, Amund OO (2021) Impact of spent engine oil contamination on the antibiotic resistome of a tropical agricultural soil. Ecotoxicology 30:1251–1271

    Article  CAS  PubMed  Google Scholar 

  • Schwendener S, Donà V, Perreten V (2020) The novel macrolide resistance genes mef(D), msr(F), and msr(H) are present on resistance islands in Macrococcus canis, Macrococcus caseolyticus, and Staphylococcus aureus. Antimicrob Agents Chemother 64(5):e00160–e220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharkey LK, Edwards TA, O’Neill AJ (2016) ABC-F proteins mediate antibiotic resistance through ribosomal protection. Mbio 7:e01975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shea CM, McIntosh MA (1991) Nucleotide sequence and genetic organization of the ferric enterobactin transport system: homology to other periplasmic binding protein-dependent systems in Escherichia coli. Mol Microbiol 5(6):1415–1428

    Article  CAS  PubMed  Google Scholar 

  • Siche S, Neubauer O, Hebbeln P, Eitinger T (2010) A bipartite S unit of an ECF-type cobalt transporter. Res Microbiol 161(10):824–829

    Article  CAS  PubMed  Google Scholar 

  • Singh KV, Malathum K, Murray BE (2001) Disruption of an Enterococcus faecium species-specific gene, a homologue of acquired macrolide resistance genes of staphylococci, is associated with an increase in macrolide susceptibility. Antimicrob Agents Chemother 45(1):263–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sobota JM, Imlay JA (2011) Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc Natl Acad Sci USA 108(21402925):5402–5407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spanning RJM, Stouthamer AH, Baker SC, Verseveld HW (2015) Paracoccus. Bergey’s manual systematic archaea bacteriology. John Wiley & Sons Inc, Hoboken, NJ, pp 1–14

    Google Scholar 

  • Szklarczyk D, Gable AL, Nastou KC et al (2021) The STRING database in 2021: customizable protein–protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res 49:D605–D612

    Article  CAS  PubMed  Google Scholar 

  • Tansirichaiya S, Rahman MA, Roberts AP (2019) The Transposon Registry. Mobile. DNA 10:40

    Google Scholar 

  • Tatusov RL, Natale DA, Garkavtsev IV et al (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tessé S, Trueba F, Berthet N, Hot C, Chesneau O (2013) Resistance genes underlying the LSA phenotype of staphylococcal isolates from France. Antimicrob Agents Chemother 57(9):4543–4546

    Article  PubMed  PubMed Central  Google Scholar 

  • Tian J, Long X, Zhang S, Qin Q, Gan L, Tian Y (2018) Screening cyhalothrin degradation strains from locust epiphytic bacteria and studying Paracoccus acridae SCU-M53 cyhalothrin degradation process. Environ Sci Pollut Res 25:11505–11515

    Article  CAS  Google Scholar 

  • Tsuda M, Genka H (2001) Identification and characterization of Tn4656, a novel class II transposon carrying a set of toluene-degrading genes from TOL plasmid pWW53. J Bacteriol 183(21):6215–6224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Laere A (1989) Trehalose, reserve and/or stress metabolite. FEMS Microbiol Rev 63:201–210

    Article  Google Scholar 

  • Wang Y, Lv Y, Cai J et al (2015) A novel gene, optrA, that confers transferable resistance to oxazolidinones and phenicols and its presence in Enterococcus faecalis and Enterococcus faecium of human and animal origin. J Antimicrob Chemother 70(8):2182–2190

    Article  CAS  PubMed  Google Scholar 

  • Welsh DT (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 24(3):263–290

    Article  CAS  PubMed  Google Scholar 

  • Welsh DT, Herbert RA (1999) Osmotically induced intracellular trehalose, but not glycine betaine accumulation promotes desiccation tolerance in Escherichia coli. FEMS Microbiol Lett 174:57–63

    Article  CAS  PubMed  Google Scholar 

  • Wilson DN (2016) The ABC of ribosome-related antibiotic resistance. Mbio 7:e00598–e1516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson DN, Hauryliuk V, Atkinson GC, O’Neill AJ (2020) Target protection as a key antibiotic resistance mechanism. Nat Rev Microbiol 18(11):637–648

    Article  CAS  PubMed  Google Scholar 

  • Wong K, Ma J, Rothnie A, Biggin PC, Kerr ID (2014) Towards understanding promiscuity in multidrug efflux pumps. Trends Biochem Sci 39:8–16

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Fan R, Wang Y et al (2019) Analysis of combined resistance to oxazolidinones and phenicols among bacteria from dogs fed with raw meat/vegetables and the respective food items. Sci Rep 9:15500

    Article  PubMed  PubMed Central  Google Scholar 

  • Zamble D (2017) Introduction to the biological chemistry of nickel. RSC Metallobiology 2017:1–11

    Google Scholar 

  • Zawadzka AM, Kim Y, Maltseva N, Nichiporuk R, Fan Y, Joachimiak A, Raymond KN (2009) Characterization of a Bacillus subtilis transporter for petrobactin, an anthrax stealth siderophore. Proc Natl Acad Sci U S A 106(51):21854–21859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Biological Sciences, Microbiology Unit, Elizade University, Ilara-Mokin, Ondo State, Nigeria

    Lateef Babatunde Salam

  2. Department of Microbiology, Lagos State University, Ojo, Lagos, Nigeria

    Oluwafemi Sunday Obayori

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LBS conceived the study, performed the experiments, and wrote the manuscript. OSO coordinated the study and contributed to the “Introduction” and “Discussion” sections of the manuscript. All the authors reviewed and approved the final version of the manuscript.

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Salam, L.B., Obayori, O.S. Functional characterization of the ABC transporters and transposable elements of an uncultured Paracoccus sp. recovered from a hydrocarbon-polluted soil metagenome. Folia Microbiol 68, 299–314 (2023). https://doi.org/10.1007/s12223-022-01012-0

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